Scyllarid Lobster Biology and Ecology

*Kari L. Lavalli, Ehud Spanier and Jason S. Goldstein*

#### **Abstract**

The family Scyllaridae is the most speciose and diverse of all families of marine lobsters. Slipper lobsters are found in both tropical and temperate habitats with hard or soft substrates and at different depths, and exhibit a wide array of morphological, anatomical, and physiological adaptations. Among the 20 genera and at least 89 species constituting 4 subfamilies, only some members of 4 genera, *Thenus* (Theninae), *Scyllarides* (Arctidinae), *Ibacus* and *Parribacus* (Ibacinae), form significant fisheries because of their large size. While scientific information on these lobsters has increased considerably in recent decades, it is still limited compared with commercially valuable spiny and clawed lobsters, and is confined to a few key species. The present chapter presents the current available knowledge on the biology of scyllarids and attempts to point out where questions remain to help focus further studies in this important group.

**Keywords:** slipper lobsters, Scyllaridae, taxonomy, genetics, anatomy, physiology, ecology, life history, behavior, fisheries

#### **1. Introduction**

Slipper lobsters, family Scyllaridae (Latreille, 1825) have been known and described since the late 1700s and are considered part of the superfamily Palinuroidea that consists of spiny lobsters (Palinuridae), furry lobsters (Synaxidae), blind claw-footed lobsters (Polychelidae), and slipper or shovel-nosed or bulldozer lobsters (Scyllaridae) [1, 2]. The Scyllaridae are organized into four subfamilies (Ibacinae, Arctidiane, Scyllarinae, and Theninae) and comprise 20 genera with at least 89 extant species thus far recognized [3–6].

Only four genera—*Scyllarides* (Arctidinae), *Ibacus* and *Parribacus* (Ibacinae), and *Thenus* (Theninae)—form any kind of significant fishery because these individual species tend to be large in size [7]. Of these four genera, *Scyllarides* (Gill, 1898) has been studied extensively due to their large adult size, which makes them economically important; their worldwide geographical distribution in tropical and subtropical habitats; and their numerous species (14) [1]. Considerable knowledge is also available for species within the genus *Thenus* because of some relevance in certain fisheries as well as the success in rearing these animals in aquaculture [8]. Research on other species generally arises with overfishing of and a shift away from sister species (generally palinurids) and thus always lags behind exploitation, which is problematic for the creation of sustainable fisheries. Although small in size, lobsters of the genus *Scyllarus* often become a minor target for fisheries (e.g., [9, 10]).

**24**

*Crustacea*

1874;**2**:29-324

**References**

[1] Hume AO. Contributions to the ornithology of India: The islands of the Bay of Bengal. Stray Feathers.

[2] Daniel A, Premkumar VK. The coconut crab in the Great Nicobar Island. Journal of the Bombay Natural History Society. 1968;**64**:574-580

[3] Alcock A. Catalogue of the Indian Decapod Crustacea in the Collection of the Indian Museum. Kolkata, India: Zoological Survey of India; 1905

[4] Reese BS, Kinzie RA. The larval development of the coconut or robber crab *Birgus latro* (L.) in the laboratory (Anomura, Paguridae). Crustaceana

[5] Eldredge LG. *Birgus latro*. In: IUCN Red List of Threatened Species v. 2010.4. 1996. Available from: http://www. iucnredlist.org [Accessed: April 19,

[6] Patankar V, D'souza E. Conservation needs of the coconut crab *Birgus latro* on the Nicobar Islands, India. Oryx. 2012;**46**(2):175-178. DOI: 10.1017/

Supplement. 1968;**2**:117-144

S0030605311000408

2011]

The present review is an attempt to summarize the somewhat patchy information available in the scientific literature on scyllarids. In addition, expanding our knowledge on slipper lobsters may prove beneficial to humans in ways beyond providing a food source, given that large proteins recently isolated from *Ibacus novemdentatus* have displayed cytotoxic activity against human cancer cells [11].

#### **2. Taxonomy, phylogeny and evolution**

Lobsters were significantly more diverse in the Mesozoic, especially during the Triassic and Jurassic, than in the Cenozoic and Holocene. The Achelata appeared 391–351 million years ago (MYA), but did not diverge into the palinurid and scyllarid lineages until the Permian (−250 MYA) [12, 13]. Fossil remains of scyllarids date back to the mid-Cretaceous (100–120 MYA) [3], but are not well-represented since their fossils come mostly from low energy (shale, clay, ironstone) or lithographic (limestone) deposits [14–16]. Today's scyllarids live in different habitats (coral and sponge reefs, and medium to high energy environments) from fossil forms, but the sparse fossil record of this group makes it difficult to speculate on when their habitat shift occurred, although their major radiation began in the Late Jurassic and continued through the Holocene [14].

Slipper lobsters are closely related to the Palinuridae and Synaxidae, all of which comprise the Achelata; they share numerous characters, most notably their unique larval phase (i.e., phyllosoma) which separate the Achelata from all other Decapoda [3]. The plate-like antennal flagellum of slipper lobsters is a highly derived feature that is common to all 89 species and distinguishes them from the palinurids and synaxids which possess whip-like antennae. The Scyllaridae underwent considerable taxonomic revision from 1991 to 2002, mostly within the Scyllarinae, and now consist of 20 genera. The highest taxonomic diversity is among the smaller species [1, 17].

The subfamily Arctidinae consists of 2 genera and 17 species. These are some of the larger scyllarids. *Arctides* and *Scyllarides* species typically have a highly vaulted carapace, a three-segmented mandibular palp, and a shallow cervical incision along the lateral margin of the carapace. The subfamily Ibacinae consists of 3 genera, *Evibacus, Ibacus* and *Parribacus*, with a total of 15 species. In these species, the carapace is significantly dorso-ventrally compressed with a deep cervical incision along the lateral margin of the carapace. The mandibular palp is simple or twosegmented, in contrast to the Arctidinae. One genus, *Thenus*, and five species are recognized presently in the subfamily Theninae [5]. The Theninae display extremes: the body is highly flattened and their eye orbits are found at the extreme anterolateral extent of the carapace. In contrast, the 52 species of Scyllarinae found within 14 genera all have vaulted carapaces covered with tubercles and their eyes are more medial in placement. Yet both Theninae and Scyllarinae lack a flagellum on the exopod of the first and third maxillipeds [18]. See **Figure 1** for representatives of these species and **Figure 2** for examples of scyllarid mouthparts.

The taxonomy of Scyllaridae is based mainly on the morphology of the adults and to lesser extent of that of their pelagic larvae, the phylosomas. Recently molecular genetic tools have been used to assess taxonomic and phylogenetic issues, and the main clades found within Scyllaridae are in agreement [13] with current taxonomy based on adult morphology [1, 19, 20] and recent molecular studies [5]. All subfamilies (Arctidinae, Theninae and Scyllarinae) are now considered monophyletic, except for the Ibacinae [5]; this contrasts with a more recent analysis [21] that concluded that the Scyllaridae are fully monophyletic. The Arctidinae appears to represent the earliest branching lineage during the evolution of this group [5], which corresponds to the fossil record. In addition, slipper lobsters have likely evolved from shallow (onshore)

**27**

**3. Life history**

**Figure 2.**

**Figure 1.**

*Philadelphia, 1852.*

to deep water (offshore) species [5]. These same molecular tools suggest that two Atlantic species, *Scyllarus depressus* and *S. subarctus*, are a strongly supported clade with low genetic differentiation, indicative of a recent split into sister taxa [22].

*Scyllarid mouthparts. (1) Aboral/ventral view of third maxilliped; (2) aboral/ventral view of second maxilliped; (3) aboral/ventral view of first maxilliped; (4) aboral/ventral view of second maxilla; (5) aboral/ventral view of first maxilla; (6) mouth; (7) aboral/ventral view of mandible; (8) oral/dorsal view of third maxilliped; (9) oral/dorsal view of first maxilliped; (10) oral/dorsal view of mandible. From Savigny, J-Cés. Iconographie des Crustacés et des Arachnides de l'Égypte. De l'Imprimerie Royale, Paris, France; 1805.*

*Different forms of scyllarid lobsters. (A) Scyllarus arctus; (B) Thenus orientalis; (C) Parribacus antarcticus. A and B from Cuvier G. Le Règne animal: D'Après son organization, pour Sevir de base a L'Histoire Naturelle des Animaux, et D'Introduction a L'Anatomie Comparèe. Accompagnée de planches Gravées. Imprime chez Paul Renouard, Paris, France, 1837; C from Dana JD. United States exploring expedition during the years 1838, 1839, 1840, 1841, 1842 under the command of Charles Wilkes, U.S.N., Vol. XIII. Crustacea. C. Sherman,* 

The life history of scyllarids parallels that of palinurids and can be divided into a series of developmental phases. These lobsters typically begin their pelagic lives

*Scyllarid Lobster Biology and Ecology*

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

#### **Figure 1.**

*Crustacea*

**2. Taxonomy, phylogeny and evolution**

continued through the Holocene [14].

The present review is an attempt to summarize the somewhat patchy information available in the scientific literature on scyllarids. In addition, expanding our knowledge on slipper lobsters may prove beneficial to humans in ways beyond providing a food source, given that large proteins recently isolated from *Ibacus novemdentatus* have displayed cytotoxic activity against human cancer cells [11].

Lobsters were significantly more diverse in the Mesozoic, especially during the Triassic and Jurassic, than in the Cenozoic and Holocene. The Achelata appeared 391–351 million years ago (MYA), but did not diverge into the palinurid and scyllarid lineages until the Permian (−250 MYA) [12, 13]. Fossil remains of scyllarids date back to the mid-Cretaceous (100–120 MYA) [3], but are not well-represented since their fossils come mostly from low energy (shale, clay, ironstone) or lithographic (limestone) deposits [14–16]. Today's scyllarids live in different habitats (coral and sponge reefs, and medium to high energy environments) from fossil forms, but the sparse fossil record of this group makes it difficult to speculate on when their habitat shift occurred, although their major radiation began in the Late Jurassic and

Slipper lobsters are closely related to the Palinuridae and Synaxidae, all of which comprise the Achelata; they share numerous characters, most notably their unique larval phase (i.e., phyllosoma) which separate the Achelata from all other Decapoda [3]. The plate-like antennal flagellum of slipper lobsters is a highly derived feature that is common to all 89 species and distinguishes them from the palinurids and synaxids which possess whip-like antennae. The Scyllaridae underwent considerable taxonomic revision from 1991 to 2002, mostly within the Scyllarinae, and now consist of 20 genera. The highest taxonomic diversity is among the smaller species [1, 17]. The subfamily Arctidinae consists of 2 genera and 17 species. These are some of the larger scyllarids. *Arctides* and *Scyllarides* species typically have a highly vaulted carapace, a three-segmented mandibular palp, and a shallow cervical incision along the lateral margin of the carapace. The subfamily Ibacinae consists of 3 genera, *Evibacus, Ibacus* and *Parribacus*, with a total of 15 species. In these species, the carapace is significantly dorso-ventrally compressed with a deep cervical incision along the lateral margin of the carapace. The mandibular palp is simple or twosegmented, in contrast to the Arctidinae. One genus, *Thenus*, and five species are recognized presently in the subfamily Theninae [5]. The Theninae display extremes: the body is highly flattened and their eye orbits are found at the extreme anterolateral extent of the carapace. In contrast, the 52 species of Scyllarinae found within 14 genera all have vaulted carapaces covered with tubercles and their eyes are more medial in placement. Yet both Theninae and Scyllarinae lack a flagellum on the exopod of the first and third maxillipeds [18]. See **Figure 1** for representatives of

these species and **Figure 2** for examples of scyllarid mouthparts.

The taxonomy of Scyllaridae is based mainly on the morphology of the adults and to lesser extent of that of their pelagic larvae, the phylosomas. Recently molecular genetic tools have been used to assess taxonomic and phylogenetic issues, and the main clades found within Scyllaridae are in agreement [13] with current taxonomy based on adult morphology [1, 19, 20] and recent molecular studies [5]. All subfamilies (Arctidinae, Theninae and Scyllarinae) are now considered monophyletic, except for the Ibacinae [5]; this contrasts with a more recent analysis [21] that concluded that the Scyllaridae are fully monophyletic. The Arctidinae appears to represent the earliest branching lineage during the evolution of this group [5], which corresponds to the fossil record. In addition, slipper lobsters have likely evolved from shallow (onshore)

**26**

*Different forms of scyllarid lobsters. (A) Scyllarus arctus; (B) Thenus orientalis; (C) Parribacus antarcticus. A and B from Cuvier G. Le Règne animal: D'Après son organization, pour Sevir de base a L'Histoire Naturelle des Animaux, et D'Introduction a L'Anatomie Comparèe. Accompagnée de planches Gravées. Imprime chez Paul Renouard, Paris, France, 1837; C from Dana JD. United States exploring expedition during the years 1838, 1839, 1840, 1841, 1842 under the command of Charles Wilkes, U.S.N., Vol. XIII. Crustacea. C. Sherman, Philadelphia, 1852.*

#### **Figure 2.**

*Scyllarid mouthparts. (1) Aboral/ventral view of third maxilliped; (2) aboral/ventral view of second maxilliped; (3) aboral/ventral view of first maxilliped; (4) aboral/ventral view of second maxilla; (5) aboral/ventral view of first maxilla; (6) mouth; (7) aboral/ventral view of mandible; (8) oral/dorsal view of third maxilliped; (9) oral/dorsal view of first maxilliped; (10) oral/dorsal view of mandible. From Savigny, J-Cés. Iconographie des Crustacés et des Arachnides de l'Égypte. De l'Imprimerie Royale, Paris, France; 1805.*

to deep water (offshore) species [5]. These same molecular tools suggest that two Atlantic species, *Scyllarus depressus* and *S. subarctus*, are a strongly supported clade with low genetic differentiation, indicative of a recent split into sister taxa [22].

#### **3. Life history**

The life history of scyllarids parallels that of palinurids and can be divided into a series of developmental phases. These lobsters typically begin their pelagic lives

as phyllosoma larvae (**Figure 3**), although some scyllarids (*Scyllarides aequinoctialis* [23, 24], *S. herklotsi* [25], *S. latus* [26], *Ibacus alticrenatus* [27] and *I. ciliates* [28] or *I. novemdentatus* [19]) hatch as a naupliosoma (pre-larva), a short-lived form lasting a few hours that bears only the first three pairs of cephalic appendages [29]. Abdominal appendages are typically absent or rudimentary in early phyllosomas, but appear in later stages [30]. Exopodites are found on all thoracic appendages of phyllosoma larvae until their metamorphic molt when they are lost from all but the first and second maxillipeds; here exopodites are retained and used for generating currents around the mouth region [31]. Scyllarid phyllosomas deviate from other decapod larvae in that they are missing a fully developed exopod on the third maxilliped and this may indicate a phylogenetic separation of feeding strategy [3].

The dispersal of phyllosomas varies among species and depends largely on whether the parental stock is found within lagoons formed by coral island barrier reefs or in deeper waters [32–36]. Those hatched in coastal lagoons tend to remain there, while those hatched in deeper water gradually move shoreward, such that final-stage phyllosomas are found much closer to shore [30]. Some phyllosomas undertake diel vertical migrations, but data are limited as to the extent of these migrations and the species-specific preferences for various depths [30, 37] as well as the efficacy of their swimming behavior. It is likely that smaller instars vertically migrate less than later, larger instars [35] and may use passive transport by occupying vertical strata that move them in specific directions [30]. Some phyllosomas even travel attached to the aboral surface of jellyfish medusae or siphonophores [38–41], which may affect larval dispersal or allow them to remain relatively near shore [29, 30]. Understanding of phyllosoma behavior and dispersion has been challenged by the ability to correctly identify species; however, recent use of molecular genetics and DNA barcoding is improving the ability to make species identification possible in the field [42, 43]*.*

#### **Figure 3.**

*Various stages of scyllarid phyllosoma larvae. Top, early stages of Scyllarides astori and Evibacus princeps. Bottom, later stages of S. astori, E. princeps, and Scyllarus martensii. From the Martin Wiggo Johnson Phyllosoma slide collection of the Scripps Institute of Oceanography Pelagic Invertebrate Collection website (https://scripps.ucsd.edu/collections/pi/overview/collection-databases-zooplankton-guide/m-wjohnson-lobster-phyllosoma-slide).*

**29**

benthic realm.

*Scyllarid Lobster Biology and Ecology*

growth on their bodies [54].

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

Phyllosomas are raptorial feeders, using their pereiopods to grasp onto food items, which are then shredded by the maxillipeds and masticated by molar processes of the mandibles [44]. Mostly fleshy foods are ingested; such food types are more readily available in coastal waters than in offshore, oligotrophic waters [29, 30, 45]. Some scyllarid phyllosomas have been observed clinging onto or "riding" the medusa stage of some gelatinous zooplankton. For example, a recent report of a videotaped scyllarid lobster phyllosoma swimming while dragging a prayid siphonophore behind it suggests that gelatinous forms may serve as a critical food and/ or defense against predation (by ingestion of the nematocysts) and refutes the idea that hitching a ride on these organisms is energy-saving due to passive transportation [41]. Recently, molecular methods using the central domain of the 18SrDNA gene have identified food items of some species of scyllarid and palinurid phyllosomas and suggest that these forms feed on appendicularians, salps, and cnidarians [46]. Ctenophores fed to phyllosomas of *Thenus orientalis* are accepted readily and provide nutritional support [47] and similar results were obtained with the phyllosomas of *T. australiensis*, *Ibacus novemdentatus*, *I. ciliatus* fed on jellyfish [48–51]. Some species of wild phyllosomas were found to contain cnidarian tissue in their hepatopancreas and feces, and these phyllosomas seem capable of encapsulating nematocysts [52] suggesting that these larvae utilize jellyfish as a food source. Few studies have examined exactly how phyllosomas consume jellyfish, but one possible mechanism is for phyllosomas to cling onto the exumbrella, feed on tentacles or oral arms first, and then consume the exumbrella [48, 53]. Phyllosomas riding on jellyfish manage to groom and clear mucus extruded by jellyfish to dampen microbial

The final-stage phyllosoma molts into the highly specialized nisto (see **Figure 4**), or post-larval stage, which, like their spiny lobster (pueruli) and clawed lobster (post-larvae) counterparts, utilize surface waters to swim toward benthic habitats to settle. Nistos are neither completely planktonic nor completely benthic—they are caught in plankton tows demonstrating that they are pelagic at least part of the time [29]. In many species of scyllarids, the nisto appears to bury into soft substrates during the day and swim actively at night; some species even change coloration daily between these two habitats to remain cryptically colored in both environments [29]. Some scyllarid nistos are excellent swimmers (using their abdominal pleopods), while others are poor swimmers; some are also capable of executing tail flips (backward swimming) as a means of escape [55]. These swimming differences may exist due to marked differences in the size of pleopods among different species [56]. However, this suggestion has not been adequately tested. As with spiny lobster pueruli, the nisto appears to rely on energy reserves, rather than to actively feed [30], although the structure of the proventriculus is transitional between the phyllosoma and the juvenile [57] which suggests that it can process and sort food particles at this stage of development. The nisto also bears a cardio-pyloric valve that divides the anterior and posterior cardiac chambers, but lacks a gastric mill. Thus, if food is consumed by the nisto, it is likely soft and processed mainly by the mouthparts prior to ingestion [57]. Nistos appear similar in form to juveniles and bear the derived feature of flattened antennae, but are transparent instead of being reddish-brown. Their abdominal pleopods still bear swimming (natatory) setae [58] to aid in transitioning them from the pelagic to the

Juvenile life history of scyllarids is lacking for all species except those that have

been successfully reared in culture (e.g., *Thenus* species [59] or *Ibacus* species [49, 60, 61]). This primarily is the result of a problem in sampling and not knowing where juvenile grounds lay. For example, in *S. latus* no live juvenile or nisto of the

#### *Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

possible in the field [42, 43]*.*

as phyllosoma larvae (**Figure 3**), although some scyllarids (*Scyllarides aequinoctialis* [23, 24], *S. herklotsi* [25], *S. latus* [26], *Ibacus alticrenatus* [27] and *I. ciliates* [28] or *I. novemdentatus* [19]) hatch as a naupliosoma (pre-larva), a short-lived form lasting a few hours that bears only the first three pairs of cephalic appendages [29]. Abdominal appendages are typically absent or rudimentary in early phyllosomas, but appear in later stages [30]. Exopodites are found on all thoracic appendages of phyllosoma larvae until their metamorphic molt when they are lost from all but the first and second maxillipeds; here exopodites are retained and used for generating currents around the mouth region [31]. Scyllarid phyllosomas deviate from other decapod larvae in that they are missing a fully developed exopod on the third maxil-

liped and this may indicate a phylogenetic separation of feeding strategy [3]. The dispersal of phyllosomas varies among species and depends largely on whether the parental stock is found within lagoons formed by coral island barrier reefs or in deeper waters [32–36]. Those hatched in coastal lagoons tend to remain there, while those hatched in deeper water gradually move shoreward, such that final-stage phyllosomas are found much closer to shore [30]. Some phyllosomas undertake diel vertical migrations, but data are limited as to the extent of these migrations and the species-specific preferences for various depths [30, 37] as well as the efficacy of their swimming behavior. It is likely that smaller instars vertically migrate less than later, larger instars [35] and may use passive transport by occupying vertical strata that move them in specific directions [30]. Some phyllosomas even travel attached to the aboral surface of jellyfish medusae or siphonophores [38–41], which may affect larval dispersal or allow them to remain relatively near shore [29, 30]. Understanding of phyllosoma behavior and dispersion has been challenged by the ability to correctly identify species; however, recent use of molecular genetics and DNA barcoding is improving the ability to make species identification

*Various stages of scyllarid phyllosoma larvae. Top, early stages of Scyllarides astori and Evibacus princeps. Bottom, later stages of S. astori, E. princeps, and Scyllarus martensii. From the Martin Wiggo Johnson Phyllosoma slide collection of the Scripps Institute of Oceanography Pelagic Invertebrate Collection website (https://scripps.ucsd.edu/collections/pi/overview/collection-databases-zooplankton-guide/m-w-*

**28**

**Figure 3.**

*johnson-lobster-phyllosoma-slide).*

Phyllosomas are raptorial feeders, using their pereiopods to grasp onto food items, which are then shredded by the maxillipeds and masticated by molar processes of the mandibles [44]. Mostly fleshy foods are ingested; such food types are more readily available in coastal waters than in offshore, oligotrophic waters [29, 30, 45]. Some scyllarid phyllosomas have been observed clinging onto or "riding" the medusa stage of some gelatinous zooplankton. For example, a recent report of a videotaped scyllarid lobster phyllosoma swimming while dragging a prayid siphonophore behind it suggests that gelatinous forms may serve as a critical food and/ or defense against predation (by ingestion of the nematocysts) and refutes the idea that hitching a ride on these organisms is energy-saving due to passive transportation [41]. Recently, molecular methods using the central domain of the 18SrDNA gene have identified food items of some species of scyllarid and palinurid phyllosomas and suggest that these forms feed on appendicularians, salps, and cnidarians [46]. Ctenophores fed to phyllosomas of *Thenus orientalis* are accepted readily and provide nutritional support [47] and similar results were obtained with the phyllosomas of *T. australiensis*, *Ibacus novemdentatus*, *I. ciliatus* fed on jellyfish [48–51]. Some species of wild phyllosomas were found to contain cnidarian tissue in their hepatopancreas and feces, and these phyllosomas seem capable of encapsulating nematocysts [52] suggesting that these larvae utilize jellyfish as a food source. Few studies have examined exactly how phyllosomas consume jellyfish, but one possible mechanism is for phyllosomas to cling onto the exumbrella, feed on tentacles or oral arms first, and then consume the exumbrella [48, 53]. Phyllosomas riding on jellyfish manage to groom and clear mucus extruded by jellyfish to dampen microbial growth on their bodies [54].

The final-stage phyllosoma molts into the highly specialized nisto (see **Figure 4**), or post-larval stage, which, like their spiny lobster (pueruli) and clawed lobster (post-larvae) counterparts, utilize surface waters to swim toward benthic habitats to settle. Nistos are neither completely planktonic nor completely benthic—they are caught in plankton tows demonstrating that they are pelagic at least part of the time [29]. In many species of scyllarids, the nisto appears to bury into soft substrates during the day and swim actively at night; some species even change coloration daily between these two habitats to remain cryptically colored in both environments [29]. Some scyllarid nistos are excellent swimmers (using their abdominal pleopods), while others are poor swimmers; some are also capable of executing tail flips (backward swimming) as a means of escape [55]. These swimming differences may exist due to marked differences in the size of pleopods among different species [56]. However, this suggestion has not been adequately tested.

As with spiny lobster pueruli, the nisto appears to rely on energy reserves, rather than to actively feed [30], although the structure of the proventriculus is transitional between the phyllosoma and the juvenile [57] which suggests that it can process and sort food particles at this stage of development. The nisto also bears a cardio-pyloric valve that divides the anterior and posterior cardiac chambers, but lacks a gastric mill. Thus, if food is consumed by the nisto, it is likely soft and processed mainly by the mouthparts prior to ingestion [57]. Nistos appear similar in form to juveniles and bear the derived feature of flattened antennae, but are transparent instead of being reddish-brown. Their abdominal pleopods still bear swimming (natatory) setae [58] to aid in transitioning them from the pelagic to the benthic realm.

Juvenile life history of scyllarids is lacking for all species except those that have been successfully reared in culture (e.g., *Thenus* species [59] or *Ibacus* species [49, 60, 61]). This primarily is the result of a problem in sampling and not knowing where juvenile grounds lay. For example, in *S. latus* no live juvenile or nisto of the

**Figure 4.**

*Nisto of Scyllarus americanus (Top). From Ref. [23]. Open access: https://archive.org/details/ larvaldevelopmen00robe. Nisto of unidentified scyllarid species in Florida waters (Bottom). Photo by Casey Butler.*

commercially exploited Mediterranean slipper lobster, *Scyllarides latus* (Latreille, 1851), had ever been sampled despite ample information available on the ecology and behavior of adults of this species [62]. Museum surveys of invertebrate collections provided a small specimen of *S. latus* (36 mm carapace length (CL)) collected in 1987 with a 20 mm mesh scientific trawl net at depth of 450–700 m on a soft and muddy bottom at least 40 km offshore of Livorno [63]. Another specimen, even smaller (11.7 mm CL), was collected in Reggio Calabria, southern Italy, in the early 1900s at a depth of >850 m and deposited in the Zoological Museum of Turin. This early scyllarid juvenile, likely a recent benthic recruit, suggests that the larvae drift large distances before settling as nistos in deeper waters with muddy habitats where they are possibly protected against the more numerous inshore predators. They then migrate as larger juveniles or sub-adults to inshore habitats [63]. Similar suggestions have been made for other scyllarids. A recent study [64] found *Scyllarus* sp. in the guts of deep sea fish which suggests that nistos are settling in deep waters. *Ibacus* juveniles appear to migrate shoreward from offshore waters to recruit into adult grounds [61]. Juveniles appear to occupy a different spatial niche from adults and are far more cryptic than adults because few individuals are found that are smaller than 20 cm TL [65, 66]. To obtain sufficient numbers of small individuals, specific sampling techniques must be developed which target the juveniles, which may prove difficult if many of the species have juvenile development in deep, oceanic waters. The exceptional discovery of a juvenile form of scyllarid in the old museum collection of Turin [63] emphasizes the importance of comprehensive surveys of crustacean collections, even old ones, in search for scyllarid life stages.

**31**

*Scyllarid Lobster Biology and Ecology*

of rapid growth.

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

Gaps in life-history make growth rate determination difficult in most species, except for those that can be cultured with high survival rates or from grow-out studies when sufficient juveniles have been captured. Juveniles of reared *S. nodifer* take ~18 months and 9–10 molts to reach adult size [67]. Other fast growing species include *Ibacus* spp. that reach sexual maturity after four to six molts [68]. Cultured *Thenus orientalis* take about 400 days (19 molts) to grow to a size of *c.* 250 g. [69]. In contrast, 7–8 years are necessary for juvenile *S. astori* to recruit fully into the adult population [65]. Hence, from what little data we have on juvenile life history, it appears that many, but not all, of the commercially important scyllarids are capable

Arctidinid adults (e.g. *Scyllarides* spp.) are typically large and tag–release studies suggest that adults molt annually (*S. latus*, [70]), although data from *S. astori* populations suggest that molts occur every 18–24 months [65, 66]. Molting typically occurs at night and in cooler to warmer months [71–73]. Softening of the old exoskeleton starts some 10–22 days pre-molt, with hardening being complete 3 weeks post-molt. The entire process takes approximately 7 hours, with lobsters remaining shelter-bound for 5–9 days post-molt [74]. Slipper lobsters do not appear to consume their exuviae since these are generally left outside of shelters [72]. Sex ratios are close to unity in those species that have been adequately sampled (*S. latus*, [26, 72]; *S. astori*, [65]). In some species, mean CL is larger for females than for males (*S. latus*, [26, 74]), while in others, males exceed females in size (*S. astori*, [66]). Shortly after mating, females extrude a large number of eggs (conservative numbers range from 24,710 to 356,000), based on TL of the individual, with those eggs ranging from 0.6 to 0.7 mm diameter [26, 66, 75–77]. In some species, spawning occurs twice a year [76]. Such high fecundity rates may be an adaptation to oceanic loss of larvae and variable recruitment of nistos due to cyclic changes in oceanic climate [29]. Eggs are brooded for 2–8 weeks before release over a number of days (*S. latus*, [74, 78]). Ovigerous females are more commonly sampled in cooler months, but not warmer months [66]. There is some evidence that females may return to inshore reefs in the autumn earlier than males and leave sooner after shedding eggs in the mid-summer, possibly to maximize thermal regimes for developing embryos [79]. Most species appear to move to colder, deeper waters when inshore water temperatures rise steeply in the summer or, for those species that remain in

lagoons, stay at locations where thermal regimes are less than 25°C [65].

15 years with a maximum size reached after 5–8 years [80].

evidence of reproductive activity during summer (July) [81].

*Ibacus* sp. adults rarely exceed 20 cm TL [1] and are thus smaller than the adults of subfamily Arctidinidae*.* Sex ratios of all four Australian commercially caught species of *Ibacus* are approximately 1:1. Males are smaller than females because they molt less frequently after attaining sexual maturity. Mating occurs when the female is hard-shelled. Fecundity is much lower than in members of the subfamily Arctidinidae and it is highly variable both within and among the four species of *Ibacus*. It increases with the size of the animal [68]. Egg incubation times have been estimated to vary between approximately 2–4 months and are likely to be temperature dependent with longer incubation in cooler water [61]. Molt frequencies of captive lobsters suggest seasonal molting but wild, tagged lobsters were caught repetitively in consecutive years without having increased in size [68]. Growth models for *I. peronii*, suggest the potential for this species to live for more than

Very little information is available on adults of *Parribacus* spp. and what does exist is mainly focused on *P. antarcticus*. Two captured females of this species bore

In *Thenus* spp. growth is quite rapid with 80% of maximum size reached by 2 years of age. Females appear to attain larger sizes than males as evidenced by fishery sampled size ranges in both Indian and Australian waters [82]. Increased

#### *Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

**Figure 4.**

*Butler.*

**30**

commercially exploited Mediterranean slipper lobster, *Scyllarides latus* (Latreille, 1851), had ever been sampled despite ample information available on the ecology and behavior of adults of this species [62]. Museum surveys of invertebrate collections provided a small specimen of *S. latus* (36 mm carapace length (CL)) collected in 1987 with a 20 mm mesh scientific trawl net at depth of 450–700 m on a soft and muddy bottom at least 40 km offshore of Livorno [63]. Another specimen, even smaller (11.7 mm CL), was collected in Reggio Calabria, southern Italy, in the early 1900s at a depth of >850 m and deposited in the Zoological Museum of Turin. This early scyllarid juvenile, likely a recent benthic recruit, suggests that the larvae drift large distances before settling as nistos in deeper waters with muddy habitats where they are possibly protected against the more numerous inshore predators. They then migrate as larger juveniles or sub-adults to inshore habitats [63]. Similar suggestions have been made for other scyllarids. A recent study [64] found *Scyllarus* sp. in the guts of deep sea fish which suggests that nistos are settling in deep waters. *Ibacus* juveniles appear to migrate shoreward from offshore waters to recruit into adult grounds [61]. Juveniles appear to occupy a different spatial niche from adults and are far more cryptic than adults because few individuals are found that are smaller than 20 cm TL [65, 66]. To obtain sufficient numbers of small individuals, specific sampling techniques must be developed which target the juveniles, which may prove difficult if many of the species have juvenile development in deep, oceanic waters. The exceptional discovery of a juvenile form of scyllarid in the old museum collection of Turin [63] emphasizes the importance of comprehensive surveys of

*larvaldevelopmen00robe. Nisto of unidentified scyllarid species in Florida waters (Bottom). Photo by Casey* 

*Nisto of Scyllarus americanus (Top). From Ref. [23]. Open access: https://archive.org/details/*

crustacean collections, even old ones, in search for scyllarid life stages.

Gaps in life-history make growth rate determination difficult in most species, except for those that can be cultured with high survival rates or from grow-out studies when sufficient juveniles have been captured. Juveniles of reared *S. nodifer* take ~18 months and 9–10 molts to reach adult size [67]. Other fast growing species include *Ibacus* spp. that reach sexual maturity after four to six molts [68]. Cultured *Thenus orientalis* take about 400 days (19 molts) to grow to a size of *c.* 250 g. [69]. In contrast, 7–8 years are necessary for juvenile *S. astori* to recruit fully into the adult population [65]. Hence, from what little data we have on juvenile life history, it appears that many, but not all, of the commercially important scyllarids are capable of rapid growth.

Arctidinid adults (e.g. *Scyllarides* spp.) are typically large and tag–release studies suggest that adults molt annually (*S. latus*, [70]), although data from *S. astori* populations suggest that molts occur every 18–24 months [65, 66]. Molting typically occurs at night and in cooler to warmer months [71–73]. Softening of the old exoskeleton starts some 10–22 days pre-molt, with hardening being complete 3 weeks post-molt. The entire process takes approximately 7 hours, with lobsters remaining shelter-bound for 5–9 days post-molt [74]. Slipper lobsters do not appear to consume their exuviae since these are generally left outside of shelters [72]. Sex ratios are close to unity in those species that have been adequately sampled (*S. latus*, [26, 72]; *S. astori*, [65]). In some species, mean CL is larger for females than for males (*S. latus*, [26, 74]), while in others, males exceed females in size (*S. astori*, [66]). Shortly after mating, females extrude a large number of eggs (conservative numbers range from 24,710 to 356,000), based on TL of the individual, with those eggs ranging from 0.6 to 0.7 mm diameter [26, 66, 75–77]. In some species, spawning occurs twice a year [76]. Such high fecundity rates may be an adaptation to oceanic loss of larvae and variable recruitment of nistos due to cyclic changes in oceanic climate [29]. Eggs are brooded for 2–8 weeks before release over a number of days (*S. latus*, [74, 78]). Ovigerous females are more commonly sampled in cooler months, but not warmer months [66]. There is some evidence that females may return to inshore reefs in the autumn earlier than males and leave sooner after shedding eggs in the mid-summer, possibly to maximize thermal regimes for developing embryos [79]. Most species appear to move to colder, deeper waters when inshore water temperatures rise steeply in the summer or, for those species that remain in lagoons, stay at locations where thermal regimes are less than 25°C [65].

*Ibacus* sp. adults rarely exceed 20 cm TL [1] and are thus smaller than the adults of subfamily Arctidinidae*.* Sex ratios of all four Australian commercially caught species of *Ibacus* are approximately 1:1. Males are smaller than females because they molt less frequently after attaining sexual maturity. Mating occurs when the female is hard-shelled. Fecundity is much lower than in members of the subfamily Arctidinidae and it is highly variable both within and among the four species of *Ibacus*. It increases with the size of the animal [68]. Egg incubation times have been estimated to vary between approximately 2–4 months and are likely to be temperature dependent with longer incubation in cooler water [61]. Molt frequencies of captive lobsters suggest seasonal molting but wild, tagged lobsters were caught repetitively in consecutive years without having increased in size [68]. Growth models for *I. peronii*, suggest the potential for this species to live for more than 15 years with a maximum size reached after 5–8 years [80].

Very little information is available on adults of *Parribacus* spp. and what does exist is mainly focused on *P. antarcticus*. Two captured females of this species bore evidence of reproductive activity during summer (July) [81].

In *Thenus* spp. growth is quite rapid with 80% of maximum size reached by 2 years of age. Females appear to attain larger sizes than males as evidenced by fishery sampled size ranges in both Indian and Australian waters [82]. Increased abdominal dimensions likely explain the greater weight of females, while maximization of reproductive efficiency via larger size and the ability to carry more eggs explains the greater mean size of females [83]. However, the two sexes eventually grow to a similar size [84]. Differences between Indian and Australian populations of thenids may reflect differences between sub-species or even between different species in view of the recent taxonomic revision of the genus [4].

In the *T. orientalis* fisheries off India, sex ratios are 1:1 [85], but off Australia they are skewed toward males [83] with a ratio of 0.57. In contrast, *T. indicus* sex ratios are at 1:1 throughout the year [83]. As with all scyllarids, fecundity of thenids scales with length. Various studies in India and Australia show at least two annual spawning periods [83, 84]; however, only a single spawning period was reported for *T. orientalis* off the Tokar delta in the Red Sea [84].

Adults of the subfamily Scyllarinae are usually small and information is very limited regarding growth and reproduction. *Scyllarus arctus* appears to have a continuous reproductive period where females can spawn up to three times per year [10]. The sex ratio is skewed toward females and mean size is larger in females.

#### **4. Genetics and population continuity**

The developmental period for scyllarid phyllosomas is far more variable than that for palinurids, and can last from a few weeks to at least 9 months [29, 30]. Lengthy duration of the larval period likely leads to wide oceanic dispersion and, ultimately, connectivity of geographically distant subpopulations resulting in panmixia in adults. Molecular tools are just starting to be used to examine population structure of individual species. In one such study, *S. latus* collected in 2 locations in the Western Mediterranean and 13 locations in four regions in the NE Atlantic, including Southern Portugal and the Macaronesian archipelagos, revealed genetic homogeneity in *S. latus* across all regions [86]. More such studies in other species are needed to understand the population genetics of scyllarid species.

#### **5. Behavior**

Except for *Scyllarides latus* and *Thenus orientalis*, both of which are readily held in laboratory settings, behavior of most slipper lobsters has not been well studied. In addition, the sensory modalities used for behaviors are not well understood as they are in nephropid and palinurid lobsters [87].

#### **5.1 Feeding behavior**

Feeding behavior of adults is dependent on the structures with which lobsters can capture, manipulate, and process their food and differs with life history stage as mouthparts, pereiopods, and the proventriculus gain substance and size. Feeding habits, primarily for the adults of *T. orientalis* [88] and *I. peronii* [89], and *Scyllarides* spp. [90] are known.

As in clawed and spiny lobsters, the esophagus of slipper lobsters is short, presumably to allow for rapid ingestion [57]. This structure leads into the proventriculus, which is divided into the anterior cardiac stomach and the posterior pyloric stomach. The gastric mill of slipper lobsters is smaller and less calcified [88] likely due to the diet specialization that has occurred in slipper lobsters—that of primarily consuming bivalve flesh, or other fleshy items. Food proceeds from the cardiac stomach to the pyloric stomach through a cardio-pyloric valve, which lacks

**33**

**Figure 5.**

*Scyllarid Lobster Biology and Ecology*

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

pereiopod setae from the process of shucking [92].

the spines and accessory teeth seen in other decapods [88]. Dense mats of setae in the pyloric stomach provide filtering of semi-digested food particles with only the smallest particles entering from the cardiac stomach and exiting into the digestive gland. Larger particles are passed into the midgut caecum and hindgut [88]. Little is

Many slipper lobsters (e.g. *Scyllarides* spp.) are bivalve specialists and these have evolved the ability to use the nails of their pereiopods to shuck bivalves [90, 91]. During the feeding sequence, slipper lobsters typically probe the outer valves with their antennules, as though "smelling" and assessing the shell for its possible value [92]. They then pick up and hold the bivalve with either the first, third, and fourth or second, third, and fourth pairs of walking legs, using the dactyl tips of the first or second walking legs to repetitively probe the valve edges [92]. The dactyl tips eventually wedge into the shell edge and then push in further and further to open the valves; this process is known as "wedging" [90]. Once the valves are opened enough to fully insert one pair of pereiopod dactyls, another pair of walking legs (second or third) are used to cut the mantle tissue along the pallial line. The lobster then uses a back-and-forth "scissoring" type motion to increase the opening angle to reach the adductor muscles [92]. The second pair of walking legs cut the adductor muscles, so that the valves open freely. With the valves open, the meat is repetitively scraped out of the valves and passed directly to the third maxillipeds [90, 92]; see **Figure 5**. Until the flesh is actually passed back to the third maxillipeds, the antennules make repeated downward motions to probe inside the valves, to touch the flesh, and to touch the shell as the legs scrap the flesh from it; it is likely that the antennules act as a dual "smell" and "taste" sensory modality due to the damage to

While bivalves are a preferred food source, slipper lobsters are also known to consume sea urchins, crustaceans, sponges, gastropods, barnacles, sea squirts, algae (*Ulva* spp.), and fish [66, 93]. Gut contents of commercially fished *T. orientalis* in India included a high proportion of mollusks (27.7%) followed by bottom sediments (24.1%), fishes (22.9%), crustaceans (10.7%), polychaetes (4.2%) and miscellaneous food items (10.4%) [84]. Scallops, goatfish and shrimps were always consumed when offered under laboratory conditions [83]. Thus, based on stomach contents and laboratory behavior, *T. orientalis* appears to be an opportunistic,

*The feeding sequence of S. aequinoctialis. (1) Lobster approaches bivalve with antennules flicking and sampling odors; (2) pereiopods grab bivalve while antennules "taste" it to assess if feeding sequence will continue; (3) "wedging" of pereiopods into closed valves; (4) probing and "shucking" of the valves, while cutting adductor muscles; (5) close-up of pereiopods ripping adductor muscle; (6) scraping of flesh out of bivalve and delivery to mouthparts.*

understood about the digestive enzymes involved in food breakdown [57].

#### *Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

abdominal dimensions likely explain the greater weight of females, while maximization of reproductive efficiency via larger size and the ability to carry more eggs explains the greater mean size of females [83]. However, the two sexes eventually grow to a similar size [84]. Differences between Indian and Australian populations of thenids may reflect differences between sub-species or even between different

In the *T. orientalis* fisheries off India, sex ratios are 1:1 [85], but off Australia they are skewed toward males [83] with a ratio of 0.57. In contrast, *T. indicus* sex ratios are at 1:1 throughout the year [83]. As with all scyllarids, fecundity of thenids scales with length. Various studies in India and Australia show at least two annual spawning periods [83, 84]; however, only a single spawning period was reported for *T.* 

Adults of the subfamily Scyllarinae are usually small and information is very limited regarding growth and reproduction. *Scyllarus arctus* appears to have a continuous reproductive period where females can spawn up to three times per year [10]. The sex ratio is skewed toward females and mean size is larger in females.

The developmental period for scyllarid phyllosomas is far more variable than that for palinurids, and can last from a few weeks to at least 9 months [29, 30]. Lengthy duration of the larval period likely leads to wide oceanic dispersion and, ultimately, connectivity of geographically distant subpopulations resulting in panmixia in adults. Molecular tools are just starting to be used to examine population structure of individual species. In one such study, *S. latus* collected in 2 locations in the Western Mediterranean and 13 locations in four regions in the NE Atlantic, including Southern Portugal and the Macaronesian archipelagos, revealed genetic homogeneity in *S. latus* across all regions [86]. More such studies in other species

Except for *Scyllarides latus* and *Thenus orientalis*, both of which are readily held in laboratory settings, behavior of most slipper lobsters has not been well studied. In addition, the sensory modalities used for behaviors are not well understood as

Feeding behavior of adults is dependent on the structures with which lobsters

can capture, manipulate, and process their food and differs with life history stage as mouthparts, pereiopods, and the proventriculus gain substance and size. Feeding habits, primarily for the adults of *T. orientalis* [88] and *I. peronii* [89], and

As in clawed and spiny lobsters, the esophagus of slipper lobsters is short, presumably to allow for rapid ingestion [57]. This structure leads into the proventriculus, which is divided into the anterior cardiac stomach and the posterior pyloric stomach. The gastric mill of slipper lobsters is smaller and less calcified [88] likely due to the diet specialization that has occurred in slipper lobsters—that of primarily consuming bivalve flesh, or other fleshy items. Food proceeds from the cardiac stomach to the pyloric stomach through a cardio-pyloric valve, which lacks

are needed to understand the population genetics of scyllarid species.

species in view of the recent taxonomic revision of the genus [4].

*orientalis* off the Tokar delta in the Red Sea [84].

**4. Genetics and population continuity**

they are in nephropid and palinurid lobsters [87].

**32**

**5. Behavior**

**5.1 Feeding behavior**

*Scyllarides* spp. [90] are known.

the spines and accessory teeth seen in other decapods [88]. Dense mats of setae in the pyloric stomach provide filtering of semi-digested food particles with only the smallest particles entering from the cardiac stomach and exiting into the digestive gland. Larger particles are passed into the midgut caecum and hindgut [88]. Little is understood about the digestive enzymes involved in food breakdown [57].

Many slipper lobsters (e.g. *Scyllarides* spp.) are bivalve specialists and these have evolved the ability to use the nails of their pereiopods to shuck bivalves [90, 91]. During the feeding sequence, slipper lobsters typically probe the outer valves with their antennules, as though "smelling" and assessing the shell for its possible value [92]. They then pick up and hold the bivalve with either the first, third, and fourth or second, third, and fourth pairs of walking legs, using the dactyl tips of the first or second walking legs to repetitively probe the valve edges [92]. The dactyl tips eventually wedge into the shell edge and then push in further and further to open the valves; this process is known as "wedging" [90]. Once the valves are opened enough to fully insert one pair of pereiopod dactyls, another pair of walking legs (second or third) are used to cut the mantle tissue along the pallial line. The lobster then uses a back-and-forth "scissoring" type motion to increase the opening angle to reach the adductor muscles [92]. The second pair of walking legs cut the adductor muscles, so that the valves open freely. With the valves open, the meat is repetitively scraped out of the valves and passed directly to the third maxillipeds [90, 92]; see **Figure 5**. Until the flesh is actually passed back to the third maxillipeds, the antennules make repeated downward motions to probe inside the valves, to touch the flesh, and to touch the shell as the legs scrap the flesh from it; it is likely that the antennules act as a dual "smell" and "taste" sensory modality due to the damage to pereiopod setae from the process of shucking [92].

While bivalves are a preferred food source, slipper lobsters are also known to consume sea urchins, crustaceans, sponges, gastropods, barnacles, sea squirts, algae (*Ulva* spp.), and fish [66, 93]. Gut contents of commercially fished *T. orientalis* in India included a high proportion of mollusks (27.7%) followed by bottom sediments (24.1%), fishes (22.9%), crustaceans (10.7%), polychaetes (4.2%) and miscellaneous food items (10.4%) [84]. Scallops, goatfish and shrimps were always consumed when offered under laboratory conditions [83]. Thus, based on stomach contents and laboratory behavior, *T. orientalis* appears to be an opportunistic,

#### **Figure 5.**

*The feeding sequence of S. aequinoctialis. (1) Lobster approaches bivalve with antennules flicking and sampling odors; (2) pereiopods grab bivalve while antennules "taste" it to assess if feeding sequence will continue; (3) "wedging" of pereiopods into closed valves; (4) probing and "shucking" of the valves, while cutting adductor muscles; (5) close-up of pereiopods ripping adductor muscle; (6) scraping of flesh out of bivalve and delivery to mouthparts.*

omnivorous, benthic feeder that burrows in soft and sandy mud, engulfs sediments consisting of sand and mud, and then preys on organisms that it encounters in this way [84].

#### **5.2 Sheltering behavior and substrate preferences**

Adult specimens of *Scyllarides* spp. are camouflaged to a certain extent due to their flattened morphology and coloration that blends into hard substrates (e.g. [72, 94]). However, in the brightly illuminated water of their shallow habitats, this camouflage provides only limited concealment against diurnal predators. Thus, most are nocturnal, foraging at night and sheltering during the day ([66, 95, 96] for *S. astori*; [72] for *S. latus*). A more recent set of lab studies documented that *S. latus* is more active at higher temperatures, and demonstrated that warming water temperatures elicited markedly longer movements [97].

Gregarious sheltering has been noted for *S. latus* (Spanier, personal observation) but predation studies at field sites demonstrate that grouping does not decrease percapita predation rates on individuals within the group. Grouped lobsters suffer an equal rate of predation as lone animals and gain only a small advantage of time, as predatory attack patterns are less focused when lobsters are grouped [98]. Reports of gregarious behavior also exist for *S. nodifer* [99], but nothing is known about the function of such behavior.

The adults of many species are found on hard and soft substrates (**Figure 6**). *Scyllarides* species sampled both on hard (rocks, caves, coral heads) and soft substrates often result from circumstances where lobsters that usually shelter in hard substrates were collected in soft substrates during their short and long term movements, but some species such as *Scyllarides elisabethae*, *S. nodifer*, and

#### **Figure 6.**

*Scyllarides latus in artificial reef structures (A, B) and natural rock outcropping (C, D). In natural outcroppings and large openings in artificial reefs, they typically co-habit space with other conspecifics (B, D). Photographs by Stephen Breitstein.*

**35**

**Figure 7.**

*Scyllarid Lobster Biology and Ecology*

dusk and just prior to dawn.

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

**5.3 Predators and antipredator behavior**

shells and bettering their swimming escape behavior [107].

buy them extra time for escape when attacked.

*S. aequinoctialis* are only found in mud or sand [1, 99, 100]. *Parribacus* species also inhabit hard substrates (corals structures, caves) or are found in sandy bottom [1, 81]. All five species of *Thenus*, and eight species of *Ibacus* inhabit relatively soft sandy or muddy substrates [4, 68] and are well-adapted for digging into the substrate in terms of their morphology as well as their behavior. *I. peronii* spends most of the day underneath the sand [101] and both *T. indicus* and *T. orientalis* spent daytime hours buried in sediment with only eyes and antennules exposed [83], but were nocturnally active, with clear peaks in activity at

The response of slipper lobsters to predator attack (e.g., by gregarious triggerfish) has been well studied [79, 98, 102–108] and consists of three strategies, two of which are typically executed in sequence: (i) the "fortress strategy" in which the animal grasps the bottom and attempts to outlast its attacker's motivation to penetrate its hard shell (described in [107]); (ii) the "swimming escape" response (described in [102, 105–107]); and (iii) remaining sheltered in dens [79, 103]. Lacking claws (like *Homarus* spp.) or long spinose antennae (like spiny lobsters; see [109–112]) with which to fend off swimming predators, slipper lobsters have developed a shell that is thicker and more durable to mechanical insult than clawed or spiny lobsters [107]. They use their short, strong legs to grasp the substrate and resist being dislodged [105, 106] (see **Figure 7**), and if this fails, they are exceptionally deft swimmers capable of evasive maneuvers [102]. Also they may suddenly change the direction of their swimming, presumably to confuse the chasing predator. This is an energetically costly response to a threat and is generally used as a last resort. Slipper lobsters may match the energy invested by clawed lobsters in claws and spiny lobsters in antennae by increasing only moderately the thickness of their

Slipper lobsters that live in complex substrates also display a variety of shelterrelated behaviors that provide a third highly effective survival strategy [105]. By combining nocturnal foraging with diurnal sheltering, as well as carrying food to their shelters for later consumption, slipper lobsters may fully minimize their exposure to diurnal predators. The tendency for cohabitation with conspecifics (as seen in *P. antarcticus* [1, 81] or *S. latus* [98]) may be adaptive because of confusion effects (which lobster to target), alerting earlier to predators due to higher levels of "prey vigilance", or being concealed among conspecifics ("dilution effect" *sensu* [113]; see **Figure 7**). If these tactics fail, their thick carapace effectively blunt cracks [107, 114, 115] and may

*Anti-predator responses of Scyllarides latus. (A) Tail flip in response to on-coming threat by triggerfish; (B) wedging into rocks in response to a predator (such as octopus) that can grip; (C) gregarious behavior in absence* 

*of shelter where each individual is concealed among other conspecifics. Photographs by Ehud Spanier.*

*Crustacea*

way [84].

function of such behavior.

omnivorous, benthic feeder that burrows in soft and sandy mud, engulfs sediments consisting of sand and mud, and then preys on organisms that it encounters in this

Adult specimens of *Scyllarides* spp. are camouflaged to a certain extent due to their flattened morphology and coloration that blends into hard substrates (e.g. [72, 94]). However, in the brightly illuminated water of their shallow habitats, this camouflage provides only limited concealment against diurnal predators. Thus, most are nocturnal, foraging at night and sheltering during the day ([66, 95, 96] for *S. astori*; [72] for *S. latus*). A more recent set of lab studies documented that *S. latus* is more active at higher temperatures, and demonstrated that warming water

Gregarious sheltering has been noted for *S. latus* (Spanier, personal observation) but predation studies at field sites demonstrate that grouping does not decrease percapita predation rates on individuals within the group. Grouped lobsters suffer an equal rate of predation as lone animals and gain only a small advantage of time, as predatory attack patterns are less focused when lobsters are grouped [98]. Reports of gregarious behavior also exist for *S. nodifer* [99], but nothing is known about the

The adults of many species are found on hard and soft substrates (**Figure 6**). *Scyllarides* species sampled both on hard (rocks, caves, coral heads) and soft substrates often result from circumstances where lobsters that usually shelter in hard substrates were collected in soft substrates during their short and long term movements, but some species such as *Scyllarides elisabethae*, *S. nodifer*, and

*Scyllarides latus in artificial reef structures (A, B) and natural rock outcropping (C, D). In natural outcroppings and large openings in artificial reefs, they typically co-habit space with other conspecifics (B, D).* 

**5.2 Sheltering behavior and substrate preferences**

temperatures elicited markedly longer movements [97].

**34**

**Figure 6.**

*Photographs by Stephen Breitstein.*

*S. aequinoctialis* are only found in mud or sand [1, 99, 100]. *Parribacus* species also inhabit hard substrates (corals structures, caves) or are found in sandy bottom [1, 81]. All five species of *Thenus*, and eight species of *Ibacus* inhabit relatively soft sandy or muddy substrates [4, 68] and are well-adapted for digging into the substrate in terms of their morphology as well as their behavior. *I. peronii* spends most of the day underneath the sand [101] and both *T. indicus* and *T. orientalis* spent daytime hours buried in sediment with only eyes and antennules exposed [83], but were nocturnally active, with clear peaks in activity at dusk and just prior to dawn.

#### **5.3 Predators and antipredator behavior**

The response of slipper lobsters to predator attack (e.g., by gregarious triggerfish) has been well studied [79, 98, 102–108] and consists of three strategies, two of which are typically executed in sequence: (i) the "fortress strategy" in which the animal grasps the bottom and attempts to outlast its attacker's motivation to penetrate its hard shell (described in [107]); (ii) the "swimming escape" response (described in [102, 105–107]); and (iii) remaining sheltered in dens [79, 103]. Lacking claws (like *Homarus* spp.) or long spinose antennae (like spiny lobsters; see [109–112]) with which to fend off swimming predators, slipper lobsters have developed a shell that is thicker and more durable to mechanical insult than clawed or spiny lobsters [107]. They use their short, strong legs to grasp the substrate and resist being dislodged [105, 106] (see **Figure 7**), and if this fails, they are exceptionally deft swimmers capable of evasive maneuvers [102]. Also they may suddenly change the direction of their swimming, presumably to confuse the chasing predator. This is an energetically costly response to a threat and is generally used as a last resort. Slipper lobsters may match the energy invested by clawed lobsters in claws and spiny lobsters in antennae by increasing only moderately the thickness of their shells and bettering their swimming escape behavior [107].

Slipper lobsters that live in complex substrates also display a variety of shelterrelated behaviors that provide a third highly effective survival strategy [105]. By combining nocturnal foraging with diurnal sheltering, as well as carrying food to their shelters for later consumption, slipper lobsters may fully minimize their exposure to diurnal predators. The tendency for cohabitation with conspecifics (as seen in *P. antarcticus* [1, 81] or *S. latus* [98]) may be adaptive because of confusion effects (which lobster to target), alerting earlier to predators due to higher levels of "prey vigilance", or being concealed among conspecifics ("dilution effect" *sensu* [113]; see **Figure 7**). If these tactics fail, their thick carapace effectively blunt cracks [107, 114, 115] and may buy them extra time for escape when attacked.

#### **Figure 7.**

*Anti-predator responses of Scyllarides latus. (A) Tail flip in response to on-coming threat by triggerfish; (B) wedging into rocks in response to a predator (such as octopus) that can grip; (C) gregarious behavior in absence of shelter where each individual is concealed among other conspecifics. Photographs by Ehud Spanier.*

#### *Crustacea*

Very little is known about the antipredator behavior of soft bottom species. Fully buried *Thenus* spp. are entirely concealed except for the eyes and antennules [83]. *Ibacus* spp. also are found on soft bottom substrates and are known to bury into those sediments, much in the same manner as *Thenus* spp. [68, 101] presumably also for concealment.

Besides triggerfish, spotted gully shark (*Triakis megalopterus* (Smith, 1849) have been reported to feed on *S. elisabethae* in South Africa [116], groupers (*Epinephelus* and *Mycteroperca* spp.) have been reported as predators of adult and juvenile *S. latus* [26] and *S. arctus*, *S. aequinoctialis*, and *S. nodifer* [56, 117]. Combers (*Serranus* spp.) and rainbow wrasse (*Coris julis* Linnaeus, 1758) apparently prey on juvenile *S. latus* [26]. Juvenile *S. aequinoctialis* were found in the gut of a large invasive alien red lionfish (*Pterois* spp.) in Belize [118].

#### **5.4 Mating behavior**

Most information on reproductive behavior comes from laboratory observations. Unlike clawed lobsters where mating usually occurs shortly after females molt, scyllarids are more similar to palinurids in that mating and molting are separate and unrelated events, although in the hooded slipper lobster (*S. deceptor*), copulation follows molting [119]. The general decoupling of molting and mating is largely due to males supplying females with external spermatophores that females use within hours or a few days. Nevertheless, some differences exist among the different subfamilies and those are summarized here. Males of *Scyllarides* spp. produce white, gelatinous spermatophores, which they carry around on the base of their fourth and fifth pereiopods ([74]; Spanier, personal observations) and transfer to females. In some species, females have been observed carrying spermatophores externally 6–10 days prior to egg extrusion (*S. latus*, [26, 74]), while in others, the lack of observable spermatophores prior to egg extrusion has led to a belief that the spermatophore is stored internally and fertilization is internal (*S. nodifer*, [55]; *S. squammosus*, [120]). Females of many species can spawn multiple broods in a season due to short brooding periods, and these broods are usually carried during spring and summer months. Only in *S. latus* have both eggs and spermatophores been observed simultaneously [74].

Male *Thenus* spp. do not appear to deposit a persistent spermatophoric mass in the process of mating [83]. Soft, non-persistent masses were observed [121] for *T. orientalis* and females oviposited within 8 hours post-mating and lost the spermatophore within 12 hours. No courtship behaviors or acts of mating have been witnessed in *Thenus orientalis* or *T. indicus* during 2000 hours of remote video observation [83], so it assumed that mating rituals are very simple. In *Ibacus* spp. spermatophoric masses were persistent, gelatinous, and opaque white in color, and were deposited in two elongated strips, approximately 20–30 mm long, close to the genital openings of the female [68]. Fertilization is likely external and occurs relatively soon after mating.

From the very limited information available on *Parribacus* spp., it appears that spermatophores are persistent even after spawning and new spermatophores are deposited atop old ones [81].

In *Scyllarus* spp. males deposit two jelly-like strings of spermatophores ventrally from the base of the fifth pereiopod to the second abdominal segment; these are used within hours to inseminate eggs and any remaining sperm mass degrades quickly [10]. Females are capable of multiple spawning events per year, but the number depends largely on environmental conditions; members of the same species may produce three broods in one area, but only two in another. This flexibility in

**37**

*Scyllarid Lobster Biology and Ecology*

**5.5 Movement patterns**

5 year period [123].

directional patterns [124].

and *Thenus* spp. [127].

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

reproduction may prove advantageous when thermal regimes are favorable for rapid gonadal maturation, shorter incubation periods, or rapid larval development [10].

Slipper lobsters movements consist of either slow, benthic walking used for daily nomadic movements within a small home range and for seasonal migrations from shallow inshore waters to deeper offshore waters or swimming movements that are used for escape or vertical migratory movements. Daily activity patterns suggest that slipper lobsters have endogenous clocks that provide for circadian rhythms with higher locomotor periods during night hours [122]. Tagging studies of *S. latus* off the coast of Israel confirm the slow, benthic walking patterns: local movements within a home range, presumably to forage and migratory offshore movements [79]. While residing inshore (February to June in the south-eastern Mediterranean), lobsters make short-range movements from reef shelters to forage and 71% return to these reef shelters. However, lobster numbers decreased in the reef shelters, ultimately decreasing to zero in summer months (June through August), and lobsters did not return to the reef until the following winter when their numbers peaked in the spring. This suggests a migration offshore that would correspond to increased water temperatures inshore [79]. Similar tagging studies off Sicily showed no such migratory movements [70]. *Scyllarides squamosus* also appears to make no long-range migratory movements, with mean distances moved from tagging location by most (97.2%) individuals being <1 km over a

Mobility of *Thenus* spp. in Australia also has been examined through use of tag and recapture studies and monitoring of commercial catch levels [83, 84]. *Thenus* spp. tend to be very mobile and capable of moving large distances, but because their movements lack any kind of pattern or directionality, they are not likely to be migratory. Likewise, *Ibacus* spp. exhibit nomadic movement patterns that have no

Swimming behavior constitutes a form of locomotion in which a single "appendage"—the abdomen—produces thrust by a combination of a rowing action and a final "squeeze" force when the abdomen presses against the cephalothorax [125]. Although the tail-flip response is known in adults and juveniles of all three major

The hydrodynamics of swimming in slipper lobsters has been studied in *Ibacus peroni*, *I. alticrenatus* [101, 126–128]*, Thenus orientalis* [83, 126, 127, 129] and *Scyllarides latus* [102, 130, 131]. *S. latus* uses a "burst-and-coast" type of swimming in response to a threat. This burst-and-coast swimming consists of large amplitude movements of the abdomen followed by periods of powerless gliding. Acceleration can reach top velocities of three body lengths per second while deceleration during gliding decreases to velocities of less than one body length per second. Escape swimming is of short duration used only in emergencies to get to safety, as it requires considerable energy. The flattened second antennae of *S. latus* (mistakenly called "shovels" or "flippers"), with their movable joints, serve as stabilizers or rudders to control the swimming movement [130]. This adjustment in lift via the second antennae is also seen in *Ibacus* spp.

In *Thenus* spp., there are two distinct forms of swimming: a locomotory form that is characterized by a slower speed (average of 29 cm s−1) and the absence of explicit stimulus, and escape swimming which is much faster (average of 1 m s−1), similar to that seen in *S. latus*, and always caused by direct stimulus or threat [83, 129].

taxonomic group of lobsters, it is best developed in slipper lobsters.

reproduction may prove advantageous when thermal regimes are favorable for rapid gonadal maturation, shorter incubation periods, or rapid larval development [10].

#### **5.5 Movement patterns**

*Crustacea*

for concealment.

**5.4 Mating behavior**

lionfish (*Pterois* spp.) in Belize [118].

observed simultaneously [74].

relatively soon after mating.

deposited atop old ones [81].

Very little is known about the antipredator behavior of soft bottom species. Fully buried *Thenus* spp. are entirely concealed except for the eyes and antennules [83]. *Ibacus* spp. also are found on soft bottom substrates and are known to bury into those sediments, much in the same manner as *Thenus* spp. [68, 101] presumably also

Besides triggerfish, spotted gully shark (*Triakis megalopterus* (Smith, 1849) have been reported to feed on *S. elisabethae* in South Africa [116], groupers (*Epinephelus* and *Mycteroperca* spp.) have been reported as predators of adult and juvenile *S. latus* [26] and *S. arctus*, *S. aequinoctialis*, and *S. nodifer* [56, 117]. Combers (*Serranus* spp.) and rainbow wrasse (*Coris julis* Linnaeus, 1758) apparently prey on juvenile *S. latus* [26]. Juvenile *S. aequinoctialis* were found in the gut of a large invasive alien red

Most information on reproductive behavior comes from laboratory observations. Unlike clawed lobsters where mating usually occurs shortly after females molt, scyllarids are more similar to palinurids in that mating and molting are separate and unrelated events, although in the hooded slipper lobster (*S. deceptor*), copulation follows molting [119]. The general decoupling of molting and mating is largely due to males supplying females with external spermatophores that females use within hours or a few days. Nevertheless, some differences exist among the different subfamilies and those are summarized here. Males of *Scyllarides* spp. produce white, gelatinous spermatophores, which they carry around on the base of their fourth and fifth pereiopods ([74]; Spanier, personal observations) and transfer to females. In some species, females have been observed carrying spermatophores externally 6–10 days prior to egg extrusion (*S. latus*, [26, 74]), while in others, the lack of observable spermatophores prior to egg extrusion has led to a belief that the spermatophore is stored internally and fertilization is internal (*S. nodifer*, [55]; *S. squammosus*, [120]). Females of many species can spawn multiple broods in a season due to short brooding periods, and these broods are usually carried during spring and summer months. Only in *S. latus* have both eggs and spermatophores been

Male *Thenus* spp. do not appear to deposit a persistent spermatophoric mass in the process of mating [83]. Soft, non-persistent masses were observed [121] for *T. orientalis* and females oviposited within 8 hours post-mating and lost the spermatophore within 12 hours. No courtship behaviors or acts of mating have been witnessed in *Thenus orientalis* or *T. indicus* during 2000 hours of remote video observation [83], so it assumed that mating rituals are very simple. In *Ibacus* spp. spermatophoric masses were persistent, gelatinous, and opaque white in color, and were deposited in two elongated strips, approximately 20–30 mm long, close to the genital openings of the female [68]. Fertilization is likely external and occurs

From the very limited information available on *Parribacus* spp., it appears that spermatophores are persistent even after spawning and new spermatophores are

In *Scyllarus* spp. males deposit two jelly-like strings of spermatophores ventrally from the base of the fifth pereiopod to the second abdominal segment; these are used within hours to inseminate eggs and any remaining sperm mass degrades quickly [10]. Females are capable of multiple spawning events per year, but the number depends largely on environmental conditions; members of the same species may produce three broods in one area, but only two in another. This flexibility in

**36**

Slipper lobsters movements consist of either slow, benthic walking used for daily nomadic movements within a small home range and for seasonal migrations from shallow inshore waters to deeper offshore waters or swimming movements that are used for escape or vertical migratory movements. Daily activity patterns suggest that slipper lobsters have endogenous clocks that provide for circadian rhythms with higher locomotor periods during night hours [122]. Tagging studies of *S. latus* off the coast of Israel confirm the slow, benthic walking patterns: local movements within a home range, presumably to forage and migratory offshore movements [79]. While residing inshore (February to June in the south-eastern Mediterranean), lobsters make short-range movements from reef shelters to forage and 71% return to these reef shelters. However, lobster numbers decreased in the reef shelters, ultimately decreasing to zero in summer months (June through August), and lobsters did not return to the reef until the following winter when their numbers peaked in the spring. This suggests a migration offshore that would correspond to increased water temperatures inshore [79]. Similar tagging studies off Sicily showed no such migratory movements [70]. *Scyllarides squamosus* also appears to make no long-range migratory movements, with mean distances moved from tagging location by most (97.2%) individuals being <1 km over a 5 year period [123].

Mobility of *Thenus* spp. in Australia also has been examined through use of tag and recapture studies and monitoring of commercial catch levels [83, 84]. *Thenus* spp. tend to be very mobile and capable of moving large distances, but because their movements lack any kind of pattern or directionality, they are not likely to be migratory. Likewise, *Ibacus* spp. exhibit nomadic movement patterns that have no directional patterns [124].

Swimming behavior constitutes a form of locomotion in which a single "appendage"—the abdomen—produces thrust by a combination of a rowing action and a final "squeeze" force when the abdomen presses against the cephalothorax [125]. Although the tail-flip response is known in adults and juveniles of all three major taxonomic group of lobsters, it is best developed in slipper lobsters.

The hydrodynamics of swimming in slipper lobsters has been studied in *Ibacus peroni*, *I. alticrenatus* [101, 126–128]*, Thenus orientalis* [83, 126, 127, 129] and *Scyllarides latus* [102, 130, 131]. *S. latus* uses a "burst-and-coast" type of swimming in response to a threat. This burst-and-coast swimming consists of large amplitude movements of the abdomen followed by periods of powerless gliding. Acceleration can reach top velocities of three body lengths per second while deceleration during gliding decreases to velocities of less than one body length per second. Escape swimming is of short duration used only in emergencies to get to safety, as it requires considerable energy. The flattened second antennae of *S. latus* (mistakenly called "shovels" or "flippers"), with their movable joints, serve as stabilizers or rudders to control the swimming movement [130]. This adjustment in lift via the second antennae is also seen in *Ibacus* spp. and *Thenus* spp. [127].

In *Thenus* spp., there are two distinct forms of swimming: a locomotory form that is characterized by a slower speed (average of 29 cm s−1) and the absence of explicit stimulus, and escape swimming which is much faster (average of 1 m s−1), similar to that seen in *S. latus*, and always caused by direct stimulus or threat [83, 129]. In locomotory swimming, the aerofoil body shape generates lift as the abdomen thrusts downward; drag is reduced by all pereiopods being extended anteriorly [127]. Lift height was controlled by the second antennae and each flexion helped to maintain the animal above the sediment [127, 129]. In comparison, escape swimming always consisted of an abdominal flexion that was proportional to the magnitude of the stimulus. While *Ibacus* spp. can tail flip, it does not do so in response to a sudden threat, but seems to be related more to a righting response when the animal is flipped over [128].

#### **6. Diseases**

There are only a few reports on diseases or parasites of slipper lobsters, in general, and of specific species in particular [132, 133]. This limited information is usually focused on commercial species and those that have potential in aquaculture. *Scyllarides* specimens die while being held in the laboratory from unknown causes. Halacarid mites*, Copidognathus* spp., cause tissue necrosis in the gills of the *P. antarcticus* [133]. Aquaculture of *Thenus* spp. and *Ibacus* spp. will require more knowledge on pathogens of these species since the phyllosomas are very susceptible to microorganisms in the water column [69, 134]. There are also reports of parasites in adults. For example, a new species of parasitic copepod, *Choniomyzon inflatus* n., has recently been collected from the external egg masses of the smooth fan lobster *Ibacus novemdentatu* [135]. The Gram-negative *Vibrio* causes mass mortality during hatchery production of phyllosoma larvae and also affects their live feed of *Artemia* nauplii. Filamentous bacteria (*Leucothrix* sp.) and protozoans (such as *Zoothamnium* spp., *Vorticella* spp. and *Acinata* spp.) can also biofoul the phyllosomas and cause mortality [8]. Traditionally, a number of antibiotics as well as other chemicals have been heavily used for controlling bacterial colonies in the rearing water. Alternative methods are the use of ultraviolet light (UV) and ozone (O3) sterilizers [8, 69].

#### **7. Environmental effects and conservation**

Overfishing, climate change, and habitat degradation are the main reasons for the drastic decline of marine populations over the past 30 years [136]. The effects of overfishing characterize many populations of commercial slipper lobsters and result in decreases in exploited stocks in the last few decades. Some species of slipper lobsters, formerly ignored, are now targeted due to the decline in other species (e.g., spiny lobsters) especially around the waters off Australia, Hawaii, India, the Galápagos Islands, and the countries surrounding the Mediterranean Sea. As a consequence, slipper lobsters have rapidly decreased in stock abundance to the point that local fisheries have collapsed [7]. Regulations established that try to protect these populations may have unexpected negative effects. For example, the prohibition against landing ovigerous females of *Scyllarus arctus* in NE Spain has biased the fishery toward males [10], which then affects natural sex ratios, opportunities for females to find mates, and ultimately population structure. Protected natural reserves/no-take zones can, to a certain extent, help rectify these effects [137], but require governmental action and policing. A fully protected, natural reserve off the northern Mediterranean coast of Israel has demonstrated significantly higher numbers of female and male *Scyllarides latus* compared to a control area with the same characteristics [138]. The specimens in the reserve were also significantly larger than those in the control, non-protected area.

**39**

*Scyllarid Lobster Biology and Ecology*

and 100% [141].

**8. Conclusions**

40 years ago.

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

Instead of regulations that may have unintended consequences or the creation of natural reserves that require political will, policing, and industry buy-in, targeted fishing moratoriums may also help to rebuild stocks. For example, depleted stocks of *S. elisabethae* recovered during a six-year moratorium from fishing and trapping off eastern South Africa [139]. However, despite years of protection, populations of *S. squammosus* in the Northwestern Hawaiian Islands, have failed to recover [140]. Possible factors that may limit population growth and recovery, include: climate change, Allee effects, and interspecific interactions. Community changes that come from overfishing of coral reef fauna might have broad and lasting results; once lost, valuable resources and ecosystem services may not quickly rebound to pre-exploitation levels and may have cascading effects on the larger fauna that rely on these resources [140]. Projected climate change impacts on the distribution of coastal lobsters, including a synthesis of 68 slipper lobsters species, suggest negative changes in diversity in areas of high commercial fishing due to habitat loss [141]. Such changes are expected to be particularly dramatic in the tropics, with species projected to contract their climatic envelope between 40

Although slipper lobsters represent the most speciose group of lobsters and have been exploited in targeted or by-catch fisheries, they have been and continue to be poorly studied compared to the less speciose but more popular clawed and spiny lobsters. Lack of knowledge of basic biological features such as life history, behavior, physiology, and disease does not bode well for the long-term health of populations especially when most scientists expect dramatic climatic changes to impact oceanic habitats and community structure. Given that these lobsters represent a potential food source for an ever-growing human population, it would be beneficial to understand much more about these lobsters with targeted studies, supported by governmental agencies, much as we saw for clawed and spiny lobsters nearly

#### *Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

is flipped over [128].

**6. Diseases**

sterilizers [8, 69].

**7. Environmental effects and conservation**

larger than those in the control, non-protected area.

In locomotory swimming, the aerofoil body shape generates lift as the abdomen thrusts downward; drag is reduced by all pereiopods being extended anteriorly [127]. Lift height was controlled by the second antennae and each flexion helped to maintain the animal above the sediment [127, 129]. In comparison, escape swimming always consisted of an abdominal flexion that was proportional to the magnitude of the stimulus. While *Ibacus* spp. can tail flip, it does not do so in response to a sudden threat, but seems to be related more to a righting response when the animal

There are only a few reports on diseases or parasites of slipper lobsters, in general, and of specific species in particular [132, 133]. This limited information is usually focused on commercial species and those that have potential in aquaculture. *Scyllarides* specimens die while being held in the laboratory from unknown causes. Halacarid mites*, Copidognathus* spp., cause tissue necrosis in the gills of the *P. antarcticus* [133]. Aquaculture of *Thenus* spp. and *Ibacus* spp. will require more knowledge on pathogens of these species since the phyllosomas are very susceptible to microorganisms in the water column [69, 134]. There are also reports of parasites in adults. For example, a new species of parasitic copepod, *Choniomyzon inflatus* n., has recently been collected from the external egg masses of the smooth fan lobster *Ibacus novemdentatu* [135]. The Gram-negative *Vibrio* causes mass mortality during hatchery production of phyllosoma larvae and also affects their live feed of *Artemia* nauplii. Filamentous bacteria (*Leucothrix* sp.) and protozoans (such as *Zoothamnium* spp., *Vorticella* spp. and *Acinata* spp.) can also biofoul the phyllosomas and cause mortality [8]. Traditionally, a number of antibiotics as well as other chemicals have been heavily used for controlling bacterial colonies in the rearing water. Alternative methods are the use of ultraviolet light (UV) and ozone (O3)

Overfishing, climate change, and habitat degradation are the main reasons for the drastic decline of marine populations over the past 30 years [136]. The effects of overfishing characterize many populations of commercial slipper lobsters and result in decreases in exploited stocks in the last few decades. Some species of slipper lobsters, formerly ignored, are now targeted due to the decline in other species (e.g., spiny lobsters) especially around the waters off Australia, Hawaii, India, the Galápagos Islands, and the countries surrounding the Mediterranean Sea. As a consequence, slipper lobsters have rapidly decreased in stock abundance to the point that local fisheries have collapsed [7]. Regulations established that try to protect these populations may have unexpected negative effects. For example, the prohibition against landing ovigerous females of *Scyllarus arctus* in NE Spain has biased the fishery toward males [10], which then affects natural sex ratios, opportunities for females to find mates, and ultimately population structure. Protected natural reserves/no-take zones can, to a certain extent, help rectify these effects [137], but require governmental action and policing. A fully protected, natural reserve off the northern Mediterranean coast of Israel has demonstrated significantly higher numbers of female and male *Scyllarides latus* compared to a control area with the same characteristics [138]. The specimens in the reserve were also significantly

**38**

Instead of regulations that may have unintended consequences or the creation of natural reserves that require political will, policing, and industry buy-in, targeted fishing moratoriums may also help to rebuild stocks. For example, depleted stocks of *S. elisabethae* recovered during a six-year moratorium from fishing and trapping off eastern South Africa [139]. However, despite years of protection, populations of *S. squammosus* in the Northwestern Hawaiian Islands, have failed to recover [140]. Possible factors that may limit population growth and recovery, include: climate change, Allee effects, and interspecific interactions. Community changes that come from overfishing of coral reef fauna might have broad and lasting results; once lost, valuable resources and ecosystem services may not quickly rebound to pre-exploitation levels and may have cascading effects on the larger fauna that rely on these resources [140]. Projected climate change impacts on the distribution of coastal lobsters, including a synthesis of 68 slipper lobsters species, suggest negative changes in diversity in areas of high commercial fishing due to habitat loss [141]. Such changes are expected to be particularly dramatic in the tropics, with species projected to contract their climatic envelope between 40 and 100% [141].

#### **8. Conclusions**

Although slipper lobsters represent the most speciose group of lobsters and have been exploited in targeted or by-catch fisheries, they have been and continue to be poorly studied compared to the less speciose but more popular clawed and spiny lobsters. Lack of knowledge of basic biological features such as life history, behavior, physiology, and disease does not bode well for the long-term health of populations especially when most scientists expect dramatic climatic changes to impact oceanic habitats and community structure. Given that these lobsters represent a potential food source for an ever-growing human population, it would be beneficial to understand much more about these lobsters with targeted studies, supported by governmental agencies, much as we saw for clawed and spiny lobsters nearly 40 years ago.

#### **Author details**

Kari L. Lavalli1 \*, Ehud Spanier2 and Jason S. Goldstein3

1 Division of Natural Sciences and Mathematics, College of General Studies, Boston University, Boston, MA, USA

2 The Leon Recanati Institute for Maritime Studies and Department for Maritime Civilizations, The Leon H. Charney School for Marine Sciences, University of Haifa, Haifa, Israel

3 Wells National Estuarine Research Reserve, Maine Coastal Ecology Center, Wells, Maine, USA

\*Address all correspondence to: klavalli@yahoo.com

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

**41**

*Scyllarid Lobster Biology and Ecology*

Vol. 13. Rome: FAO; 1991

**References**

Boston; 2010. pp. 426-532

Group; 2007. pp. 3-21

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

[1] Holthuis LB. Marine Lobsters of the World. FAO Fisheries Synopsis No.125. [9] Özcan T, Ateş AS, Bakir K, Katağan T.

Levantine Sea coast of Turkey. In: Turan C, Salihoğlu B, Özgür Özbek E, Öztürk B, editors. The Turkish Part of the Mediterranean Sea: Marine Biodiversity,

Governance. Turkish Marine Research Foundation (TUDAV), Publication No: 43; Istanbul, Turkey; 2016. 2016. pp. 392-406. Available from: http:// tudav.org/wp-content/uploads/2018/04/ MEDITERRANEAN\_SEA\_2016.pdf

Commercial crustaceans on the

Fisheries, Conservation and

[10] Alborés I, García-Soler C, Fernández L. Reproductive biology of the slipper lobster *Scyllarus arctus* in Galicia (NW Spain): Implications for fisheries management. Fisheries

[11] Fujii Y, Fujiwara T, Koide Y, Hasan I, Sugawara S, Rajia S, et al. Internalization of a novel, huge lectin from *Ibacus novemdentatus* (slipper lobster) induces apoptosis of mammalian cancer cells. Glycoconjugate

Research. 2019;**212**:1-11

Journal. 2017;**34**(1):85-94

2006. pp. 113-145

[12] Patek SN, Feldmann RM, Porter M, Tshudy D. Phylogeny and evolution of lobsters. In: Phillips BF, editor. Lobsters: Biology, Management, Aquaculture and Fisheries. Oxford: Blackwell Publishing;

[13] Bracken-Grissom HD, Ahyong ST,

Schweitzer CE, Breinholt JW, et al. The emergences of the lobsters: Phylogenetic relationships, morphological evolution and divergence time comparisons of an ancient group (Decapoda: Achelata, Astacidea, Glypheidea, Polychelidae). Systematic Biology. 2014;**63**:457-479

[14] Schweitzer CE, Feldmann RM. Lobster (Decapoda) diversity and evolutionary patterns through time. Journal of Crustacean Biology.

2014;**34**(6):820-847

Wilkinson RD, Feldmann RM,

[2] Lavalli KL, Spanier E. The Palinura. In: Forest J, von Vaupel Klein JC, editors. The Crustacea, Traite de Zoologie 9A— Decapoda. Koninklijke Brill: Leiden,

[3] Webber WR, Booth JD. Taxonomy and evolution. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster**,** Crustacean Issues 17. New York: CRC Press, Francis & Taylor

[4] Burton TE, Davie PJF. A revision of the shovel-nosed lobsters of the genus *Thenus* (Crustacea: Decapoda: Scyllaridae), with descriptions of three new species. Zootaxa. 2007;**1429**:1-38

[5] Yang CH, Bracken-Grissom H, Kim D, Crandall KA, Chan TY. Phylogenetic relationships, character evolution, and taxonomic implications within the slipper lobsters (Crustacea: Decapoda: Scyllaridae). Molecular Phylogenetics and Evolution. 2012;**62**(1):237-250

[6] Davis KE, Hesketh TW, Delmer C, Wills MA. Towards a supertree of Arthropoda: A species-level supertree of the spiny, slipper and coral lobsters (Decapoda: Achelata). PLoS ONE. 2015;**10**(10):e0140110. DOI: 10.1371/

[7] Spanier E, Lavalli KL. Slipper lobster fisheries—Present status and future perspectives. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster, Crustacean Issues 17. Vol. 2007. New York: CRC Press, Francis & Taylor Group; 2007. pp. 377-391

[8] Vijayakumaran M, Radhakrishnan EV. Slipper lobsters. In: Fotedar R, Phillips B, editors. Recent Advances and New Species in Aquaculture. Oxford, UK: Wiley-Blackwell; 2011. pp. 85-102

journal.pone.0140110

#### **References**

*Crustacea*

**40**

**Author details**

Kari L. Lavalli1

Haifa, Israel

Maine, USA

\*, Ehud Spanier2

\*Address all correspondence to: klavalli@yahoo.com

provided the original work is properly cited.

Boston University, Boston, MA, USA

and Jason S. Goldstein3

1 Division of Natural Sciences and Mathematics, College of General Studies,

2 The Leon Recanati Institute for Maritime Studies and Department for Maritime Civilizations, The Leon H. Charney School for Marine Sciences, University of Haifa,

3 Wells National Estuarine Research Reserve, Maine Coastal Ecology Center, Wells,

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

[1] Holthuis LB. Marine Lobsters of the World. FAO Fisheries Synopsis No.125. Vol. 13. Rome: FAO; 1991

[2] Lavalli KL, Spanier E. The Palinura. In: Forest J, von Vaupel Klein JC, editors. The Crustacea, Traite de Zoologie 9A— Decapoda. Koninklijke Brill: Leiden, Boston; 2010. pp. 426-532

[3] Webber WR, Booth JD. Taxonomy and evolution. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster**,** Crustacean Issues 17. New York: CRC Press, Francis & Taylor Group; 2007. pp. 3-21

[4] Burton TE, Davie PJF. A revision of the shovel-nosed lobsters of the genus *Thenus* (Crustacea: Decapoda: Scyllaridae), with descriptions of three new species. Zootaxa. 2007;**1429**:1-38

[5] Yang CH, Bracken-Grissom H, Kim D, Crandall KA, Chan TY. Phylogenetic relationships, character evolution, and taxonomic implications within the slipper lobsters (Crustacea: Decapoda: Scyllaridae). Molecular Phylogenetics and Evolution. 2012;**62**(1):237-250

[6] Davis KE, Hesketh TW, Delmer C, Wills MA. Towards a supertree of Arthropoda: A species-level supertree of the spiny, slipper and coral lobsters (Decapoda: Achelata). PLoS ONE. 2015;**10**(10):e0140110. DOI: 10.1371/ journal.pone.0140110

[7] Spanier E, Lavalli KL. Slipper lobster fisheries—Present status and future perspectives. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster, Crustacean Issues 17. Vol. 2007. New York: CRC Press, Francis & Taylor Group; 2007. pp. 377-391

[8] Vijayakumaran M, Radhakrishnan EV. Slipper lobsters. In: Fotedar R, Phillips B, editors. Recent Advances and New Species in Aquaculture. Oxford, UK: Wiley-Blackwell; 2011. pp. 85-102

[9] Özcan T, Ateş AS, Bakir K, Katağan T. Commercial crustaceans on the Levantine Sea coast of Turkey. In: Turan C, Salihoğlu B, Özgür Özbek E, Öztürk B, editors. The Turkish Part of the Mediterranean Sea: Marine Biodiversity, Fisheries, Conservation and Governance. Turkish Marine Research Foundation (TUDAV), Publication No: 43; Istanbul, Turkey; 2016. 2016. pp. 392-406. Available from: http:// tudav.org/wp-content/uploads/2018/04/ MEDITERRANEAN\_SEA\_2016.pdf

[10] Alborés I, García-Soler C, Fernández L. Reproductive biology of the slipper lobster *Scyllarus arctus* in Galicia (NW Spain): Implications for fisheries management. Fisheries Research. 2019;**212**:1-11

[11] Fujii Y, Fujiwara T, Koide Y, Hasan I, Sugawara S, Rajia S, et al. Internalization of a novel, huge lectin from *Ibacus novemdentatus* (slipper lobster) induces apoptosis of mammalian cancer cells. Glycoconjugate Journal. 2017;**34**(1):85-94

[12] Patek SN, Feldmann RM, Porter M, Tshudy D. Phylogeny and evolution of lobsters. In: Phillips BF, editor. Lobsters: Biology, Management, Aquaculture and Fisheries. Oxford: Blackwell Publishing; 2006. pp. 113-145

[13] Bracken-Grissom HD, Ahyong ST, Wilkinson RD, Feldmann RM, Schweitzer CE, Breinholt JW, et al. The emergences of the lobsters: Phylogenetic relationships, morphological evolution and divergence time comparisons of an ancient group (Decapoda: Achelata, Astacidea, Glypheidea, Polychelidae). Systematic Biology. 2014;**63**:457-479

[14] Schweitzer CE, Feldmann RM. Lobster (Decapoda) diversity and evolutionary patterns through time. Journal of Crustacean Biology. 2014;**34**(6):820-847

[15] Nyborg T, Garassino A. A new genus of slipper lobster (Crustacea: Decapoda: Scyllaridae) from the Eocene of California and Oregon (USA). Neues Jahrbuch für Geologie und Paläontologie (Abhandlungen). 2017;**283**(3):309-316

[16] Audo D. First occurrence of Ibacinae (Eucrustacea: Decapoda: Scyllaridae) from the Eocene of Pakistan. Journal of Systematic Palaeontology. 2019;**17**(6):533-538

[17] Chan TY. Annotated checklist of the world's marine lobsters (Crustacea: Decapoda: Astacidea, Glypheidea, Achelata, Polychelida). The Raffles Bulletin of Zoology. 2010;**23**:153-181

[18] Lavalli KL, Spanier E. Introduction to the biology and fisheries of slipper lobsters. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 3-21

[19] Holthuis LB. A revision of the family Scyllaridae (Crustacea: Decapoda: Macrura). 1. Subfamily Ibacinae. Zoologische Verhandelingen. 1985;**218**:1-130

[20] Holthuis LB. The Indo-Pacific scyllarine lobsters (Crustacea, Decapoda, Scyllaridae). Zoosystema. 2002;**24**(3):499-683

[21] Wolfe JM, Breinholt JW, Crandall KA, Lemmon AR, Lemmon EM, Timm LE, et al. A phylogenomic framework, evolutionary timeline and genomic resources for comparative studies of decapod crustaceans. Proceedings of the Royal Society B. 2019;**286**(1901):20190079

[22] Genis-Armero R, Guerao G, Abelló P, Ignacio González-Gordillo J, Cuesta JA, Corbari L, et al. Possible amphi-Atlantic dispersal of *Scyllarus* lobsters (Crustacea: Scyllaridae):

Molecular and larval evidence. Zootaxa. 2017;**4306**(3):325-338

[23] Robertson RB. The larval development of some western Atlantic lobsters of the family Scyllaridae [thesis]. Coral Gables, Florida: University of Miami; 1968

[24] Robertson PB. The early larval development of the scyllarid lobster *Scyllarides aequinoctialis* (Lund) in the laboratory, with a revision of the larval characters of the genus. Deep-Sea Research. 1969;**16**:557-586

[25] Crosnier A. Naupliosoma, phyllosomes et pseudibacus de *Scyllarides herklotsi* (Herklots) (Crustacea, Decapoda, Scyllaridae) recoltes par l'ombango dans le sud du Golfe de Guinee. Cahiers O.R.S.T.O.M. Oceanographie. 1972;**10**:139-149

[26] Martins HR. Biological studies of the exploited stock of the Mediterranean locust lobster *Scyllarides latus* (Latreille, 1803) (Decapoda: Scyllaridae) in the Azores. Journal of Crustacean Biology. 1985;**5**(2):294-305

[27] Lesser JHR. Identification of early larvae of New Zealand spiny and shovelnosed lobsters (Decapoda, Palinuridae and Scyllaridae). Crustaceana. 1974;**27**:259-277

[28] Harada E. Notes on the naupliosoma and newly hatched phyllosoma of *Ibacus ciliatus* (Von Siebold). Publications of the Seto Marine Biological Laboratory. 1958;**7**:173-179

[29] Booth JD, Webber WR, Sekiguchi H, Coutures E. Diverse larval recruitment strategies within the Scyllaridae. New Zealand Journal of Marine and Freshwater Research. 2005;**39**:581-592

[30] Sekiguchi H, Booth JD, Webber WR. Early life histories of slipper lobsters. In: Lavalli KL, Spanier E,

**43**

*Scyllarid Lobster Biology and Ecology*

Group; 2007. pp. 69-90

1995. pp. 467-510

1994;**45**:925-944

1971;**19**:1-36

1971;**20**:77-103

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis

Bulletin of the Japanese Society of Scientific Fisheries. 1963;**29**:349-353

[39] Thomas LR. Phyllosoma larvae associated with medusae. Nature.

[40] Herrnkind WF, Halusky J, Kanciruk P. A further note on phyllosoma larvae associated with medusae. Bulletin of Marine Science. 1976;**26**:110-112

[41] Ates R, Lindsay DJ, Sekiguchi H. First record of an association between a phyllosoma larva and a prayid siphonophore. Plankton and Benthos

[42] Palero F, Guerao G, Clark PF, Abelló P. *Scyllarus arctus* (Crustacea: Decapoda: Scyllaridae) final stage phyllosoma identified by DNA analysis, with morphological description. Journal of the Marine Biological Association of the United Kingdom. 2011;**91**(2):485-492

[43] Wakabayashi K, Yang CH, Shy JY, He CH, Chan TY. Correct identification and redescription of the larval stages and early juveniles of the slipper lobster *Eduarctus martensii* (Pfeffer, 1881) (Decapoda: Scyllaridae). Journal of Crustacean Biology. 2017;**37**(2):204-219

[44] Mikami S, Takashima F. Development of the proventriculus in larvae of the slipper lobster, *Ibacus ciliatus* (Decapoda: Scyllaridae). Aquaculture. 1993;**116**:199-217

[45] Mikami S, Greenwood JG, Takashima F. Functional morphology and cytology of the phyllosomal digestive system *Ibacus ciliatus* and *Panulirus japonicus* (Decapoda, Scyllaridae and Palinuridae). Crustaceana. 1994;**67**:212-225

[46] Suzuki N, Murakami K, Takeyama H, Chow S. Molecular attempt to identify prey organisms of lobster phyllosoma larvae. Fishery Science.

2006;**72**:342-349

Research. 2007;**2**:66-69

1963;**198**:208

[31] Lavalli KL, Factor JR. The feeding apparatus. In: Factor JR, editor. The Biology of the Lobster, *Homarus americanus*. New York: Academic Press;

[32] Baisre JA. Phyllosoma larvae and the phylogeny of Palinuroidea (Crustacea: Decapoda): A review. Australian Journal of Marine and Freshwater Research.

[33] Johnson MW. The palinurid and scyllarid lobster larvae of the tropical eastern Pacific and their distribution as related to the prevailing hydrography. Bulletin of the Scripps Institute of Oceanography, University of California.

[34] Johnson MW. The phyllosoma larvae of slipper lobsters from the Hawaiian Islands and adjacent areas (Decapoda, Scyllaridae). Crustaceana.

[35] Yeung C, McGowan MF. Differences

in inshore-offshore and vertical distribution of phyllosoma larvae of *Panulirus*, *Scyllarus* and *Scyllarides* in the Florida keys in May–June, 1989. Bulletin of Marine Science. 1991;**49**:699-714

[36] Coutures E. Distribution of phyllosoma larvae of Scyllaridae and Palinuridae (Decapoda: Palinuridae) in the south-western lagoon of New Caledonia. Marine and Freshwater

Research. 2000;**51**:363-369

Oceanography. 2001;**57**:743

[37] Minami H, Inoue N, Sekiguchi H. Vertical distributions of phyllosoma larvae of palinurid and scyllarid lobsters in the western North Pacific. Journal of

[38] Shojima Y. Scyllarid phyllosomas' habit of accompanying the jelly-fish.

*Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

[15] Nyborg T, Garassino A. A new genus of slipper lobster (Crustacea: Decapoda: Scyllaridae) from the Eocene of California and Oregon (USA). Neues Jahrbuch für Geologie und Paläontologie (Abhandlungen). Molecular and larval evidence. Zootaxa.

development of some western Atlantic lobsters of the family Scyllaridae [thesis]. Coral Gables, Florida: University of Miami; 1968

[24] Robertson PB. The early larval development of the scyllarid lobster *Scyllarides aequinoctialis* (Lund) in the laboratory, with a revision of the larval characters of the genus. Deep-Sea

Research. 1969;**16**:557-586

1972;**10**:139-149

1985;**5**(2):294-305

1974;**27**:259-277

1958;**7**:173-179

[25] Crosnier A. Naupliosoma, phyllosomes et pseudibacus de *Scyllarides herklotsi* (Herklots) (Crustacea, Decapoda, Scyllaridae) recoltes par l'ombango dans le sud du Golfe de Guinee. Cahiers O.R.S.T.O.M. Oceanographie.

[26] Martins HR. Biological studies of the exploited stock of the Mediterranean locust lobster *Scyllarides latus* (Latreille, 1803) (Decapoda: Scyllaridae) in the Azores. Journal of Crustacean Biology.

[27] Lesser JHR. Identification of early larvae of New Zealand spiny and shovelnosed lobsters (Decapoda, Palinuridae

[28] Harada E. Notes on the naupliosoma and newly hatched phyllosoma of *Ibacus ciliatus* (Von Siebold). Publications of the Seto Marine Biological Laboratory.

[29] Booth JD, Webber WR, Sekiguchi H, Coutures E. Diverse larval recruitment strategies within the Scyllaridae. New Zealand Journal of Marine and Freshwater Research. 2005;**39**:581-592

[30] Sekiguchi H, Booth JD, Webber WR. Early life histories of slipper lobsters. In: Lavalli KL, Spanier E,

and Scyllaridae). Crustaceana.

2017;**4306**(3):325-338

[23] Robertson RB. The larval

[16] Audo D. First occurrence of Ibacinae (Eucrustacea: Decapoda: Scyllaridae)

Journal of Systematic Palaeontology.

[17] Chan TY. Annotated checklist of the world's marine lobsters (Crustacea: Decapoda: Astacidea, Glypheidea, Achelata, Polychelida). The Raffles Bulletin of Zoology. 2010;**23**:153-181

[18] Lavalli KL, Spanier E. Introduction to the biology and fisheries of slipper lobsters. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis

2017;**283**(3):309-316

2019;**17**(6):533-538

Group; 2007. pp. 3-21

1985;**218**:1-130

2002;**24**(3):499-683

2019;**286**(1901):20190079

P, Ignacio González-Gordillo J, Cuesta JA, Corbari L, et al. Possible amphi-Atlantic dispersal of *Scyllarus* lobsters (Crustacea: Scyllaridae):

[19] Holthuis LB. A revision of the family Scyllaridae (Crustacea: Decapoda: Macrura). 1. Subfamily Ibacinae. Zoologische Verhandelingen.

[20] Holthuis LB. The Indo-Pacific scyllarine lobsters (Crustacea, Decapoda, Scyllaridae). Zoosystema.

[21] Wolfe JM, Breinholt JW, Crandall KA, Lemmon AR, Lemmon EM, Timm LE, et al. A phylogenomic framework, evolutionary timeline and genomic resources for comparative studies of decapod crustaceans. Proceedings of the Royal Society B.

[22] Genis-Armero R, Guerao G, Abelló

from the Eocene of Pakistan.

**42**

editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 69-90

[31] Lavalli KL, Factor JR. The feeding apparatus. In: Factor JR, editor. The Biology of the Lobster, *Homarus americanus*. New York: Academic Press; 1995. pp. 467-510

[32] Baisre JA. Phyllosoma larvae and the phylogeny of Palinuroidea (Crustacea: Decapoda): A review. Australian Journal of Marine and Freshwater Research. 1994;**45**:925-944

[33] Johnson MW. The palinurid and scyllarid lobster larvae of the tropical eastern Pacific and their distribution as related to the prevailing hydrography. Bulletin of the Scripps Institute of Oceanography, University of California. 1971;**19**:1-36

[34] Johnson MW. The phyllosoma larvae of slipper lobsters from the Hawaiian Islands and adjacent areas (Decapoda, Scyllaridae). Crustaceana. 1971;**20**:77-103

[35] Yeung C, McGowan MF. Differences in inshore-offshore and vertical distribution of phyllosoma larvae of *Panulirus*, *Scyllarus* and *Scyllarides* in the Florida keys in May–June, 1989. Bulletin of Marine Science. 1991;**49**:699-714

[36] Coutures E. Distribution of phyllosoma larvae of Scyllaridae and Palinuridae (Decapoda: Palinuridae) in the south-western lagoon of New Caledonia. Marine and Freshwater Research. 2000;**51**:363-369

[37] Minami H, Inoue N, Sekiguchi H. Vertical distributions of phyllosoma larvae of palinurid and scyllarid lobsters in the western North Pacific. Journal of Oceanography. 2001;**57**:743

[38] Shojima Y. Scyllarid phyllosomas' habit of accompanying the jelly-fish.

Bulletin of the Japanese Society of Scientific Fisheries. 1963;**29**:349-353

[39] Thomas LR. Phyllosoma larvae associated with medusae. Nature. 1963;**198**:208

[40] Herrnkind WF, Halusky J, Kanciruk P. A further note on phyllosoma larvae associated with medusae. Bulletin of Marine Science. 1976;**26**:110-112

[41] Ates R, Lindsay DJ, Sekiguchi H. First record of an association between a phyllosoma larva and a prayid siphonophore. Plankton and Benthos Research. 2007;**2**:66-69

[42] Palero F, Guerao G, Clark PF, Abelló P. *Scyllarus arctus* (Crustacea: Decapoda: Scyllaridae) final stage phyllosoma identified by DNA analysis, with morphological description. Journal of the Marine Biological Association of the United Kingdom. 2011;**91**(2):485-492

[43] Wakabayashi K, Yang CH, Shy JY, He CH, Chan TY. Correct identification and redescription of the larval stages and early juveniles of the slipper lobster *Eduarctus martensii* (Pfeffer, 1881) (Decapoda: Scyllaridae). Journal of Crustacean Biology. 2017;**37**(2):204-219

[44] Mikami S, Takashima F. Development of the proventriculus in larvae of the slipper lobster, *Ibacus ciliatus* (Decapoda: Scyllaridae). Aquaculture. 1993;**116**:199-217

[45] Mikami S, Greenwood JG, Takashima F. Functional morphology and cytology of the phyllosomal digestive system *Ibacus ciliatus* and *Panulirus japonicus* (Decapoda, Scyllaridae and Palinuridae). Crustaceana. 1994;**67**:212-225

[46] Suzuki N, Murakami K, Takeyama H, Chow S. Molecular attempt to identify prey organisms of lobster phyllosoma larvae. Fishery Science. 2006;**72**:342-349

[47] Gopakumar G, Madhu K, Jayashankar R, Madhu R, Kizhakudan JK, Jose J, et al. Live feed research for larviculture of marine finfish and shellfish. Marine Fisheries Information Service India, T&E Series. 2008;**197**:1-6

[48] Wakabayashi K, Sato R, Ishii H, Akiba T, Nogata Y, Tanaka Y. Culture of phyllosomas of *Ibacus novemdentatus* (Decapoda: Scyllaridae) in a closed recirculating system using jellyfish as food. Aquaculture. 2012;**330**:162-166

[49] Wakabayashi K, Nagai S, Tanaka Y. The complete larval development of *Ibacus ciliatus* from hatching to the nisto and juvenile stages using jellyfish as the sole diet. Aquaculture. 2016;**450**:102-107

[50] Wakabayashi K, Sato H, Yoshie-Stark Y, Ogushi M, Tanaka Y. Differences in the biochemical compositions of two dietary jellyfish species and their effects on the growth and survival of *Ibacus novemdentatus* phyllosomas. Aquaculture Nutrition. 2016;**22**(1):25-33

[51] Wakabayashi K, Phillips BF. Morphological descriptions of laboratory reared larvae and postlarvae of the Australian shovel-nosed lobster *Thenus australiensis* Burton & Davie, 2007 (Decapoda, Scyllaridae). Crustaceana. 2016;**89**(1):97-117

[52] Kamio M, Wakabayashi K, Nagai H, Tanaka Y. Phyllosomas of smooth fan lobsters (*Ibacus novemdentatus*) encase jellyfish cnidae in peritrophic membranes in their feces. Plankton and Benthos Research. 2016;**11**(3):100. DOI: 10.3800/pbr.11.100

[53] Wakabayashi K, Sato R, Hirai A, Ishii H, Akiba T, Tanaka Y. Predation by the phyllosoma larva of *Ibacus novemdentatus* on various kinds of venomous jellyfish. The Biological Bulletin. 2012;**222**(1):1-5

[54] Kamio M, Furukawa D, Wakabayashi K, Hiei K, Yano H, Sato H, et al. Grooming behavior by elongated third maxillipeds of phyllosoma larvae of the smooth fan lobster riding on jellyfishes. Journal of Experimental Marine Biology and Ecology. 2015;**463**:115-124

[55] Lyons WG. Scyllarid lobsters (Crustacea, Decapoda). Florida Marine Research Laboratory, Memoirs of the Hourglass Cruises. 1970;**1**(4):1-74

[56] Webber WR, Booth JD. Larval stages, developmental ecology, and distribution of *Scyllarus* sp. Z (probably *Scyllarus aoteanus* Powell, 1949) (Decapoda: Scyllaridae). New Zealand Journal of Marine and Freshwater Research. 2001;**35**(5):1025-1056

[57] Johnston D. Feeding morphology and digestive system of slipper lobsters. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. New York: CRC Press; 2007. pp. 111-132

[58] Williamson DI. Names of larvae in the Decapoda and Euphausiacea. Crustaceana. 1969;**16**:210-213

[59] Kizhakudan JK. Culture potential of the *Thenus orientalis* sand lobster (Lund). In: Kurup BM, Ravindran K, editors. Sustain Fish. Cochin, India: School of Industrial Fisheries, Cochin University of Science & Technology; 2006. pp. 256-263

[60] Atkinson JM, Boustead NC. The complete larval development of the scyllarid lobster *Ibacus alticrenatus* bate, 1888 in New Zealand waters. Crustaceana. 1982;**42**:275-287

[61] Stewart J, Kennelly SJ. Fecundity and egg-size of the Balmain bug *Ibacus peronii* (Leach, 1815) (Decapoda, Scyllaridae) off the east coast of Australia. Crustaceana. 1997;**70**:191-197

**45**

*Scyllarid Lobster Biology and Ecology*

2006. pp. 462-496

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC

[70] Bianchini M, Bono G, Ragonese S. Long-term recaptures and growth of slipper lobsters, *Scyllarides latus*, in the strait of Sicily (Mediterranean Sea). Crustaceana. 2001;**74**(7):673-680

S. Behavioural observations on slipper lobster *Scyllarides latus* (Latreille 1803) (Decapoda, Scyllaridae) reared in laboratory. In: Proceedings of the 6th Colloquium Crustacea Decapoda Mediterranea, Florence; 12-15 September 1996. pp. 25-26

[72] Spanier E, Lavalli KL. Natural history of *Scyllarides latus* (Crustacea:

contemporary biological knowledge of the Mediterranean slipper lobster. Journal of Natural History.

[73] Bianchini ML, Ragonese S. Growth

of slipper lobsters of the genus *Scyllarides*. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis

[74] Almog-Shtayer G. Behaviouralecological aspects of Mediterranean lobsters in the past and of the slipper lobster, *Scyllarides latus*, in the present [thesis]. Israel: University of Haifa; 1988

[75] DeMartini EE, Williams HA. Fecundity and egg size of *Scyllarides squammosus* (Decapoda: Scyllaridae) at Mare Reef, Northwestern Hawaiian Islands. Journal of Crustacean Biology.

[76] Lima FA, Martinelli-Lemos JM, Silva KC, Klautau AG, Cintra IH. Population structure and fecundity of *Scyllarides delfosi* Holthuis,

2001;**21**:891-896

Group; 2007. pp. 199-220

Decapoda): A review of the

1998;**32**(6):1769-1786

Press; 2007. pp. 91-110

[71] Chessa LA, Pais A, Serra

[63] Spanier E, Lavalli KL. First record of an early benthic juvenile likely to be that of the Mediterranean slipper lobster, *Scyllarides latu*s (Latreille, 1802). Crustaceana. 2013;**86**(3):259-267

[64] Anastasopoulou A, Mytilineou C,

Smith CJ, Papadopoulou KN. Crustacean prey in the diet of fishes from deep waters of the Eastern Ionian Sea. Journal of the Marine Biological Association of the United Kingdom.

[65] Hearn A. Evaluación de las poblaciones de langostas en la Reserva Marina de Galápagos. Informe Final 2002-2004. Fundación Charles Darwin y Dirección Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador; 2004

[66] Hearn A, Toral-Granda V, Martinez C, Reck G. Biology and fishery of the Galápagos slipper lobster. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press (Taylor & Francis Group); 2007.

[67] Rudloe A. Preliminary studies of the mariculture potential of the slipper lobster, *Scyllarides nodifer*. Aquaculture.

[68] Haddy JA, Stewart J, Graham KJ. Fishery and biology of commercially exploited Australian fan lobsters (*Ibacus* spp.). In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group;

[69] Mikami S, Kuballa AV. Larvae and larval rearing of scyllarids. In: Lavalli

2019;**99**(1):259-267

pp. 287-308

1983;**34**:165-169

2007. pp. 359-373

[62] Spanier E, Lavalli KL. *Scyllarides* spp. In: Phillips BF, editor. Lobsters: Biology Management, Aquaculture and Fisheries Part 2: Lobsters of Commercial Importance. Oxford, UK: Blackwell;

#### *Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

[47] Gopakumar G, Madhu K,

Jayashankar R, Madhu R, Kizhakudan JK, Jose J, et al. Live feed research for larviculture of marine finfish and shellfish. Marine Fisheries Information Service India, T&E Series. 2008;**197**:1-6 [54] Kamio M, Furukawa D,

[55] Lyons WG. Scyllarid lobsters (Crustacea, Decapoda). Florida Marine Research Laboratory, Memoirs of the Hourglass Cruises. 1970;**1**(4):1-74

[56] Webber WR, Booth JD. Larval stages, developmental ecology, and distribution of *Scyllarus* sp. Z (probably

*Scyllarus aoteanus* Powell, 1949) (Decapoda: Scyllaridae). New Zealand Journal of Marine and Freshwater Research. 2001;**35**(5):1025-1056

[57] Johnston D. Feeding morphology and digestive system of slipper lobsters. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. New York: CRC Press; 2007.

[58] Williamson DI. Names of larvae in the Decapoda and Euphausiacea. Crustaceana. 1969;**16**:210-213

[59] Kizhakudan JK. Culture potential of the *Thenus orientalis* sand lobster (Lund). In: Kurup BM, Ravindran K, editors. Sustain Fish. Cochin, India: School of Industrial Fisheries, Cochin University of Science & Technology;

[60] Atkinson JM, Boustead NC. The complete larval development of the scyllarid lobster *Ibacus alticrenatus* bate, 1888 in New Zealand waters. Crustaceana. 1982;**42**:275-287

[61] Stewart J, Kennelly SJ. Fecundity and egg-size of the Balmain bug *Ibacus peronii* (Leach, 1815)

(Decapoda, Scyllaridae) off the east coast of Australia. Crustaceana.

2015;**463**:115-124

pp. 111-132

2006. pp. 256-263

1997;**70**:191-197

Wakabayashi K, Hiei K, Yano H, Sato H, et al. Grooming behavior by elongated third maxillipeds of phyllosoma larvae of the smooth fan lobster riding on jellyfishes. Journal of Experimental Marine Biology and Ecology.

[48] Wakabayashi K, Sato R, Ishii H,

Scyllaridae) in a closed recirculating system using jellyfish as food. Aquaculture. 2012;**330**:162-166

[49] Wakabayashi K, Nagai S, Tanaka Y. The complete larval development of *Ibacus ciliatus* from hatching to the nisto and juvenile stages using jellyfish as the sole diet. Aquaculture.

[50] Wakabayashi K, Sato H, Yoshie-Stark Y, Ogushi M, Tanaka Y. Differences in the biochemical compositions of two dietary jellyfish species and their effects on the growth and survival of *Ibacus novemdentatus* phyllosomas. Aquaculture Nutrition.

[51] Wakabayashi K, Phillips BF. Morphological descriptions of laboratory reared larvae and postlarvae of the Australian shovel-nosed lobster *Thenus australiensis* Burton & Davie, 2007 (Decapoda, Scyllaridae). Crustaceana. 2016;**89**(1):97-117

[52] Kamio M, Wakabayashi K, Nagai H, Tanaka Y. Phyllosomas of smooth fan lobsters (*Ibacus novemdentatus*) encase jellyfish cnidae in peritrophic membranes in their feces. Plankton and Benthos Research. 2016;**11**(3):100. DOI:

[53] Wakabayashi K, Sato R, Hirai A, Ishii H, Akiba T, Tanaka Y. Predation by the phyllosoma larva of *Ibacus novemdentatus* on various kinds of venomous jellyfish. The Biological

Akiba T, Nogata Y, Tanaka Y. Culture of phyllosomas of *Ibacus novemdentatus* (Decapoda:

2016;**450**:102-107

2016;**22**(1):25-33

10.3800/pbr.11.100

Bulletin. 2012;**222**(1):1-5

**44**

[62] Spanier E, Lavalli KL. *Scyllarides* spp. In: Phillips BF, editor. Lobsters: Biology Management, Aquaculture and Fisheries Part 2: Lobsters of Commercial Importance. Oxford, UK: Blackwell; 2006. pp. 462-496

[63] Spanier E, Lavalli KL. First record of an early benthic juvenile likely to be that of the Mediterranean slipper lobster, *Scyllarides latu*s (Latreille, 1802). Crustaceana. 2013;**86**(3):259-267

[64] Anastasopoulou A, Mytilineou C, Smith CJ, Papadopoulou KN. Crustacean prey in the diet of fishes from deep waters of the Eastern Ionian Sea. Journal of the Marine Biological Association of the United Kingdom. 2019;**99**(1):259-267

[65] Hearn A. Evaluación de las poblaciones de langostas en la Reserva Marina de Galápagos. Informe Final 2002-2004. Fundación Charles Darwin y Dirección Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador; 2004

[66] Hearn A, Toral-Granda V, Martinez C, Reck G. Biology and fishery of the Galápagos slipper lobster. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press (Taylor & Francis Group); 2007. pp. 287-308

[67] Rudloe A. Preliminary studies of the mariculture potential of the slipper lobster, *Scyllarides nodifer*. Aquaculture. 1983;**34**:165-169

[68] Haddy JA, Stewart J, Graham KJ. Fishery and biology of commercially exploited Australian fan lobsters (*Ibacus* spp.). In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 359-373

[69] Mikami S, Kuballa AV. Larvae and larval rearing of scyllarids. In: Lavalli

KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press; 2007. pp. 91-110

[70] Bianchini M, Bono G, Ragonese S. Long-term recaptures and growth of slipper lobsters, *Scyllarides latus*, in the strait of Sicily (Mediterranean Sea). Crustaceana. 2001;**74**(7):673-680

[71] Chessa LA, Pais A, Serra S. Behavioural observations on slipper lobster *Scyllarides latus* (Latreille 1803) (Decapoda, Scyllaridae) reared in laboratory. In: Proceedings of the 6th Colloquium Crustacea Decapoda Mediterranea, Florence; 12-15 September 1996. pp. 25-26

[72] Spanier E, Lavalli KL. Natural history of *Scyllarides latus* (Crustacea: Decapoda): A review of the contemporary biological knowledge of the Mediterranean slipper lobster. Journal of Natural History. 1998;**32**(6):1769-1786

[73] Bianchini ML, Ragonese S. Growth of slipper lobsters of the genus *Scyllarides*. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 199-220

[74] Almog-Shtayer G. Behaviouralecological aspects of Mediterranean lobsters in the past and of the slipper lobster, *Scyllarides latus*, in the present [thesis]. Israel: University of Haifa; 1988

[75] DeMartini EE, Williams HA. Fecundity and egg size of *Scyllarides squammosus* (Decapoda: Scyllaridae) at Mare Reef, Northwestern Hawaiian Islands. Journal of Crustacean Biology. 2001;**21**:891-896

[76] Lima FA, Martinelli-Lemos JM, Silva KC, Klautau AG, Cintra IH. Population structure and fecundity of *Scyllarides delfosi* Holthuis,

1960 (Scyllaridae) on the Amazon continental shelf. Crustaceana. 2018;**91**(9):1027-1103

[77] Almeida Duarte LFD, Severino-Rodrigues E, Pinheiro MA, Gasalla MA. Slipper lobsters (Scyllaridae) off the southeastern coast of Brazil: Relative growth, population structure, and reproductive biology. Fishery Bulletin. 2015;**113**:55-68

[78] Bianchini ML, Ragonese S. *In ovo* embryonic development of the Mediterranean slipper lobster, *Scyllarides latus*. The Lobster Newsletter. 2003;**16**:10-12

[79] Spanier E, Tom M, Pisanty S, Almog G. Seasonality and shelter selection by the slipper lobster *Scyllarides latus* in the southeastern Mediterranean. Marine Ecology Progress Series. 1988;**42**:247-255

[80] Stewart J, Kennelly SJ. Growth of the scyllarid lobsters *Ibacus peronii* and *I. chacei*. Marine Biology. 2000;**136**:921-930

[81] Sharp WC, Hunt JH, Teehan WH. Observations on the ecology of *Scyllarides aequinoctialis, Scyllarides nodifer*, and *Parribacus antarcticus* and a description of the Florida scyllarid lobster fishery. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster*.* Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 231-242

[82] Kagwade PV, Kabli LM. Age and growth of the sand lobster *Thenus orientalis* (Lund) from Bombay waters. Indian Journal of Fisheries. 1996;**43**(3):241-247

[83] Jones CM. Biology and fishery of the bay lobster, *Thenus* spp. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster*.* Crustacean Issues 17. New York: CRC Press; 2007. pp. 325-358

[84] Radhakrishnan EV, Manisseri MK, Deshmukh VD. Biology and fishery of the slipper lobster, *Thenus orientalis,* in India. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster*.* Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 309-324

[85] Subramanian VT. Fishery of sand lobster *Thenus orientalis* (Lund) along Chennai coast. Indian Journal of Fisheries. 2004;**51**(1):111-115

[86] Faria J, Froufe E, Tuya F, Alexandrino P, Pérez-Losada M. Panmixia in the endangered slipper lobster *Scyllarides latus* from the northeastern Atlantic and western Mediterranean. Journal of Crustacean Biology. 2013;**33**(4):557-566

[87] Lerosey-Aubril R, Meyer R. The sensory dorsal organs of crustaceans. Biological Reviews. 2013;**88**(2):406-426

[88] Johnston DJ, Alexander CG. Functional morphology of the mouthparts and alimentary tract of the slipper lobster *Thenus orientalis* (Decapoda: Scyllaridae). Marine and Freshwater Research. 1999;**50**:213-223

[89] Suthers IM, Anderson DT. Functional morphology of mouthparts and gastric mill of *Ibacus peronii* (leach) (Palinura: Scyllaridae). Australian Journal of Maine and Freshwater Research. 1981;**32**:931-944

[90] Lau CJ. Feeding behavior of the Hawaiian slipper lobster, *Scyllarides squammosus*, with review of decapod crustacean feeding tactics on molluscan prey. Bulletin of Marine Science. 1987;**41**:378-391

[91] Spanier E. Mollusca as food for the slipper lobster *Scyllarides latus* in the coastal waters of Israel. Levant. 1987;**68**:713-716

[92] Lavalli KL, Malcom CN, Goldstein JS. Description of pereiopod setae

**47**

*Scyllarid Lobster Biology and Ecology*

of scyllarid lobsters, *Scyllarides aequinoctialis, Scyllarides latus*, and *Scyllarides nodifer*, with observations on the feeding during consumption of bivalves and gastropods. Bulletin of Marine Science. 2018;**94**(3):571-601

[93] Martínez CE. Ecología trófica de *Panulirus gracilis*, *P. penicillatus* y *Scyllarides astori* (Decapoda, Palinura) en sitios de pesca de langosta en las islas Galápagos [thesis]. Ecuador: Universidad del Azuay; 2000. 102 pp

[94] Ogren LH. Concealment behaviour of the Spanish lobster, *Scyllarides nodifer* (Stimpson), with observations on its diel activity. Northeast Gulf Science.

[95] Barr L. Some aspects of the life history, ecology and behaviour of the lobsters of the Galápagos Islands. Stanford Oceanographic Expedition.

[96] Martínez CE, Toral V, Edgar G. Langostino. In: Danulat E, Edgar GJ, editors. Reserva Marina de Galápagos, Línea Base de la Biodiversidad. Fundación Charles Darwin y Servicio Parque Nacional Galápagos; Santa Cruz, Galápagos, Ecuador; 2002. pp. 216-232

[97] Goldstein JS, Spanier E. In the heat of the moment: Effects of elevated temperature on seasonal movements in slipper lobsters (*Scyllarides latus*) in the

*Scyllarides latus*? Marine and Freshwater

eastern Mediterranean. In prep.

[98] Lavalli KL, Spanier E. Does gregariousness function as an antipredator mechanism in the Mediterranean slipper lobster,

Research. 2001;**52**:1133-1143

[99] Moe MA Jr. Lobsters: Florida, Bahamas, the Caribbean. Plantation, FL: Green Turtle Publications; 1991. 510 pp

[100] Hardwick CW Jr, Cline CB. Reproductive status, sex ratios

1977;**1**(2):115-116

1968;**17**:254-262

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

and morphometrics of the slipper lobster *Scyllarides nodifer* (Stimpson) (Decapoda: Scyllaridae) in the

Gulf Science. 1990;**11**(2):131-136

Biology. 2006;**26**(1):69-72

Marine Biology and Ecology.

Shelter preferences in the

Ecology. 1992;**164**:103-116

[103] Spanier E, Almog-Shtayer G.

[104] Spanier E, Almog-Shtayer G, Fiedler U. The Mediterranean slipper lobster *Scyllarides latus*: The known and the unknown. Bios. 1993;**1**(1):49-58

[105] Barshaw DE, Spanier E. The

slipper lobster, *Scyllarides latus* Decapoda. Scyllaridae. Crustaceana.

[106] Barshaw DE, Spanier E. Anti-predator behaviours of the

*latus*. Bulletin of Marine Science.

1994;**67**(2):187-197

1994;**55**(2):375-382

Series. 2003;**256**:171-182

undiscovered lobster—A first look at the social behaviour of the Mediterranean

Mediterranean slipper lobster *Scyllarides* 

[107] Barshaw DE, Lavalli KL, Spanier E. Is offence the best defence: The response of three morphological types of lobsters to predation. Marine Ecology Progress

[108] Lavalli KL, Spanier E, Grasso F. Behavior and sensory biology of slipper lobsters. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the

Mediterranean slipper lobster: Effects of physical properties. Journal of Experimental Marine Biology and

1991;**145**:15-31

[101] Faulkes Z. Digging mechanisms and substrate preferences of shovel nosed lobsters, *Ibacus peroni* (Decapoda: Scyllaridae). Journal of Crustacean

Northeastern Gulf of Mexico. Northeast

[102] Spanier E, Weihs D, Almog-Shtayer G. Swimming of the Mediterranean slipper lobster. Journal of Experimental

*Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

1960 (Scyllaridae) on the Amazon continental shelf. Crustaceana.

[84] Radhakrishnan EV, Manisseri MK, Deshmukh VD. Biology and fishery of the slipper lobster, *Thenus orientalis,* in India. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster*.* Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group;

[85] Subramanian VT. Fishery of sand lobster *Thenus orientalis* (Lund) along Chennai coast. Indian Journal of Fisheries. 2004;**51**(1):111-115

[86] Faria J, Froufe E, Tuya F, Alexandrino P, Pérez-Losada M. Panmixia in the endangered slipper lobster *Scyllarides latus* from the northeastern Atlantic and western Mediterranean. Journal of Crustacean

Biology. 2013;**33**(4):557-566

[87] Lerosey-Aubril R, Meyer R.

[88] Johnston DJ, Alexander CG. Functional morphology of the mouthparts and alimentary tract of the slipper lobster *Thenus orientalis* (Decapoda: Scyllaridae). Marine and Freshwater Research. 1999;**50**:213-223

The sensory dorsal organs of crustaceans. Biological Reviews. 2013;**88**(2):406-426

[89] Suthers IM, Anderson DT. Functional morphology of mouthparts and gastric mill of *Ibacus peronii* (leach) (Palinura: Scyllaridae). Australian Journal of Maine and Freshwater Research. 1981;**32**:931-944

[90] Lau CJ. Feeding behavior of the Hawaiian slipper lobster, *Scyllarides squammosus*, with review of decapod crustacean feeding tactics on molluscan prey. Bulletin of Marine Science.

[91] Spanier E. Mollusca as food for the slipper lobster *Scyllarides latus* in the coastal waters of Israel. Levant.

[92] Lavalli KL, Malcom CN, Goldstein JS. Description of pereiopod setae

1987;**41**:378-391

1987;**68**:713-716

2007. pp. 309-324

[77] Almeida Duarte LFD, Severino-Rodrigues E, Pinheiro MA, Gasalla MA. Slipper lobsters (Scyllaridae) off the southeastern coast of Brazil: Relative growth, population structure, and reproductive biology. Fishery Bulletin.

[78] Bianchini ML, Ragonese S. *In ovo* embryonic development of the Mediterranean slipper lobster, *Scyllarides latus*. The Lobster Newsletter.

[79] Spanier E, Tom M, Pisanty S, Almog G. Seasonality and shelter selection by the slipper lobster *Scyllarides latus* in the southeastern Mediterranean. Marine Ecology Progress Series.

[80] Stewart J, Kennelly SJ. Growth of the scyllarid lobsters *Ibacus peronii* and *I. chacei*. Marine Biology.

[81] Sharp WC, Hunt JH, Teehan WH. Observations on the ecology of *Scyllarides aequinoctialis, Scyllarides nodifer*, and *Parribacus antarcticus* and a description of the Florida scyllarid lobster fishery. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster*.* Crustacean Issues 17. New York: CRC Press, Taylor & Francis

Group; 2007. pp. 231-242

1996;**43**(3):241-247

Press; 2007. pp. 325-358

[82] Kagwade PV, Kabli LM. Age and growth of the sand lobster *Thenus orientalis* (Lund) from Bombay waters. Indian Journal of Fisheries.

[83] Jones CM. Biology and fishery of the bay lobster, *Thenus* spp. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster*.* Crustacean Issues 17. New York: CRC

2018;**91**(9):1027-1103

2015;**113**:55-68

2003;**16**:10-12

1988;**42**:247-255

2000;**136**:921-930

**46**

of scyllarid lobsters, *Scyllarides aequinoctialis, Scyllarides latus*, and *Scyllarides nodifer*, with observations on the feeding during consumption of bivalves and gastropods. Bulletin of Marine Science. 2018;**94**(3):571-601

[93] Martínez CE. Ecología trófica de *Panulirus gracilis*, *P. penicillatus* y *Scyllarides astori* (Decapoda, Palinura) en sitios de pesca de langosta en las islas Galápagos [thesis]. Ecuador: Universidad del Azuay; 2000. 102 pp

[94] Ogren LH. Concealment behaviour of the Spanish lobster, *Scyllarides nodifer* (Stimpson), with observations on its diel activity. Northeast Gulf Science. 1977;**1**(2):115-116

[95] Barr L. Some aspects of the life history, ecology and behaviour of the lobsters of the Galápagos Islands. Stanford Oceanographic Expedition. 1968;**17**:254-262

[96] Martínez CE, Toral V, Edgar G. Langostino. In: Danulat E, Edgar GJ, editors. Reserva Marina de Galápagos, Línea Base de la Biodiversidad. Fundación Charles Darwin y Servicio Parque Nacional Galápagos; Santa Cruz, Galápagos, Ecuador; 2002. pp. 216-232

[97] Goldstein JS, Spanier E. In the heat of the moment: Effects of elevated temperature on seasonal movements in slipper lobsters (*Scyllarides latus*) in the eastern Mediterranean. In prep.

[98] Lavalli KL, Spanier E. Does gregariousness function as an antipredator mechanism in the Mediterranean slipper lobster, *Scyllarides latus*? Marine and Freshwater Research. 2001;**52**:1133-1143

[99] Moe MA Jr. Lobsters: Florida, Bahamas, the Caribbean. Plantation, FL: Green Turtle Publications; 1991. 510 pp

[100] Hardwick CW Jr, Cline CB. Reproductive status, sex ratios

and morphometrics of the slipper lobster *Scyllarides nodifer* (Stimpson) (Decapoda: Scyllaridae) in the Northeastern Gulf of Mexico. Northeast Gulf Science. 1990;**11**(2):131-136

[101] Faulkes Z. Digging mechanisms and substrate preferences of shovel nosed lobsters, *Ibacus peroni* (Decapoda: Scyllaridae). Journal of Crustacean Biology. 2006;**26**(1):69-72

[102] Spanier E, Weihs D, Almog-Shtayer G. Swimming of the Mediterranean slipper lobster. Journal of Experimental Marine Biology and Ecology. 1991;**145**:15-31

[103] Spanier E, Almog-Shtayer G. Shelter preferences in the Mediterranean slipper lobster: Effects of physical properties. Journal of Experimental Marine Biology and Ecology. 1992;**164**:103-116

[104] Spanier E, Almog-Shtayer G, Fiedler U. The Mediterranean slipper lobster *Scyllarides latus*: The known and the unknown. Bios. 1993;**1**(1):49-58

[105] Barshaw DE, Spanier E. The undiscovered lobster—A first look at the social behaviour of the Mediterranean slipper lobster, *Scyllarides latus* Decapoda. Scyllaridae. Crustaceana. 1994;**67**(2):187-197

[106] Barshaw DE, Spanier E. Anti-predator behaviours of the Mediterranean slipper lobster *Scyllarides latus*. Bulletin of Marine Science. 1994;**55**(2):375-382

[107] Barshaw DE, Lavalli KL, Spanier E. Is offence the best defence: The response of three morphological types of lobsters to predation. Marine Ecology Progress Series. 2003;**256**:171-182

[108] Lavalli KL, Spanier E, Grasso F. Behavior and sensory biology of slipper lobsters. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 133-181

[109] Zimmer-Faust RK, Spanier E. Gregariousness and sociality in spiny lobsters: Implications for den habitations. Journal of Experimental Marine Biology and Ecology. 1987;**105**:57-71

[110] Spanier E, Zimmer-Faust RK. Some physical properties of shelter that influence den preference in spiny lobsters. Journal of Experimental Marine Biology and Ecology. 1988;**122**:137-149

[111] Lozano-Alvarez E, Spanier E. Behavior and growth of captive sub-adults spiny lobsters, *Panulirus argus,* under the risk of predation. Marine and Freshwater Research. 1997;**48**(8):707-713

[112] Herrnkind WF, Childress MJ, Lavalli KL. Defense coordination and other benefits among exposed spiny lobsters: Inferences from mass migratory and mesocosm studies of group size and behavior. Marine and Freshwater Research. 2001;**52**:1133-1143

[113] Hamilton WD. Geometry for the selfish herd. Journal of Theoretical Biology. 1971;**31**:294-311

[114] Horne FR, Tarsitano SF. The mineralization and biomechanics of the exoskeleton. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis Group; 2007. pp. 183-198

[115] Tarsitano SF, Lavalli KL, Horne F, Spanier E. The constructional properties of the exoskeleton of homarid, scyllarid, and palinurid lobsters. Hydrobiologia. 2006;**557**:9-20

[116] Smale MJ, Goosen AJJ. Reproduction and feeding of spotted gully shark, *Triakis megalopterus*, off the Eastern Cape, South Africa. Fishery Bulletin. 1999;**97**:987-998

[117] Barreiros JP, Santos RS. Notes on the food habits and predatory behaviour of the dusky grouper, *Epinephelus marginatus* (Lowe, 1834) (Pisces: Serranidae) in the Azores. Arquipelago Life and Marine Sciences. 1998;**16A**:29-35

[118] Mizrahi M, Chapman JK, Gough CLA, Humber F, Anderson LG. Management implications of the influence of biological variability of invasive lionfish diet in Belize. Management. 2017;**8**(1):61-70

[119] Oliveira G, Freire AS, Bertuol PRK. Reproductive biology of the slipper lobster *Scyllarides deceptor* (Decapoda: Scyllaridae) along the southern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom. 2008;**88**:1433-1440

[120] DeMartini EE, McCracken ML, Moffitt RB, Wetherall JA. Relative pleopod length as an indicator of size at sexual maturity in slipper (*Scyllarides squammosus*) and spiny Hawaiian (*Panulirus marginatus*) lobsters. Fishery Bulletin. 2005;**103**:23-33

[121] Kizhakudan JK, Thirumilu P, Rajapackiam S, Manibal C. Captive breeding and seed production of scyllarid lobsters—Opening new vistas in crustacean aquaculture. Marine Fisheries Information Service India, T & E Series. 2004;**181**:1-4

[122] Goldstein JS, Dubofsky EA, Spanier E. Into a rhythm: Diel activity patterns and behaviour in Mediterranean slipper lobsters, *Scyllarides latus*. ICES Journal of Marine Science. 2015;**72**(Suppl. 1):i147-i154

[123] O'Malley JM, Walsh WA. Annual and long-term movement patterns of spiny lobster, *Panulirus marginatus*, and

**49**

*Scyllarid Lobster Biology and Ecology*

in the Northwestern Hawaiian islands. Bulletin of Marine Science.

[125] Neil DM, Ansel AD. The

2013;**89**(2):529-549

1995;**75**:55-70

Fisheries. 1985;**44**:35-37

Ecology. 1986;**101**:85-89

2004;**33**:113-123

1992;**5**(1):8-9

[127] Jacklyn PM, Ritz DA. Hydrodynamics of swimming in scyllarid lobsters. Journal of Experimental Marine Biology and

*DOI: http://dx.doi.org/10.5772/intechopen.88218*

slipper lobster, *Scyllarides squammosus*,

Management; 8-13 February 2004;

potenzialità del ripoplamento attivo per la magnosa, Scyllarides latus (*Crostacei Decapodi*). Final report to MiRAAF

[134] Perry LT. Relationships between culture conditions and moult death syndrome (MDS) in larval development of the bay lobsters *Thenus orientalis* (Lund, 1793) and *Thenus indicus* Leach, 1815 (Decapoda: Scyllaridae) [thesis]. School of Biological Sciences, University

[135] Wakabayashi K, Otake S, Tanaka Y, Nagasawa K. *Choniomyzon inflatus* n. sp. (Crustacea: Copepoda: Nicothoidae) associated with *Ibacus novemdentatus* (Crustacea: Decapoda: Scyllaridae) from Japanese waters. Systematic Parasitology. 2013;**84**(2):157-165

[136] WWF. 2015. Living Blue Planet Report. Species, habitats and human well-being. In: Tanzer J, Phua C, Lawrence A, Gonzales A, Roxburgh T, Gamblin P, editors. WWF, Gland, Switzerland. Available from: https:// www.wwf.de/fileadmin/fm-wwf/ Publikationen-PDF/Living-Blue-Planet-

[137] Gillespie KM, Vincent AC. Tropical invertebrate response to marine reserves varies with protection duration, habitat type, and exploitation history. Aquatic Conservation: Marine and Freshwater Ecosystems. 2019;**29**(3):511-520

[138] Miller E, Spanier E, Yahel R, Diamant R. Do marine nature reserves enhance the conservation

Tasmania, Australia. p. 61

(Pesca Marittima); 1997; 1

[133] Newell IM. A parasitic species of *Copidognathus* (Acari: Halacaridae). Proceedings of the Hawaiin Entomollogical Society.

1956;**16**(1):122-125

of Queensland; 2001

Report-2015.pdf

[132] Bianchini ML, Raisa PF. Valutazione della fattibilità e

[124] Stewart J, Kennelly SJ. Contrasting movements of two exploited Scyllarid lobsters of the genus *Ibacus* off the east coast of Australia. Fisheries Research. 1998;**2-3**:127-132. DOI: 10.1016/ S0165-7836(98)00104-0

orientation of tail-flip escape swimming in decapod and mysid crustaceans. Journal of the Marine Biological Association of the United Kingdom.

[126] Ritz DA, Jacklyn PM. Believe it or not—Bugs fly through water. Australian

[128] Faulkes Z. Loss of escape responses and giant neurons in the tailflipping circuits of slipper lobsters, *Ibacus* spp. (Decapoda, Palinura, Scyllaridae). Arthropod Structure and Development.

[129] Jones C. The biology and behaviour of bay lobsters, *Thenus* spp. (Decapoda: Scyllaridae) in Northern Queensland, Australia [thesis]. Brisbane, Australia: University of Queensland; 1988

[131] Spanier E, Weihs D. Hydrodynamic

[130] Spanier E, Weihs D. Why do shovel-nosed (slipper) lobsters have shovels? The Lobster Newsletter.

aspects of locomotion in the Mediterranean slipper lobster*, Scyllarides latus*. In: Proceedings of the 7th International Conference and Workshop on Lobster Biology and

*Scyllarid Lobster Biology and Ecology DOI: http://dx.doi.org/10.5772/intechopen.88218*

*Crustacea*

Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis gully shark, *Triakis megalopterus*, off the Eastern Cape, South Africa. Fishery

[117] Barreiros JP, Santos RS. Notes on the food habits and predatory behaviour of the dusky grouper, *Epinephelus marginatus* (Lowe, 1834) (Pisces: Serranidae) in the Azores. Arquipelago Life and Marine Sciences.

[118] Mizrahi M, Chapman JK, Gough CLA, Humber F, Anderson LG. Management implications of the influence of biological variability of invasive lionfish diet in Belize. Management. 2017;**8**(1):61-70

[119] Oliveira G, Freire AS, Bertuol PRK. Reproductive biology of the slipper lobster *Scyllarides deceptor* (Decapoda: Scyllaridae) along the southern Brazilian coast. Journal of the Marine Biological Association of the United Kingdom. 2008;**88**:1433-1440

[120] DeMartini EE, McCracken ML, Moffitt RB, Wetherall JA. Relative pleopod length as an indicator of size at sexual maturity in slipper (*Scyllarides squammosus*) and spiny Hawaiian (*Panulirus marginatus*) lobsters. Fishery

[121] Kizhakudan JK, Thirumilu P, Rajapackiam S, Manibal C. Captive breeding and seed production of scyllarid lobsters—Opening new vistas in crustacean aquaculture. Marine Fisheries Information Service India,

[122] Goldstein JS, Dubofsky EA, Spanier E. Into a rhythm: Diel activity patterns and behaviour in Mediterranean slipper lobsters, *Scyllarides latus*. ICES Journal of Marine Science. 2015;**72**(Suppl.

[123] O'Malley JM, Walsh WA. Annual and long-term movement patterns of spiny lobster, *Panulirus marginatus*, and

Bulletin. 2005;**103**:23-33

T & E Series. 2004;**181**:1-4

1):i147-i154

Bulletin. 1999;**97**:987-998

1998;**16A**:29-35

[109] Zimmer-Faust RK, Spanier E. Gregariousness and sociality in spiny lobsters: Implications for den habitations. Journal of Experimental

[110] Spanier E, Zimmer-Faust RK. Some physical properties of shelter that influence den preference in spiny lobsters. Journal of Experimental Marine Biology and Ecology.

[111] Lozano-Alvarez E, Spanier E. Behavior and growth of captive sub-adults spiny lobsters, *Panulirus argus,* under the risk of predation. Marine and Freshwater Research.

[112] Herrnkind WF, Childress MJ, Lavalli KL. Defense coordination and other benefits among exposed spiny lobsters: Inferences from mass migratory and mesocosm studies of group size and behavior. Marine and Freshwater Research. 2001;**52**:1133-1143

[113] Hamilton WD. Geometry for the selfish herd. Journal of Theoretical

[114] Horne FR, Tarsitano SF. The mineralization and biomechanics of the exoskeleton. In: Lavalli KL, Spanier E, editors. The Biology and Fisheries of the Slipper Lobster. Crustacean Issues 17. New York: CRC Press, Taylor & Francis

[115] Tarsitano SF, Lavalli KL, Horne F, Spanier E. The constructional properties of the exoskeleton of homarid, scyllarid, and palinurid lobsters. Hydrobiologia.

Reproduction and feeding of spotted

Biology. 1971;**31**:294-311

Group; 2007. pp. 183-198

[116] Smale MJ, Goosen AJJ.

2006;**557**:9-20

Marine Biology and Ecology.

1987;**105**:57-71

1988;**122**:137-149

1997;**48**(8):707-713

Group; 2007. pp. 133-181

**48**

slipper lobster, *Scyllarides squammosus*, in the Northwestern Hawaiian islands. Bulletin of Marine Science. 2013;**89**(2):529-549

[124] Stewart J, Kennelly SJ. Contrasting movements of two exploited Scyllarid lobsters of the genus *Ibacus* off the east coast of Australia. Fisheries Research. 1998;**2-3**:127-132. DOI: 10.1016/ S0165-7836(98)00104-0

[125] Neil DM, Ansel AD. The orientation of tail-flip escape swimming in decapod and mysid crustaceans. Journal of the Marine Biological Association of the United Kingdom. 1995;**75**:55-70

[126] Ritz DA, Jacklyn PM. Believe it or not—Bugs fly through water. Australian Fisheries. 1985;**44**:35-37

[127] Jacklyn PM, Ritz DA. Hydrodynamics of swimming in scyllarid lobsters. Journal of Experimental Marine Biology and Ecology. 1986;**101**:85-89

[128] Faulkes Z. Loss of escape responses and giant neurons in the tailflipping circuits of slipper lobsters, *Ibacus* spp. (Decapoda, Palinura, Scyllaridae). Arthropod Structure and Development. 2004;**33**:113-123

[129] Jones C. The biology and behaviour of bay lobsters, *Thenus* spp. (Decapoda: Scyllaridae) in Northern Queensland, Australia [thesis]. Brisbane, Australia: University of Queensland; 1988

[130] Spanier E, Weihs D. Why do shovel-nosed (slipper) lobsters have shovels? The Lobster Newsletter. 1992;**5**(1):8-9

[131] Spanier E, Weihs D. Hydrodynamic aspects of locomotion in the Mediterranean slipper lobster*, Scyllarides latus*. In: Proceedings of the 7th International Conference and Workshop on Lobster Biology and

Management; 8-13 February 2004; Tasmania, Australia. p. 61

[132] Bianchini ML, Raisa PF. Valutazione della fattibilità e potenzialità del ripoplamento attivo per la magnosa, Scyllarides latus (*Crostacei Decapodi*). Final report to MiRAAF (Pesca Marittima); 1997; 1

[133] Newell IM. A parasitic species of *Copidognathus* (Acari: Halacaridae). Proceedings of the Hawaiin Entomollogical Society. 1956;**16**(1):122-125

[134] Perry LT. Relationships between culture conditions and moult death syndrome (MDS) in larval development of the bay lobsters *Thenus orientalis* (Lund, 1793) and *Thenus indicus* Leach, 1815 (Decapoda: Scyllaridae) [thesis]. School of Biological Sciences, University of Queensland; 2001

[135] Wakabayashi K, Otake S, Tanaka Y, Nagasawa K. *Choniomyzon inflatus* n. sp. (Crustacea: Copepoda: Nicothoidae) associated with *Ibacus novemdentatus* (Crustacea: Decapoda: Scyllaridae) from Japanese waters. Systematic Parasitology. 2013;**84**(2):157-165

[136] WWF. 2015. Living Blue Planet Report. Species, habitats and human well-being. In: Tanzer J, Phua C, Lawrence A, Gonzales A, Roxburgh T, Gamblin P, editors. WWF, Gland, Switzerland. Available from: https:// www.wwf.de/fileadmin/fm-wwf/ Publikationen-PDF/Living-Blue-Planet-Report-2015.pdf

[137] Gillespie KM, Vincent AC. Tropical invertebrate response to marine reserves varies with protection duration, habitat type, and exploitation history. Aquatic Conservation: Marine and Freshwater Ecosystems. 2019;**29**(3):511-520

[138] Miller E, Spanier E, Yahel R, Diamant R. Do marine nature reserves enhance the conservation of the Mediterranean slipper lobster (*Scyllarides latus*)?—Preliminary results. In: Proceedings of the 2nd Israeli Conference for Conservation Science—A Sustainable Future for Humans and Nature; 16-17 April 2019; Technion, Haifa. p. 24

[139] Groeneveld JC, Kirkman SP, Boucher M, Yemane D. From biomass mining to sustainable fishing—Using abundance and size to define a spatial management framework for deep-water lobster. African Journal of Marine Science. 2012;**34**(4):547-557

[140] Schultz JK, O'Malley JM, Kehn EE, Polovina JJ, Parrish FA, Kosaki RK. Tempering expectations of recovery for previously exploited populations in a fully protected marine reserve. Journal of Marine Biology. 2011;**2011**. DOI: 10.1155/2011/749131

[141] Boavida-Portugal J, Rosa R, Calado R, Pinto M, Boavida-Portugal I, Araújo MB, et al. Climate change impacts on the distribution of coastal lobsters. Marine Biology. 2018;**165**(12):186

**51**

Chile [6].

**Chapter 4**

1782)

**Abstract**

*Walter Reyes A.*

within seminatural ponds.

**1. Introduction**

Management of the Interaction

and Cannibalism of Postlarvae and

Adults of the Freshwater Shrimp

*Cryphiops caementarius* (Molina,

*Cryphiops caementarius* shrimp inhabits the rivers of the western slope of the Andes of Peru and Chile. But the greatest population densities found in the rivers of Arequipa (Peru) have social, economic, commercial, and gastronomic importance. Researches on this species of shrimp date from 1950. The males of *C. caementarius* are aggressive by having one of the most developed chelipeds, causing greater interaction and cannibalism. To reduce the interaction of the species, it has been used two culture systems. For postlarvae, using brackish water can maintain high survival (>85%), but only in initial culture which lasts for 50 days. For the fattening of adult males, culturing in separate containers conditioned in various levels

the culture is also performed with tilapia. It is still required to demonstrate the technical and economic feasibility of fattening male shrimp in individual containers

The Palaemonid shrimps that inhabit the rivers of the western slope of the Andes are represented by 12 species, three of which correspond to the genus *Palaemon*, eight to *Macrobrachium,* and one to *Cryphiops* [1]. Of these, *Cryphiops caementarius* (Molina, 1782) inhabits the rivers of the coast of Peru and Chile. However, only in Peru, it has social, economic, and commercial importance since it is extracted from the Pativilca River in Lima to the Tambo River in Arequipa, where there is high population density [2], which, in 2016, was captured as 1112.9 t [3]. In addition, the species has culinary importance whose potential markets are restaurants in the regions of Lima and Arequipa in Peru [4]. *C. caementarius* is also distributed until Valparaiso in Chile [5], although with less commercial importance due to the low population densities and because it is a vulnerable species in the northern region and in danger of extinction in the Metropolitan Region of

**Keywords:** freshwater shrimp, cannibalism, interaction, culture systems

), and with this system,

improves the survival (87–100%) and yield (1.0 kg m<sup>−</sup><sup>2</sup>

#### **Chapter 4**

*Crustacea*

of the Mediterranean slipper lobster (*Scyllarides latus*)?—Preliminary results. In: Proceedings of the 2nd Israeli Conference for Conservation Science—A Sustainable Future for Humans and Nature; 16-17 April 2019;

[139] Groeneveld JC, Kirkman SP, Boucher M, Yemane D. From biomass mining to sustainable fishing—Using abundance and size to define a spatial management framework for deep-water lobster. African Journal of Marine Science. 2012;**34**(4):547-557

[140] Schultz JK, O'Malley JM, Kehn EE, Polovina JJ, Parrish FA, Kosaki RK. Tempering expectations of recovery for previously exploited populations in a fully protected marine reserve. Journal of Marine Biology. 2011;**2011**. DOI:

[141] Boavida-Portugal J, Rosa R, Calado R, Pinto M, Boavida-Portugal I, Araújo MB, et al. Climate change impacts on the distribution of coastal lobsters. Marine Biology. 2018;**165**(12):186

Technion, Haifa. p. 24

10.1155/2011/749131

**50**

Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater Shrimp *Cryphiops caementarius* (Molina, 1782)

*Walter Reyes A.*

#### **Abstract**

*Cryphiops caementarius* shrimp inhabits the rivers of the western slope of the Andes of Peru and Chile. But the greatest population densities found in the rivers of Arequipa (Peru) have social, economic, commercial, and gastronomic importance. Researches on this species of shrimp date from 1950. The males of *C. caementarius* are aggressive by having one of the most developed chelipeds, causing greater interaction and cannibalism. To reduce the interaction of the species, it has been used two culture systems. For postlarvae, using brackish water can maintain high survival (>85%), but only in initial culture which lasts for 50 days. For the fattening of adult males, culturing in separate containers conditioned in various levels improves the survival (87–100%) and yield (1.0 kg m<sup>−</sup><sup>2</sup> ), and with this system, the culture is also performed with tilapia. It is still required to demonstrate the technical and economic feasibility of fattening male shrimp in individual containers within seminatural ponds.

**Keywords:** freshwater shrimp, cannibalism, interaction, culture systems

#### **1. Introduction**

The Palaemonid shrimps that inhabit the rivers of the western slope of the Andes are represented by 12 species, three of which correspond to the genus *Palaemon*, eight to *Macrobrachium,* and one to *Cryphiops* [1]. Of these, *Cryphiops caementarius* (Molina, 1782) inhabits the rivers of the coast of Peru and Chile. However, only in Peru, it has social, economic, and commercial importance since it is extracted from the Pativilca River in Lima to the Tambo River in Arequipa, where there is high population density [2], which, in 2016, was captured as 1112.9 t [3]. In addition, the species has culinary importance whose potential markets are restaurants in the regions of Lima and Arequipa in Peru [4]. *C. caementarius* is also distributed until Valparaiso in Chile [5], although with less commercial importance due to the low population densities and because it is a vulnerable species in the northern region and in danger of extinction in the Metropolitan Region of Chile [6].

Other species of *Cryphiops* inhabit caves in the state of Chiapas in Mexico, as *C.* (*Bithynops*) *luscus* and *C.* (*Bithynops*) *perspicax* [7] and *C. (Bithynops) villalobosi* inhabits rivers and streams [8]. In Brazil, *C. brasiliensis* inhabit in a river of the Federal District [9]. All these species are small in size, whose populations are not attractive to trade.

Researches related to shrimp *C. caementarius* date from 1950, and the generated interest is in order to establish commercial cultivation. However, the culturing is affected as the strong interaction given the size and thicker of the second pair of pereiopods that is a sign that the species is aggressive, and for the cannibalism that happens between congeners. These limitations affect the growth and yield of shrimp.

The purpose of this chapter was to review progress in research with that of the freshwater shrimp *C. caementarius*, related to alternative solutions to the problems of the management of the interaction and cannibalism of postlarvae and adults.

#### **2. Interaction**

In decapod crustaceans, there are those who are very aggressive as portunids crabs (*Scylla*, *Callinectes*, and *Portunus*), king crabs (*Lithodes* and *paralithodes*), followed by chelated lobsters (*Homarus* and *Nephrops*) and spiny lobsters (*Panulirus* and *Jasus*), and also, those who are less aggressive as crayfish (*Procambarus*, *Cherax*, *Pacifastacus*, and *Astacus*) and penaeids (*Litopenaeus*) and are less cannibals [10]. Therefore, the aggressiveness between congeners depends on the species.

In the territorialist decapod crustaceans, the second pair of pereopods (chelipeds) is long and thick and also those are used for attack and defense, for agonistic interaction and for courtship and mating [11]. Males of *C. caementarius* have one of the most developed chelipeds (**Figure 1**), either the right or the left. In females, the chelipeds are of similar size. This morphological feature of the chelipeds makes males an aggressive species whose interaction and cannibalism are observed in aquariums, tanks, and ponds [12], but this behavior has not been assessed yet. In *Callinectes arcuatus* and *C. bellicosus*, the chelipeds are dimorphic, and generally, the right cheliped is the largest and the thicker that permit to consume mollusks and crustaceans [13].

The interaction of male *C. caementarius* is greater than that of females, because of this situation, males always show serious injuries in the cephalothorax, abdomen, and chelipeds, although it is common to observe shrimps without chelipeds. In juvenile *C. caementarius*, interaction and increasing stocking density cause high metabolic rate (87–91%) that affects the growth in weight [14] and probably the physiological state of the animal. In *Macrobrachium rosenbergii*, the chelipeds of older males are larger and thicker with which they access easily to food and shelter, in addition to giving them greater ability to combat due to the visualization of the

**53**

PLs m<sup>−</sup><sup>2</sup>

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater…*

opponent [15, 16]. This explains why the most affected parts of the crustaceans are

All decapod crustaceans use chelipeds for interaction, access to food, shelter, and mating, resulting in energy expenditure during the fight and can reach the autotomy of appendages and even cannibalism. Cannibalism, defined as intraspecific predation, is a behavior established in a wide variety of animals [18] and is considered as the process of killing and eating an individual of the same species [19], whether it consumes all or part of it. In *C. caementarius*, cannibalism is often a response to captivity, lack of shelter, ecdysis, increased density, lack of food, and

The molting fluid accumulated between the old cuticle and epidermis is the product of degradation of the old cuticle [20], which is released with ecdysis and acts as a chemical stimulant [21]. In the Hermit crabs, *Clibanarius digueti* and *Paguristes perrieri*, the odor of the injured animals of the same species as well as other species is a feeding signal [22]. Similarly, the odor released during autotomy to escape a predatory aggression influences agonistic behavior in decapod crustaceans [10]. The *C. caementarius* adults who are close to the ecdysis (premuda D3 and D4) during ecdysis (E) or after ecdysis (postmoult A) are more prone to cannibalism, mainly after the ecdysis, where the soft exoskeleton, which takes time to harden, makes movement and defense difficult for himself. The cannibalism of C. caementarius starts from Zoea 8 and increases as they grow [23, 24]. These observations indicate that cannibalism may have a genetic component, at least in the species, as suggested in other cannibalistic

In *M. rosenbergii*, interaction and cannibalism by molt is attenuated with the use of shelters [25, 26], artificial substrates [27, 28], and by increasing tryptophan in the diet [29], with which high survival is maintained and growth is improved. Further

The crustacean's cultivation comprises producing postlarvae in hatchery, the postlarvae growth until reaching juvenile stage or condition of preadult and the fattening until reaching commercial weight (>20 g). Postlarvae adapt to environmental conditions during the initial culture, and those who survive are resistant, and have higher growth rate. However, as mentioned, the problem is the interaction and cannibalism that happens throughout the animal's life. Similar advantages are reported during the nursery phase of *M. rosenbergii* postlarvae due to the interac-

To reduce cannibalism of postlarvae during communal cultivation and obtain juveniles with greater weight (200 mg) for stocking in ponds, growing in brackish water should be performed. Recent postlarvae of *C. caementarius* (11 mm total length and 40 mg total weight) have remarkable euryhalinity and achieve greater weight when grown for 50 days in brackish water of 12‰ and with density of 114

 [31]. These results demonstrate the physiological efficiency of organisms to accumulate biomass in such salinity conditions, probably because they are in their isosmotic point. In addition, 95% of postlarvae survive in water with salinity of 12‰, 70% live in water of 24‰, and 40% in fresh water. This high survival of postlarvae in brackish water than in fresh water is due to the reduction

research is needed to evaluate these culturing systems in *C. caementarius*.

**4. Cultivation of postlarvae in brackish water**

the pereopods, pleopods, antennae, antennules, and uropods [17].

poor water quality, and it is probably a natural behavior.

*DOI: http://dx.doi.org/10.5772/intechopen.87438*

**3. Cannibalism**

species [19].

tion and cannibalism [30].

**Figure 1.** *Body parts and appendages of the freshwater shrimp C. caementarius.*

opponent [15, 16]. This explains why the most affected parts of the crustaceans are the pereopods, pleopods, antennae, antennules, and uropods [17].

#### **3. Cannibalism**

*Crustacea*

shrimp.

**2. Interaction**

attractive to trade.

Other species of *Cryphiops* inhabit caves in the state of Chiapas in Mexico, as *C.* (*Bithynops*) *luscus* and *C.* (*Bithynops*) *perspicax* [7] and *C. (Bithynops) villalobosi* inhabits rivers and streams [8]. In Brazil, *C. brasiliensis* inhabit in a river of the Federal District [9]. All these species are small in size, whose populations are not

Researches related to shrimp *C. caementarius* date from 1950, and the generated

The purpose of this chapter was to review progress in research with that of the freshwater shrimp *C. caementarius*, related to alternative solutions to the problems of the management of the interaction and cannibalism of postlarvae and adults.

In decapod crustaceans, there are those who are very aggressive as portunids crabs (*Scylla*, *Callinectes*, and *Portunus*), king crabs (*Lithodes* and *paralithodes*), followed by chelated lobsters (*Homarus* and *Nephrops*) and spiny lobsters (*Panulirus* and *Jasus*), and also, those who are less aggressive as crayfish (*Procambarus*, *Cherax*, *Pacifastacus*, and *Astacus*) and penaeids (*Litopenaeus*) and are less cannibals [10]. Therefore, the

In the territorialist decapod crustaceans, the second pair of pereopods (chelipeds) is long and thick and also those are used for attack and defense, for agonistic interaction and for courtship and mating [11]. Males of *C. caementarius* have one of the most developed chelipeds (**Figure 1**), either the right or the left. In females, the chelipeds are of similar size. This morphological feature of the chelipeds makes males an aggressive species whose interaction and cannibalism are observed in aquariums, tanks, and ponds [12], but this behavior has not been assessed yet. In *Callinectes arcuatus* and *C. bellicosus*, the chelipeds are dimorphic, and generally, the right cheliped is the largest and the thicker that permit to consume mollusks and crustaceans [13]. The interaction of male *C. caementarius* is greater than that of females, because of this situation, males always show serious injuries in the cephalothorax, abdomen, and chelipeds, although it is common to observe shrimps without chelipeds. In juvenile *C. caementarius*, interaction and increasing stocking density cause high metabolic rate (87–91%) that affects the growth in weight [14] and probably the physiological state of the animal. In *Macrobrachium rosenbergii*, the chelipeds of older males are larger and thicker with which they access easily to food and shelter, in addition to giving them greater ability to combat due to the visualization of the

aggressiveness between congeners depends on the species.

*Body parts and appendages of the freshwater shrimp C. caementarius.*

interest is in order to establish commercial cultivation. However, the culturing is affected as the strong interaction given the size and thicker of the second pair of pereiopods that is a sign that the species is aggressive, and for the cannibalism that happens between congeners. These limitations affect the growth and yield of

**52**

**Figure 1.**

All decapod crustaceans use chelipeds for interaction, access to food, shelter, and mating, resulting in energy expenditure during the fight and can reach the autotomy of appendages and even cannibalism. Cannibalism, defined as intraspecific predation, is a behavior established in a wide variety of animals [18] and is considered as the process of killing and eating an individual of the same species [19], whether it consumes all or part of it. In *C. caementarius*, cannibalism is often a response to captivity, lack of shelter, ecdysis, increased density, lack of food, and poor water quality, and it is probably a natural behavior.

The molting fluid accumulated between the old cuticle and epidermis is the product of degradation of the old cuticle [20], which is released with ecdysis and acts as a chemical stimulant [21]. In the Hermit crabs, *Clibanarius digueti* and *Paguristes perrieri*, the odor of the injured animals of the same species as well as other species is a feeding signal [22]. Similarly, the odor released during autotomy to escape a predatory aggression influences agonistic behavior in decapod crustaceans [10]. The *C. caementarius* adults who are close to the ecdysis (premuda D3 and D4) during ecdysis (E) or after ecdysis (postmoult A) are more prone to cannibalism, mainly after the ecdysis, where the soft exoskeleton, which takes time to harden, makes movement and defense difficult for himself. The cannibalism of C. caementarius starts from Zoea 8 and increases as they grow [23, 24]. These observations indicate that cannibalism may have a genetic component, at least in the species, as suggested in other cannibalistic species [19].

In *M. rosenbergii*, interaction and cannibalism by molt is attenuated with the use of shelters [25, 26], artificial substrates [27, 28], and by increasing tryptophan in the diet [29], with which high survival is maintained and growth is improved. Further research is needed to evaluate these culturing systems in *C. caementarius*.

#### **4. Cultivation of postlarvae in brackish water**

The crustacean's cultivation comprises producing postlarvae in hatchery, the postlarvae growth until reaching juvenile stage or condition of preadult and the fattening until reaching commercial weight (>20 g). Postlarvae adapt to environmental conditions during the initial culture, and those who survive are resistant, and have higher growth rate. However, as mentioned, the problem is the interaction and cannibalism that happens throughout the animal's life. Similar advantages are reported during the nursery phase of *M. rosenbergii* postlarvae due to the interaction and cannibalism [30].

To reduce cannibalism of postlarvae during communal cultivation and obtain juveniles with greater weight (200 mg) for stocking in ponds, growing in brackish water should be performed. Recent postlarvae of *C. caementarius* (11 mm total length and 40 mg total weight) have remarkable euryhalinity and achieve greater weight when grown for 50 days in brackish water of 12‰ and with density of 114 PLs m<sup>−</sup><sup>2</sup> [31]. These results demonstrate the physiological efficiency of organisms to accumulate biomass in such salinity conditions, probably because they are in their isosmotic point. In addition, 95% of postlarvae survive in water with salinity of 12‰, 70% live in water of 24‰, and 40% in fresh water. This high survival of postlarvae in brackish water than in fresh water is due to the reduction

of cannibalism probably because the released substances before, during, and after ecdysis are attenuated by ions of the brackish water from the culture medium [31].

Furthermore, the culture of postlarvae *C. caementarius* in brackish water with 12‰ allows increasing the density up to 500 PLs m<sup>−</sup><sup>2</sup> without affecting the growth and survival after 60 days of culture [32]. In juveniles of *M. tenellum* [33] and *M. rosenbergii*, the higher growth and higher survival (>90%) are obtained in water with 10‰ salinity [34]. Under these conditions of salinity and density, it is convenient to use shelters or artificial substrates to enhance the growth of postlarvae.

#### **5. Adult shrimp culturing in individual containers**

The main problems of the communal culturing of adult crustaceans are the interaction and cannibalism per molt, which are accentuated as the animals grow and affect the growth and survival, respectively. In the communal culturing of *C. caementarius*, survival decreases to 17% in aquariums [12] and 25% in tanks [24, 35]. In seminatural ponds, it is likely to obtain survivals between 40 and 50%, and even the density is 5 shrimp m<sup>−</sup><sup>2</sup> , due to increased cannibalism. These survival results of the species prevent the establishment of commercial cultivation.

Cultivation in individual containers was first used in lobster *H. americanus* where the container shape (circular, square, and rectangular) does not affect the growth, but the size of these (20–181 cm2 ) retards the growth [36]. Larger containers were also used (750 cm2 ) [37]. The cultures in individual containers and conditioned at several levels used are *Cherax tenuimanus* [38], *C. quadricarinatus* [39], and *H. americanus* [40, 41]. Although the circular containers can have mesh as used in *H. gammarus* [42]. In any type of culture container, physical interaction of organisms is avoided, improving the growth and survival.

The first cultivation system in individual containers was performed with adult females *C. caementarius* [43] and then with males [12], both in aquariums (**Figure 2**) and fiberglass tanks (**Figure 3**). In this system, the species tolerates cultivation in containers of reduced physical space (133–284 cm2 ), not being affected by ovarian maturation, the spawning, the molting period, and the growth and survival during 4–6 months of culture. Moreover, the lower specific density factor k = 16 means that the species requires less space than the other crustaceans [12] obtained. The specific density factor is an indicator when the size of the containers inhibits the species growth, and the k factor is ≤ 22 from *C. quadricarinatus* [39], k ≤ 45 from *C. tenuimanus* [38], and k ≤ 50 from *C. destructor* [44]. That is, these species of crustaceans cannot tolerate reduced physical spaces during cultivation in individual containers.

#### **Figure 2.**

*System culture of C. caementarius in individual containers conditioned in aquariums with water recirculation system and biofilter.*

**55**

*\**

**Table 1.**

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater…*

Individual containers are conditioned in various levels, both aquariums and tanks or seminatural ponds, thus increasing the planting density. In aquariums (0.186 m2 and effective volume of 55 L), the containers are installed in three levels, but in two columns, making a total of six containers per aquarium equivalent to 32 shrimps m<sup>−</sup><sup>2</sup>

*System culture of C. caementarius in individual containers conditioned in fiberglass tanks with water* 

ume of 100 L), the containers are installed in five levels, but in three columns, mak-

significant differences with those of smaller areas (**Table 1**) are seen. In *C. quadricari-*

sold by weight, including the chelipeds, then it is preferable to use the large containers. Shrimp farming in individual containers installed in seminatural ponds has not been investigated, but environmental and productivity pond water conditions could

The effective density is the number of surviving organisms at the end of the culture period according to the area of the container. In *C. caementarius*, the effec-

times higher than that one obtained in semi-intensive monoculture of *M. rosenbergii*

tainers, the final effective density after 100 days of culture was between 143 and 348

**Final weight (g)**

 **period<sup>−</sup><sup>1</sup> Area )**

133 13 94.34 ± 0.00 8.09 ± 1.37ª 0.763 ± 0.129ª 7.64 ± 1.29ª 201 16 94.34 ± 0.00 9.99 ± 0.62ªb 0.941 ± 0.058ª 9.42 ± 0.59ª 284 19 81.76 ± 10.89 13.20 ± 1.99b 1.049 ± 0.059ª 10.49 ± 0.59ª

*Data were estimated for a 4-month period. Letters a and b in superscript in a column indicate that there is a* 

*Estimated production (mean ± standard deviation) of males of C. caementarius cultivated during 4 months in* 

is considered high, and therefore, cultivation is intensive, which could produce

per period in 4 months (**Table 1**), and get 31.5 t ha<sup>−</sup><sup>1</sup>

**density (shrimp m<sup>−</sup><sup>2</sup>**

**)**

*individual containers of different sizes conditioned in five levels inside fiberglass tanks [12].*

and an effective vol-

is achieved [39]. But, as shrimp *C. caementarius* is

, obtained by cultivation in individual containers,

[45]. However, in *C. quadricarinatus*, stocked in individual con-

y<sup>−</sup><sup>1</sup>

**Estimated performance (kg m<sup>−</sup><sup>2</sup> )**

(**Figure 3**). In both

, which is 10

**Estimated production\* (t ha<sup>−</sup><sup>1</sup>**

), although no

tanks where

(**Figure 2**). In fiberglass tanks (with a bottom area of 0.159 m2

high yield in containers of 490 cm2

tive density of 94 shrimps m<sup>−</sup><sup>2</sup>

y<sup>−</sup><sup>1</sup>

**Container Effective** 

**Diameter (cm)**

*significant difference (p < 0.05).*

10.5 t ha<sup>−</sup><sup>1</sup>

**(cm2 )**

**Figure 3.**

*recirculation system and biofilter.*

reaching 3 t ha<sup>−</sup><sup>1</sup>

ing a total of 15 containers per tank equivalent to 94 shrimps m<sup>−</sup><sup>2</sup>

cases, the increased production is achieved in large containers (284 cm2

*natus*, the culture containers are conditioned in seven levels within 3 m2

benefit the growth, color of the shrimp, and reduce the feed conversion.

*DOI: http://dx.doi.org/10.5772/intechopen.87438*

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater… DOI: http://dx.doi.org/10.5772/intechopen.87438*

**Figure 3.**

*Crustacea*

of cannibalism probably because the released substances before, during, and after ecdysis are attenuated by ions of the brackish water from the culture medium [31]. Furthermore, the culture of postlarvae *C. caementarius* in brackish water with

and survival after 60 days of culture [32]. In juveniles of *M. tenellum* [33] and *M. rosenbergii*, the higher growth and higher survival (>90%) are obtained in water with 10‰ salinity [34]. Under these conditions of salinity and density, it is convenient to use shelters or artificial substrates to enhance the growth of postlarvae.

The main problems of the communal culturing of adult crustaceans are the interaction and cannibalism per molt, which are accentuated as the animals grow and affect the growth and survival, respectively. In the communal culturing of *C. caementarius*, survival decreases to 17% in aquariums [12] and 25% in tanks [24, 35]. In seminatural ponds, it is likely to obtain survivals between 40 and 50%,

results of the species prevent the establishment of commercial cultivation. Cultivation in individual containers was first used in lobster *H. americanus* where the container shape (circular, square, and rectangular) does not affect the

conditioned at several levels used are *Cherax tenuimanus* [38], *C. quadricarinatus* [39], and *H. americanus* [40, 41]. Although the circular containers can have mesh as used in *H. gammarus* [42]. In any type of culture container, physical interaction of

The first cultivation system in individual containers was performed with adult females *C. caementarius* [43] and then with males [12], both in aquariums (**Figure 2**) and fiberglass tanks (**Figure 3**). In this system, the species tolerates cultivation in

maturation, the spawning, the molting period, and the growth and survival during 4–6 months of culture. Moreover, the lower specific density factor k = 16 means that the species requires less space than the other crustaceans [12] obtained. The specific density factor is an indicator when the size of the containers inhibits the species growth, and the k factor is ≤ 22 from *C. quadricarinatus* [39], k ≤ 45 from *C. tenuimanus* [38], and k ≤ 50 from *C. destructor* [44]. That is, these species of crustaceans cannot tolerate reduced physical spaces during cultivation in individual containers.

*System culture of C. caementarius in individual containers conditioned in aquariums with water recirculation* 

without affecting the growth

, due to increased cannibalism. These survival

) retards the growth [36]. Larger con-

), not being affected by ovarian

) [37]. The cultures in individual containers and

12‰ allows increasing the density up to 500 PLs m<sup>−</sup><sup>2</sup>

**5. Adult shrimp culturing in individual containers**

organisms is avoided, improving the growth and survival.

containers of reduced physical space (133–284 cm2

and even the density is 5 shrimp m<sup>−</sup><sup>2</sup>

tainers were also used (750 cm2

growth, but the size of these (20–181 cm2

**54**

**Figure 2.**

*system and biofilter.*

*System culture of C. caementarius in individual containers conditioned in fiberglass tanks with water recirculation system and biofilter.*

Individual containers are conditioned in various levels, both aquariums and tanks or seminatural ponds, thus increasing the planting density. In aquariums (0.186 m2 and effective volume of 55 L), the containers are installed in three levels, but in two columns, making a total of six containers per aquarium equivalent to 32 shrimps m<sup>−</sup><sup>2</sup> (**Figure 2**). In fiberglass tanks (with a bottom area of 0.159 m2 and an effective volume of 100 L), the containers are installed in five levels, but in three columns, making a total of 15 containers per tank equivalent to 94 shrimps m<sup>−</sup><sup>2</sup> (**Figure 3**). In both cases, the increased production is achieved in large containers (284 cm2 ), although no significant differences with those of smaller areas (**Table 1**) are seen. In *C. quadricarinatus*, the culture containers are conditioned in seven levels within 3 m2 tanks where high yield in containers of 490 cm2 is achieved [39]. But, as shrimp *C. caementarius* is sold by weight, including the chelipeds, then it is preferable to use the large containers. Shrimp farming in individual containers installed in seminatural ponds has not been investigated, but environmental and productivity pond water conditions could benefit the growth, color of the shrimp, and reduce the feed conversion.

The effective density is the number of surviving organisms at the end of the culture period according to the area of the container. In *C. caementarius*, the effective density of 94 shrimps m<sup>−</sup><sup>2</sup> , obtained by cultivation in individual containers, is considered high, and therefore, cultivation is intensive, which could produce 10.5 t ha<sup>−</sup><sup>1</sup> per period in 4 months (**Table 1**), and get 31.5 t ha<sup>−</sup><sup>1</sup> y<sup>−</sup><sup>1</sup> , which is 10 times higher than that one obtained in semi-intensive monoculture of *M. rosenbergii* reaching 3 t ha<sup>−</sup><sup>1</sup> y<sup>−</sup><sup>1</sup> [45]. However, in *C. quadricarinatus*, stocked in individual containers, the final effective density after 100 days of culture was between 143 and 348


*\* Data were estimated for a 4-month period. Letters a and b in superscript in a column indicate that there is a significant difference (p < 0.05).*

#### **Table 1.**

*Estimated production (mean ± standard deviation) of males of C. caementarius cultivated during 4 months in individual containers of different sizes conditioned in five levels inside fiberglass tanks [12].*

individuals m<sup>−</sup><sup>2</sup> and the yield between 4 and 8 kg m<sup>−</sup><sup>2</sup> [39]. Future research should establish in detail the conditions of the cultivation system in individual containers, to intensify the cultivation of *C. caementarius*. Parallel to this, a technical-economic study must be made to know the feasibility of shrimp farming in the system.

However, the cultivation of *C. caementarius* in individual containers causes loss of body color and of cephalothoracic appendages (**Figure 4**), but the use of *Capsicum annuum* (250 mg kg<sup>−</sup><sup>1</sup> ) [12] and in the diet (300 mg kg<sup>−</sup><sup>1</sup> ) improves pigmentation of the body [46]. Consequently, the shrimp diet should contain carotenoid pigments, since crustaceans cannot synthesize carotenoids de novo [47]. Body depigmentation attributed to diet happens in *C. tenuimanus* [38] and *H. gammarus* [40], when they are grown in individual containers.

In the culture of *C. caementarius* in individual containers, the management of food at the commercial level would imply a cost of additional labor that increases the cost of cultivation. It is, therefore, necessary to design a food distribution system as used in *Homarus* sp. [48] and *H. gammarus* [49]. In species of *Scylla*, the most sophisticated designed system to date includes cameras linked to a computer system that regularly scans the cells to see if there are one or two crabs in each container indicating that the crab has made an ecdysis, by the presence of exoskeleton and crab. In addition, this system also includes a sophisticated water recirculation system [50].

In studies with male shrimps *C. caementarius* in individual containers installed in aquaria and tanks with recirculation system with water and biological filters, growth is evaluated by eyestalk ablation [51] per culturing at different water hardness [52] and by different inputs used in the diet such as paprika [46], yeast [53], common salt [54], biological silage [55], and soya lecithin [56]. Survival of >90% are obtained in all these investigations, which demonstrates the effectiveness of the culture system by avoiding the physical interaction and cannibalism of river shrimp. In similar culture conditions, survivals between 71 and 83% in *C. tenuimanus* [38] and 96% in *C. quadricarinatus* [39] are achieved. However, the system requires individual containers to be improved with regard to handling molting, feed system, monitoring of the species, the recirculation system automation, and use in seminatural ponds. In the same way, the individual containers are not only useful for enhancing the growth of *C. caementarius*, but also for the management of female reproduction, and in the case of shrimp males, also for selecting those with the highest rates of specific growth (>1% weight day<sup>−</sup><sup>1</sup> ) for the purposes of genetic improvement.

#### **Figure 4.**

*Color of the C. caementarius body after culturing in individual containers: (A) female of normal color; (B) female depigmented; (C) male of normal color; and (D) male depigmented.*

**57**

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater…*

The co-culturing is done out with two species share a common aquatic environment (aquarium, tank, or pond), but whose construction does not allow physical interaction between organisms because they remain separate, and therefore, both species are a major management factor. Instead, in the polyculture, two or three species within the aquatic environment interact constantly competing for space and

Combinations of species in a co-culturing allow maximizing the performance of those who are territorial and aggressive. The co-culture of *Oreochromis niloticus* in cages inside ponds with *M. rosenbergii* [57] is well known. Also, it is known to co-culture of *C. caementarius* male shrimp in individual containers inside aquariums with *O. niloticus* fingerlings (**Figure 5**), where tilapia production was estimated at

container [12]. In other researches, co-culture of *C. caementarius* shrimp with tilapia *O. niloticus* at different densities were performed [58], and co-culturing shrimp with tilapia was performed to evaluate different concentrations of biological silage [55]. In both cases, 100% survival was achieved and production of species is improved. Co-cultivation of shrimp/tilapia mainly generates high nitrates that may be used in the cultivation of vegetables, whose integration would result in an aquaponics system.

The communal transport of male adult shrimps *C. caementarius* for fattening purposes is difficult due to the increased interaction causing injuries, chelipeds loss, shrimp death mainly of those who are about to carry out ecdysis or those who molt during the transport. In addition, the increased mortality depends on the density and transport time; but water temperature is a dominant factor that affects shrimp

*(A) Co-culture of C. caementarius in individual containers with O. niloticus. (B) System of co-culture in* 

The transport of adult *C. caementarius* shrimps in individual containers is performed by using plastic cups where a shrimp (≥4 cm of total length) is introduced into each plastic cup (250 mL). The plastic cup has holes to allow the water flow (**Figure 6A**). Then, all plastic cups are conditioned in plastic containers (45 L) with water of river (**Figure 6B**) and with either continuous or intermittent aeration (**Figure 6C**). The average water temperature is around 20°C. This system allows to transport 77 shrimps (17 shrimps for 10 L) per container for 5 h and with 100% survival [12]. However, the ideal size of transporting cups of live shrimps has not been studied, but as they support very small physical space, it is possible to use

smaller plastic cups or to use PVC pipes according to the animal size.

. The tilapia consumed only food that came out of the shrimp culture

*DOI: http://dx.doi.org/10.5772/intechopen.87438*

food, and therefore only one species is the main one.

**6. Co-culture of shrimp/tilapia**

**7. Transportation of adult shrimp**

*aquarium. (C) Co-culture system in fiberglass tank.*

during transport [59].

0.511 kg m<sup>−</sup><sup>3</sup>

**Figure 5.**

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater… DOI: http://dx.doi.org/10.5772/intechopen.87438*

#### **6. Co-culture of shrimp/tilapia**

*Crustacea*

individuals m<sup>−</sup><sup>2</sup>

system [50].

growth (>1% weight day<sup>−</sup><sup>1</sup>

*Capsicum annuum* (250 mg kg<sup>−</sup><sup>1</sup>

[40], when they are grown in individual containers.

and the yield between 4 and 8 kg m<sup>−</sup><sup>2</sup>

establish in detail the conditions of the cultivation system in individual containers, to intensify the cultivation of *C. caementarius*. Parallel to this, a technical-economic

pigmentation of the body [46]. Consequently, the shrimp diet should contain carotenoid pigments, since crustaceans cannot synthesize carotenoids de novo [47]. Body depigmentation attributed to diet happens in *C. tenuimanus* [38] and *H. gammarus*

In the culture of *C. caementarius* in individual containers, the management of food at the commercial level would imply a cost of additional labor that increases the cost of cultivation. It is, therefore, necessary to design a food distribution system as used in *Homarus* sp. [48] and *H. gammarus* [49]. In species of *Scylla*, the most sophisticated designed system to date includes cameras linked to a computer system that regularly scans the cells to see if there are one or two crabs in each container indicating that the crab has made an ecdysis, by the presence of exoskeleton and crab. In addition, this system also includes a sophisticated water recirculation

In studies with male shrimps *C. caementarius* in individual containers installed in aquaria and tanks with recirculation system with water and biological filters, growth is evaluated by eyestalk ablation [51] per culturing at different water hardness [52] and by different inputs used in the diet such as paprika [46], yeast [53], common salt [54], biological silage [55], and soya lecithin [56]. Survival of >90% are obtained in all these investigations, which demonstrates the effectiveness of the culture system by avoiding the physical interaction and cannibalism of river shrimp. In similar culture conditions, survivals between 71 and 83% in *C. tenuimanus* [38] and 96% in *C. quadricarinatus* [39] are achieved. However, the system requires individual containers to be improved with regard to handling molting, feed system, monitoring of the species, the recirculation system automation, and use in seminatural ponds. In the same way, the individual containers are not only useful for enhancing the growth of *C. caementarius*, but also for the management of female reproduction, and in the case of shrimp males, also for selecting those with the highest rates of specific

) for the purposes of genetic improvement.

*Color of the C. caementarius body after culturing in individual containers: (A) female of normal color;* 

*(B) female depigmented; (C) male of normal color; and (D) male depigmented.*

) [12] and in the diet (300 mg kg<sup>−</sup><sup>1</sup>

study must be made to know the feasibility of shrimp farming in the system. However, the cultivation of *C. caementarius* in individual containers causes loss of body color and of cephalothoracic appendages (**Figure 4**), but the use of

[39]. Future research should

) improves

**56**

**Figure 4.**

The co-culturing is done out with two species share a common aquatic environment (aquarium, tank, or pond), but whose construction does not allow physical interaction between organisms because they remain separate, and therefore, both species are a major management factor. Instead, in the polyculture, two or three species within the aquatic environment interact constantly competing for space and food, and therefore only one species is the main one.

Combinations of species in a co-culturing allow maximizing the performance of those who are territorial and aggressive. The co-culture of *Oreochromis niloticus* in cages inside ponds with *M. rosenbergii* [57] is well known. Also, it is known to co-culture of *C. caementarius* male shrimp in individual containers inside aquariums with *O. niloticus* fingerlings (**Figure 5**), where tilapia production was estimated at 0.511 kg m<sup>−</sup><sup>3</sup> . The tilapia consumed only food that came out of the shrimp culture container [12]. In other researches, co-culture of *C. caementarius* shrimp with tilapia *O. niloticus* at different densities were performed [58], and co-culturing shrimp with tilapia was performed to evaluate different concentrations of biological silage [55]. In both cases, 100% survival was achieved and production of species is improved. Co-cultivation of shrimp/tilapia mainly generates high nitrates that may be used in the cultivation of vegetables, whose integration would result in an aquaponics system.

#### **Figure 5.**

*(A) Co-culture of C. caementarius in individual containers with O. niloticus. (B) System of co-culture in aquarium. (C) Co-culture system in fiberglass tank.*

#### **7. Transportation of adult shrimp**

The communal transport of male adult shrimps *C. caementarius* for fattening purposes is difficult due to the increased interaction causing injuries, chelipeds loss, shrimp death mainly of those who are about to carry out ecdysis or those who molt during the transport. In addition, the increased mortality depends on the density and transport time; but water temperature is a dominant factor that affects shrimp during transport [59].

The transport of adult *C. caementarius* shrimps in individual containers is performed by using plastic cups where a shrimp (≥4 cm of total length) is introduced into each plastic cup (250 mL). The plastic cup has holes to allow the water flow (**Figure 6A**). Then, all plastic cups are conditioned in plastic containers (45 L) with water of river (**Figure 6B**) and with either continuous or intermittent aeration (**Figure 6C**). The average water temperature is around 20°C. This system allows to transport 77 shrimps (17 shrimps for 10 L) per container for 5 h and with 100% survival [12]. However, the ideal size of transporting cups of live shrimps has not been studied, but as they support very small physical space, it is possible to use smaller plastic cups or to use PVC pipes according to the animal size.

#### **Figure 6.**

*Transport system of live shrimps of C. caementarius. (A) Plastic cup with a shrimp. (B) Plastic cups put into a plastic container. (C) Aerator system.*

On the other hand, the conventional transport of *C. caementarius*, an adult shrimp of 6 cm of total length, is also carried out in 4‰ of water salinity, because with this salinity, the shrimps do not show interaction or cannibalism and all survive in these conditions for 45 days [60]. The *M. rosenbergii* broodstock are transported in containers with brackish water (12‰), with oxygen and at low temperature to reduce metabolism, thus obtaining mortalities <10% [61]. In addition, aerated plastic barrels, or trucks with aerated water tanks, are used [62]. Other techniques such as increasing air humidity, the use of refrigerated sawdust or chips, and purging to reduce nitrogenous waste have been developed to increase the survival during transportation of live specimens of shrimp, prawns, lobsters, and crabs [63].

#### **8. Conclusions**

The male shrimps *C. caementarius* are aggressive for having one of the chelipeds more developed, causing greater interaction and cannibalism in any culture system. Female shrimps are less aggressive. To reduce interaction and shrimp cannibalism, two management systems are proposed. For postlarvae, using brackish water (12‰) keeps high survival (>85%) but only in the initial culture which lasts for 50 days. For the fattening of adult males, growing in individual containers conditioned in multiple levels allows high survival (87 and 100%) and yields between 0.7 and 1.0 kg m<sup>−</sup><sup>2</sup> . Furthermore, in this system, the co-culture of shrimp/tilapia is also performed to maximize performance. It is still required to demonstrate the technical and economic feasibility of fattening male shrimp in individual containers within seminatural ponds.

#### **Acknowledgements**

The author would like to thank the Department of Biology, Microbiology, and Biotechnology of the Faculty of Sciences of the National University of Santa, for allowing the use of laboratories and instruments and equipment for conducting various investigations.

**59**

**Author details**

Walter Reyes A.

Universidad Nacional del Santa, Chimbote, Perú

provided the original work is properly cited.

\*Address all correspondence to: wreyes@uns.edu.pe

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater…*

*DOI: http://dx.doi.org/10.5772/intechopen.87438*

#### **Conflict of interest**

The author has no conflict of interest.

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater… DOI: http://dx.doi.org/10.5772/intechopen.87438*

#### **Author details**

*Crustacea*

**Figure 6.**

*plastic container. (C) Aerator system.*

**8. Conclusions**

**Acknowledgements**

various investigations.

**Conflict of interest**

The author has no conflict of interest.

On the other hand, the conventional transport of *C. caementarius*, an adult shrimp of 6 cm of total length, is also carried out in 4‰ of water salinity, because with this salinity, the shrimps do not show interaction or cannibalism and all survive in these conditions for 45 days [60]. The *M. rosenbergii* broodstock are transported in containers with brackish water (12‰), with oxygen and at low temperature to reduce metabolism, thus obtaining mortalities <10% [61]. In addition, aerated plastic barrels, or trucks with aerated water tanks, are used [62]. Other techniques such as increasing air humidity, the use of refrigerated sawdust or chips, and purging to reduce nitrogenous waste have been developed to increase the survival during

*Transport system of live shrimps of C. caementarius. (A) Plastic cup with a shrimp. (B) Plastic cups put into a* 

transportation of live specimens of shrimp, prawns, lobsters, and crabs [63].

The male shrimps *C. caementarius* are aggressive for having one of the chelipeds more developed, causing greater interaction and cannibalism in any culture system. Female shrimps are less aggressive. To reduce interaction and shrimp cannibalism, two management systems are proposed. For postlarvae, using brackish water (12‰) keeps high survival (>85%) but only in the initial culture which lasts for 50 days. For the fattening of adult males, growing in individual containers conditioned in multiple levels allows high survival (87 and 100%) and yields between 0.7 and 1.0 kg m<sup>−</sup><sup>2</sup>

Furthermore, in this system, the co-culture of shrimp/tilapia is also performed to maximize performance. It is still required to demonstrate the technical and economic feasibility of fattening male shrimp in individual containers within seminatural ponds.

The author would like to thank the Department of Biology, Microbiology, and Biotechnology of the Faculty of Sciences of the National University of Santa, for allowing the use of laboratories and instruments and equipment for conducting

.

**58**

Walter Reyes A. Universidad Nacional del Santa, Chimbote, Perú

\*Address all correspondence to: wreyes@uns.edu.pe

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

#### **References**

[1] Méndez M. Claves de identificación y distribución de los langostinos y camarones (Crustacea: Decapoda) del mar y ríos de la costa del Perú. Boletín Instituto del Mar del Perú. 1981;**5**:1-170

[2] Zacarías S, Yépez V. Camarón de río *Cryphiops caementarius* (Molina, 1782) en la costa centro-sur del Perú, 2007. Informe Instituto del Mar del Perú. 2015;**42**(3):398-415

[3] Produce (Ministerio de Producción). Anuario estadístico pesquero y acuícola 2016. Perú: Ministerio de la Producción; 2017. p. 42

[4] Carrillo AA, Pacora A, Risco RA, Zerpa R. Plan estratégico para el camarón de río [tesis]. Lima: Pontificia Universidad Católica del Perú; 2012

[5] Moscoso V. Catálogo de crustáceos decápodos y estomatópodos del Perú. Boletín Instituto del Mar del Perú. 2012;**27**:1-209

[6] Bahamonde N, Carvacho A, Jara C, López M, Ponce F, Retamal MA, et al. Categorías de conservación de decápodos nativos de aguas continentales de Chile. Boletín del Museo Nacional de Historia Natural del Paraguay. 1998;**47**:91-100

[7] Hobbs HH. Biogeography of subterranean decapods in north and central America and the Caribbean region (Caridea, Astacidea, Brachyura). Hydrobiologia. 1994;**287**:95-104

[8] Villalobos JL, Nates JC, Díaz AC. Revisión de los géneros *Cryphiops* Dana, 1852 y *Bithynops* holthuis, 1973, de la familia Palaemonidae (Crustacea, Decapoda), y descripción de una especie nueva para el estado de Chiapas, México. Anales del Instituto de Biología, Universidad Nacional Autónoma de México. Serie Zoología. 1989;**60**(2):159-184

[9] Gomes MM. Descrição de uma espécie nova do género *Cryphiops* (Decapoda, Natantia, Palaemonidae). Revista Brasileira de Biologia. 1973;**33**(2):169-173

[10] Romano N, Zeng C. Cannibalism of decapod crustaceans and implications for their aquaculture: A review of its prevalence, influencing factors, and mitigating methods. Reviews in Fisheries Science & Aquaculture. 2017;**25**(1):42-69. DOI: 10.1080/23308249.2016.1221379

[11] Mariappan P, Balasundaram C, Schmithz B. Decapod crustacean chelipeds: An overview. Journal of Biosciences. 2000;**25**(3):301-313

[12] Reyes W. Engorde del camarón nativo de los ríos costeros del Perú. Un estudio en sistema de recipientes individuales y con recirculación de agua. Alemania: Publicia; 2016. 89 p

[13] Rodríguez A. Hábitos alimentarios de las jaibas *Callinectes bellicosus* STIMPSON y *C. arcuatus* ORDWAY (Brachiura: Portunidae) en Bahía Magdalena, Baja California Sur México [tesis]. La Paz, Baja California Sur, México: Instituto Politécnico Nacional Centro Interdisciplinario de Ciencias Marinas; 2014

[14] Zúñiga O, Ramos R. Balance energético en juveniles de *Cryphiops caementarius* (Crustacea, Palaemonidae). Biota. 1987;**3**:33-43

[15] Barki A, Harpaz S, Karplus I. Contradictory asymmetries in body and weapon size, and assessment in fighting male prawns, *Macrobrachium rosenbergii*. Aggresive Behavior. 1997;**23**:81-91

[16] Barki A, Karplus I, Goren M. Effects of size and morphotype on dominance hierarchies and resource competition in

**61**

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater…*

[25] Shivananda H, Kumarswamy R, Palaksha KJ, Sujatha HR, Shankar R. Effect of different types of shelters on survival and growth of giant freshwater prawn, *Macrobrachium rosenbergii*. Journal of Marine Science and Technology. 2012;**20**(2):153-157

[26] Santos DB, Pontes CS, Campos PMO, Arruda MF. Behavioral profile of *Macrobrachium rosenbergii* in mixed and monosex culture submitted to shelters of different colors. Acta Scientiarum. Biological Sciences. 2015;**37**(3):273-279

[27] Mamun MAA, Hossain MA,

2010;**8**(2):333-340

2010;**310**:84-90

Hossain MS, Ali ML. Effects of different types of artificial substrates on nursery production of freshwater prawn, *Macrobrachium rosenbergii* (de Man) in recirculatory system. Journal of the Bangladesh Agricultural University.

[28] Tuly DM, Islam MS, Hasnahena M, Hasan MR, Hasan MT. Use of artificial substrate in pond culture of freshwater prawn (*Macrobrachium rosenbergii*): A new approach regarding growth performance and economic return. Journal of Fisheries. 2014;**2**(1):53-58

[29] Laranja JLQ, Quinitio ET, Catacutan MR, Coloso RM. Effects of dietary L-tryptophan on the agonistic behavior, growth and survival of juvenile mud crab *Scylla serrata*. Aquaculture.

[30] Coyle SD, Alston DE, Sampaio

management. In: New MB, Valenti WC, Tidwell JH, D'Abramo LR, Kutty MN, editors. Freshwater Prawn. Biology and Farming. United Kingdom: Wiley-

[31] Reyes WE, Bacilio S, Villavicencio M, Mendoza R. Efecto de la salinidad en el crecimiento y supervivencia de postlarvas del camarón de río *Cryphiops caementarius* Molina, 1782 (Crustacea, Palaemonidae), en laboratorio.

CMS. Nursery systems and

Blackwell; 2010. pp. 108-126

*DOI: http://dx.doi.org/10.5772/intechopen.87438*

the freshwater prawn *Macrobrachium rosenbergii*. Animal Behaviour.

[17] Santos DB, Pontes CS. Behavioral repertoire of the giant freshwater prawn *Macrobrachium rosenbergii* (De Man, 1879) in laboratory. Journal of Animal Behaviour and Biometeorology.

[18] Fox LR. Cannibalism in natural population. Annual Review of Ecology

and Systematics. 1975;**6**:87-106

[19] Polis GA. The evolution and dynamics of intraspecific predation. Annual Review of Ecology, Evolution, and Systematics. 1981;**12**:225-251

[20] Dennell R. Integument and exoekeleton. In: Waterman TH, editor. The Physiology of Crustacea. Metabolismo and Growth. Vol. 1. Cambridge: Academic Press; 1960.

[21] Adams JA, Moore PA. Discrimination of conspecific male molt odor signals by male crayfish *Orconectes rusticus*. Journal of Crustacean Biology. 2003;**23**(1):7-14

[22] Tran MV. The scent of cannibalism: The olfactory basis of cannibalism in hermit crabs. Journal of Experimental

Marine Biology and Ecology.

Pesca. 1977;**1**(159):240-248

Nacional de Trujillo; 2008

[23] Ponce JE. Importancia del flujo de agua en los estanques-criaderos de camarón. Actas del Simposio sobre Acuicultura en América Latina,

Montevideo, Uruguay, 26 de noviembre a 2 de diciembre de 1974. Documentos de Investigación. FAO, Informes de

[24] Reyes WE. Efecto de dos probióticos bioencapsulados en nauplios de *Artemia franciscana* en el desarrollo larval del camarón de río *Cryphiops caementarius*, en laboratorio [tesis]. Perú: Universidad

1992;**44**(3):547-555

2016;**4**(4):109-115

pp. 447-472

2014;**457**:8-14

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater… DOI: http://dx.doi.org/10.5772/intechopen.87438*

the freshwater prawn *Macrobrachium rosenbergii*. Animal Behaviour. 1992;**44**(3):547-555

[17] Santos DB, Pontes CS. Behavioral repertoire of the giant freshwater prawn *Macrobrachium rosenbergii* (De Man, 1879) in laboratory. Journal of Animal Behaviour and Biometeorology. 2016;**4**(4):109-115

[18] Fox LR. Cannibalism in natural population. Annual Review of Ecology and Systematics. 1975;**6**:87-106

[19] Polis GA. The evolution and dynamics of intraspecific predation. Annual Review of Ecology, Evolution, and Systematics. 1981;**12**:225-251

[20] Dennell R. Integument and exoekeleton. In: Waterman TH, editor. The Physiology of Crustacea. Metabolismo and Growth. Vol. 1. Cambridge: Academic Press; 1960. pp. 447-472

[21] Adams JA, Moore PA. Discrimination of conspecific male molt odor signals by male crayfish *Orconectes rusticus*. Journal of Crustacean Biology. 2003;**23**(1):7-14

[22] Tran MV. The scent of cannibalism: The olfactory basis of cannibalism in hermit crabs. Journal of Experimental Marine Biology and Ecology. 2014;**457**:8-14

[23] Ponce JE. Importancia del flujo de agua en los estanques-criaderos de camarón. Actas del Simposio sobre Acuicultura en América Latina, Montevideo, Uruguay, 26 de noviembre a 2 de diciembre de 1974. Documentos de Investigación. FAO, Informes de Pesca. 1977;**1**(159):240-248

[24] Reyes WE. Efecto de dos probióticos bioencapsulados en nauplios de *Artemia franciscana* en el desarrollo larval del camarón de río *Cryphiops caementarius*, en laboratorio [tesis]. Perú: Universidad Nacional de Trujillo; 2008

[25] Shivananda H, Kumarswamy R, Palaksha KJ, Sujatha HR, Shankar R. Effect of different types of shelters on survival and growth of giant freshwater prawn, *Macrobrachium rosenbergii*. Journal of Marine Science and Technology. 2012;**20**(2):153-157

[26] Santos DB, Pontes CS, Campos PMO, Arruda MF. Behavioral profile of *Macrobrachium rosenbergii* in mixed and monosex culture submitted to shelters of different colors. Acta Scientiarum. Biological Sciences. 2015;**37**(3):273-279

[27] Mamun MAA, Hossain MA, Hossain MS, Ali ML. Effects of different types of artificial substrates on nursery production of freshwater prawn, *Macrobrachium rosenbergii* (de Man) in recirculatory system. Journal of the Bangladesh Agricultural University. 2010;**8**(2):333-340

[28] Tuly DM, Islam MS, Hasnahena M, Hasan MR, Hasan MT. Use of artificial substrate in pond culture of freshwater prawn (*Macrobrachium rosenbergii*): A new approach regarding growth performance and economic return. Journal of Fisheries. 2014;**2**(1):53-58

[29] Laranja JLQ, Quinitio ET, Catacutan MR, Coloso RM. Effects of dietary L-tryptophan on the agonistic behavior, growth and survival of juvenile mud crab *Scylla serrata*. Aquaculture. 2010;**310**:84-90

[30] Coyle SD, Alston DE, Sampaio CMS. Nursery systems and management. In: New MB, Valenti WC, Tidwell JH, D'Abramo LR, Kutty MN, editors. Freshwater Prawn. Biology and Farming. United Kingdom: Wiley-Blackwell; 2010. pp. 108-126

[31] Reyes WE, Bacilio S, Villavicencio M, Mendoza R. Efecto de la salinidad en el crecimiento y supervivencia de postlarvas del camarón de río *Cryphiops caementarius* Molina, 1782 (Crustacea, Palaemonidae), en laboratorio.

**60**

1989;**60**(2):159-184

*Crustacea*

**References**

[1] Méndez M. Claves de identificación y distribución de los langostinos y camarones (Crustacea: Decapoda) del mar y ríos de la costa del Perú. Boletín Instituto del Mar del Perú. 1981;**5**:1-170 [9] Gomes MM. Descrição de uma espécie nova do género *Cryphiops* (Decapoda, Natantia, Palaemonidae).

[10] Romano N, Zeng C. Cannibalism

implications for their aquaculture: A review of its prevalence, influencing factors, and mitigating methods. Reviews in Fisheries Science & Aquaculture. 2017;**25**(1):42-69. DOI: 10.1080/23308249.2016.1221379

[11] Mariappan P, Balasundaram C, Schmithz B. Decapod crustacean chelipeds: An overview. Journal of Biosciences. 2000;**25**(3):301-313

[12] Reyes W. Engorde del camarón nativo de los ríos costeros del Perú. Un estudio en sistema de recipientes individuales y con recirculación de agua.

[13] Rodríguez A. Hábitos alimentarios de las jaibas *Callinectes bellicosus* STIMPSON y *C. arcuatus* ORDWAY (Brachiura: Portunidae) en Bahía Magdalena, Baja California Sur México [tesis]. La Paz, Baja California Sur, México: Instituto Politécnico Nacional Centro Interdisciplinario de Ciencias

Alemania: Publicia; 2016. 89 p

[14] Zúñiga O, Ramos R. Balance energético en juveniles de

*Cryphiops caementarius* (Crustacea, Palaemonidae). Biota. 1987;**3**:33-43

[15] Barki A, Harpaz S, Karplus I. Contradictory asymmetries in body and weapon size, and assessment in fighting male prawns, *Macrobrachium rosenbergii*. Aggresive Behavior.

[16] Barki A, Karplus I, Goren M. Effects of size and morphotype on dominance hierarchies and resource competition in

Marinas; 2014

1997;**23**:81-91

Revista Brasileira de Biologia.

of decapod crustaceans and

1973;**33**(2):169-173

[2] Zacarías S, Yépez V. Camarón de río *Cryphiops caementarius* (Molina, 1782) en la costa centro-sur del Perú, 2007. Informe Instituto del Mar del Perú.

[3] Produce (Ministerio de Producción). Anuario estadístico pesquero y acuícola 2016. Perú: Ministerio de la Producción;

[4] Carrillo AA, Pacora A, Risco RA, Zerpa R. Plan estratégico para el camarón de río [tesis]. Lima: Pontificia Universidad Católica del Perú; 2012

[5] Moscoso V. Catálogo de crustáceos decápodos y estomatópodos del Perú. Boletín Instituto del Mar del Perú.

[6] Bahamonde N, Carvacho A, Jara C, López M, Ponce F, Retamal MA, et al. Categorías de conservación de decápodos nativos de aguas continentales de Chile. Boletín del Museo Nacional de Historia Natural del

Paraguay. 1998;**47**:91-100

[7] Hobbs HH. Biogeography of subterranean decapods in north and central America and the Caribbean region (Caridea, Astacidea, Brachyura).

Hydrobiologia. 1994;**287**:95-104

[8] Villalobos JL, Nates JC, Díaz AC. Revisión de los géneros *Cryphiops* Dana, 1852 y *Bithynops* holthuis, 1973, de la familia Palaemonidae (Crustacea, Decapoda), y descripción de una especie nueva para el estado de Chiapas, México. Anales del Instituto de Biología, Universidad Nacional Autónoma de México. Serie Zoología.

2015;**42**(3):398-415

2017. p. 42

2012;**27**:1-209

Comunicación Científica. In: IV Congreso Iberoamericano Virtual de Acuicultura CIVA 2006; Zaragoza, España. 2006. pp. 341-346

[32] Cano F, Carrión S, Reyes W. Efecto de altas densidades de siembra en el crecimiento y supervivencia de postlarvas de *Cryphiops caementarius* (Crustacea: Palaemonidae) en agua salobre. Revista Citecsa. 2014;**5**(8):62-78

[33] Vega-Villasante F, Galavíz-Parada JD, Guzmán-Arroyo M, Flores CA, Espinosa-Chaurand LD. Efecto de diferentes salinidades sobre el crecimiento y supervivencia de juveniles del langostino de río *Macrobrachium tenellum* (Smith, 1871). Zootecnia Tropical. 2011;**29**(4):467-473

[34] Chand BK, Trivedi RK, Dubey SK, Rout SK, Beg MM, Das UK. Effect of salinity on survival and growth of giant freshwater prawn *Macrobrachium rosenbergii* (de Man). Aquaculture Reports. 2015;**2**:26-33. DOI: 10.1016/j. aqrep.2015.05.002

[35] Ponce JE, Eguren MC. Evaluación del crecimiento del camarón de río *Cryphiops caementarius* (Molina) en una poza piloto en Camaná. Véritas. 2005;**9**(1):95-101

[36] Shleser RA. The effects of feeding frequency and space on the growth of the American lobster, *Homarus americanus*. Journal of the World Aquaculture Society. 1974;**5**(1-4):149-155

[37] Van Olst JC, Carlberg JM. The effects on container size and transparency on growth and survival of lobster cultured individually. Proceeding of the Annual Meeting– World Mariculture Society. 1978;**9**(1-4):469-479

[38] Jussila J. Physiological responses of astacid and parastacid crayfishes (Crustacea: Decapoda) to conditions of intensive culture [tesis]. Australia: University of Kuopio; 1977

[39] Manor R, Segev R, Pimenta M, Aflalo ED, Sagi A. Intensification of redclaw crayfish *Cherax quadricarinatus* culture II. Growout in a separate cell system. Aquaculture Engineering. 2002;**26**:263-276

[40] Ford RF, Van Olst JC, Calberg JM, Dorband WR, Johnson RL. Beneficial use thermal effluent in lobster culture. Journal of the World Aquaculture Society. 1975;**6**(1-4):509-519

[41] Kristiansen TS, Drengstig A, Bergheim A, Drengstin T, Svensen R, Kollsgård I, et al. Development of methods for intensive farming of European lobster in recirculated seawater. Results from experiments conducted at Kvitsay lobster hatchery from 2000 to 2004. Fisken og havet. 2004;**6**:1-52

[42] Daniels CL, Wills B, Ruiz-Perez M, Miles E, Wilson RW, Boothroyd D. Development of sea based container culture for rearing European lobster (*Homarus gammarus*) around south west England. Aquaculture. 2015;**448**:186-195

[43] Reyes WE. Crecimiento, reproducción y supervivencia de hembras del camarón de río *Cryphiops caementarius* criados en recipientes individuales. Sciéndo. 2011;**14**(1-2):75-86

[44] Geddes MC, Mills BJ, Walker KF. Growth in the Australian freshwater crayfish *Cherax destructor c*lark, under laboratory conditions. Australian Journal of Marine & Freshwater Research. 1988;**39**:555-568

[45] New MB. Farming freshwater prawn. A manual for the culture of the giant river prawn (*Macrobrachium rosenbergii*). FAO Fisheries Technical Paper. 2002;**428**:1-212

**63**

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater…*

laboratorio [tesis], Perú. Universidad

[54] Ramirez M, Cántaro R, Reyes W. Growth and survival of males of *Cryphiops caementarius* (Palaemonidae) with diets supplemented with common salt. Latin American Journal Aquatic Research. 2018;**46**(2):469-474. DOI: 10.3856/vol46-issue2-fulltext-22

[55] Terrones S, Reyes W. Efecto de dietas con ensilado biológico de residuos de molusco en el crecimiento del camarón *Cryphiops caementarius* y tilapia *Oreochromis niloticus* en co-cultivo intensivo. Scientia Agropecuaria, 2018;**9**(2):167-176. DOI: 10.17268/sci.agropecu.2018.02.01

[56] Acosta A, Quiñones D, Reyes W. Efecto de dietas con lecitina de soya en el crecimiento, muda y supervivencia

de machos del camarón de río *Cryphiops caementarius* (Crustacea: Palaemonidae). Scientia Agropecuaria. 2018;**9**(1):143-151. DOI: 10.17268/sci.

[57] Danaher J, Tidwell J, Coyle S, Dasgupta D. Effects of two densities of caged monosex nile tilapia,

Society. 2007;**38**(3):367-382

[58] Mogollón AV. Cocultivo de machos del camarón de río *Cryphiops caementarius* en recipientes individuales dentro de acuario con machos de *Oreochromis niloticus* a diferentes densidades de siembra y sus efectos

*Oreochromis niloticus*, on water quality, phytoplankton populations, and production when polyculture with *Macrobrachium rosenbergii* in temperate pond. Journal of the World Aquaculture

agropecu.2018.01.15

[53] Cornejo J, Pérez L, Reyes W. Effect of *Saccharomyces cerevisiae* yeast in the diet of male shrimp *Cryphiops caementarius* (Crustacea, Palaemonidae) on total and differential hemocytes count. Revista Bio Ciencias.

Nacional del Santa; 2015

2015;**3**(3):173-186

*DOI: http://dx.doi.org/10.5772/intechopen.87438*

[46] Fuentes AS, Quezada LJ. Efecto de diferentes concentraciones de harina de *Calendula officinalis* "marigold" en la pigmentación de camarones machos adultos de *Cryphiops caementarius* [tesis]. Perú: Universidad Nacional del

[47] Meyers SP. Papel del carotenoide astaxantina en nutrición de especies acuáticas. In: Civera-Cerecedo R, Pérez-Estrada CJ, Ricque-Marie D, Cruz-Suárez LE, editors. Avances en Nutrición Acuícola IV. Memorias del IV Simposium Internacional de Nutrición Acuícola; 1998; La Paz, B.C.S., México.

[48] Wickins JF, Jones E, Beard TW, Edwards DB. Food distribution equipament for individuallyhoused juvenile lobster (*Homarus* spp.). Aquaculture Engineering.

[49] Drengstig A, Bergheim A. Commercial land-based farming of European lobster (*Homarus gammarus* L.) in recirculating aquaculture system (RAS) using a single cage approach. Aquacultural Engineering.

[50] Shelley C, Lovatelli A. Mude crab aquaculture. A practical manual. In: FAO Fisheries and Aquaculture Technical Paper. Vol. 567. 2011. pp. 1-78

[51] Pérez RA, Tinoco KL. Cocultivo de machos del camarón de río *Cryphiops* 

pedúnculo ocular criados en recipientes individuales dentro de tanques con machos de tilapia *Oreochromis niloticus* y su efecto en el crecimiento de las especies [tesis]. Perú: Universidad

[52] Graciano FP, Vásquez JF. Efecto de diferentes niveles de dureza del agua en la muda, crecimiento y supervivencia de adultos del camarón ede río *Cryphiops caementarius* en condiciones de

*caementarius* con ablación del

Nacional del Santa; 2013

Santa; 2015

2000. pp. 473-491

1987;**6**:277-288

2013;**53**:14-18

*Management of the Interaction and Cannibalism of Postlarvae and Adults of the Freshwater… DOI: http://dx.doi.org/10.5772/intechopen.87438*

[46] Fuentes AS, Quezada LJ. Efecto de diferentes concentraciones de harina de *Calendula officinalis* "marigold" en la pigmentación de camarones machos adultos de *Cryphiops caementarius* [tesis]. Perú: Universidad Nacional del Santa; 2015

*Crustacea*

Comunicación Científica. In: IV Congreso Iberoamericano Virtual de Acuicultura CIVA 2006; Zaragoza,

[32] Cano F, Carrión S, Reyes W. Efecto de altas densidades de siembra en el crecimiento y supervivencia de postlarvas de *Cryphiops caementarius* (Crustacea: Palaemonidae) en agua salobre. Revista Citecsa. 2014;**5**(8):62-78 of intensive culture [tesis]. Australia:

[39] Manor R, Segev R, Pimenta M, Aflalo ED, Sagi A. Intensification of redclaw crayfish *Cherax quadricarinatus* culture II. Growout in a separate cell system. Aquaculture Engineering.

[40] Ford RF, Van Olst JC, Calberg JM, Dorband WR, Johnson RL. Beneficial use thermal effluent in lobster culture. Journal of the World Aquaculture Society. 1975;**6**(1-4):509-519

[41] Kristiansen TS, Drengstig A, Bergheim A, Drengstin T, Svensen R, Kollsgård I, et al. Development of methods for intensive farming of European lobster in recirculated seawater. Results from experiments conducted at Kvitsay lobster hatchery from 2000 to 2004. Fisken og havet.

[42] Daniels CL, Wills B, Ruiz-Perez M, Miles E, Wilson RW, Boothroyd D. Development of sea based container culture for rearing European lobster (*Homarus gammarus*) around south west England. Aquaculture.

University of Kuopio; 1977

2002;**26**:263-276

2004;**6**:1-52

2015;**448**:186-195

2011;**14**(1-2):75-86

[43] Reyes WE. Crecimiento, reproducción y supervivencia de hembras del camarón de río *Cryphiops caementarius* criados en recipientes individuales. Sciéndo.

[44] Geddes MC, Mills BJ, Walker KF. Growth in the Australian freshwater crayfish *Cherax destructor c*lark, under laboratory conditions. Australian Journal of Marine & Freshwater Research. 1988;**39**:555-568

[45] New MB. Farming freshwater prawn. A manual for the culture of the giant river prawn (*Macrobrachium rosenbergii*). FAO Fisheries Technical

Paper. 2002;**428**:1-212

[33] Vega-Villasante F, Galavíz-Parada JD, Guzmán-Arroyo M, Flores CA, Espinosa-Chaurand LD. Efecto de diferentes salinidades sobre el

crecimiento y supervivencia de juveniles del langostino de río *Macrobrachium tenellum* (Smith, 1871). Zootecnia Tropical. 2011;**29**(4):467-473

[34] Chand BK, Trivedi RK, Dubey SK, Rout SK, Beg MM, Das UK. Effect of salinity on survival and growth of giant freshwater prawn *Macrobrachium rosenbergii* (de Man). Aquaculture Reports. 2015;**2**:26-33. DOI: 10.1016/j.

[35] Ponce JE, Eguren MC. Evaluación del crecimiento del camarón de río *Cryphiops caementarius* (Molina) en una poza piloto en Camaná. Véritas.

[36] Shleser RA. The effects of feeding frequency and space on the growth of the American lobster, *Homarus americanus*. Journal of the World Aquaculture Society.

[37] Van Olst JC, Carlberg JM. The effects on container size and

World Mariculture Society. 1978;**9**(1-4):469-479

transparency on growth and survival of lobster cultured individually. Proceeding of the Annual Meeting–

[38] Jussila J. Physiological responses of astacid and parastacid crayfishes (Crustacea: Decapoda) to conditions

aqrep.2015.05.002

2005;**9**(1):95-101

1974;**5**(1-4):149-155

España. 2006. pp. 341-346

**62**

[47] Meyers SP. Papel del carotenoide astaxantina en nutrición de especies acuáticas. In: Civera-Cerecedo R, Pérez-Estrada CJ, Ricque-Marie D, Cruz-Suárez LE, editors. Avances en Nutrición Acuícola IV. Memorias del IV Simposium Internacional de Nutrición Acuícola; 1998; La Paz, B.C.S., México. 2000. pp. 473-491

[48] Wickins JF, Jones E, Beard TW, Edwards DB. Food distribution equipament for individuallyhoused juvenile lobster (*Homarus* spp.). Aquaculture Engineering. 1987;**6**:277-288

[49] Drengstig A, Bergheim A. Commercial land-based farming of European lobster (*Homarus gammarus* L.) in recirculating aquaculture system (RAS) using a single cage approach. Aquacultural Engineering. 2013;**53**:14-18

[50] Shelley C, Lovatelli A. Mude crab aquaculture. A practical manual. In: FAO Fisheries and Aquaculture Technical Paper. Vol. 567. 2011. pp. 1-78

[51] Pérez RA, Tinoco KL. Cocultivo de machos del camarón de río *Cryphiops caementarius* con ablación del pedúnculo ocular criados en recipientes individuales dentro de tanques con machos de tilapia *Oreochromis niloticus* y su efecto en el crecimiento de las especies [tesis]. Perú: Universidad Nacional del Santa; 2013

[52] Graciano FP, Vásquez JF. Efecto de diferentes niveles de dureza del agua en la muda, crecimiento y supervivencia de adultos del camarón ede río *Cryphiops caementarius* en condiciones de

laboratorio [tesis], Perú. Universidad Nacional del Santa; 2015

[53] Cornejo J, Pérez L, Reyes W. Effect of *Saccharomyces cerevisiae* yeast in the diet of male shrimp *Cryphiops caementarius* (Crustacea, Palaemonidae) on total and differential hemocytes count. Revista Bio Ciencias. 2015;**3**(3):173-186

[54] Ramirez M, Cántaro R, Reyes W. Growth and survival of males of *Cryphiops caementarius* (Palaemonidae) with diets supplemented with common salt. Latin American Journal Aquatic Research. 2018;**46**(2):469-474. DOI: 10.3856/vol46-issue2-fulltext-22

[55] Terrones S, Reyes W. Efecto de dietas con ensilado biológico de residuos de molusco en el crecimiento del camarón *Cryphiops caementarius* y tilapia *Oreochromis niloticus* en co-cultivo intensivo. Scientia Agropecuaria, 2018;**9**(2):167-176. DOI: 10.17268/sci.agropecu.2018.02.01

[56] Acosta A, Quiñones D, Reyes W. Efecto de dietas con lecitina de soya en el crecimiento, muda y supervivencia de machos del camarón de río *Cryphiops caementarius* (Crustacea: Palaemonidae). Scientia Agropecuaria. 2018;**9**(1):143-151. DOI: 10.17268/sci. agropecu.2018.01.15

[57] Danaher J, Tidwell J, Coyle S, Dasgupta D. Effects of two densities of caged monosex nile tilapia, *Oreochromis niloticus*, on water quality, phytoplankton populations, and production when polyculture with *Macrobrachium rosenbergii* in temperate pond. Journal of the World Aquaculture Society. 2007;**38**(3):367-382

[58] Mogollón AV. Cocultivo de machos del camarón de río *Cryphiops caementarius* en recipientes individuales dentro de acuario con machos de *Oreochromis niloticus* a diferentes densidades de siembra y sus efectos

en el crecimiento y supervivencia de las especies [tesis]. Perú. Universidad Nacional del Santa; 2013

[59] Coyle SD, Tidwell JH, Yasharian DK, Caporelli A, Skudlarek NA. The effect of biomass density, temperature, and substrate on transport survival of market-size freshwater prawn, *Macrobrachium rosenbergii*. Journal of Applied Aquaculture. 2005;**17**(4):61-71. DOI: 10.1300/J028v17n04\_04

[60] Escobar C, Pachamoro MA, Reyes W. Supervivencia y crecimiento de machos adultos del camarón de río *Cryphiops caementarius* Molina 1782 (Crustacea, Palaemonidae) expuestos a salinidades. Ecología Aplicada. 2017;**16**(2):75-82. DOI: 10.21704/rea. v16i2.1010

[61] Ahmed N. Freshwater prawn hatcheries in Bangladesh: Concern of broodstock. Aquaculture Asia Magazine, July-September, 2008. pp. 22-26

[62] Yang G, Frinsko M, Chen X, Wang J, Hu G, Gao Q. Current status of the giant freshwater prawn (*Macrobrachium rosenbergii*) industry in China, with special reference to live transportation. Aquaculture Research. 2012;**43**:1049-1055. DOI: 10.1111/j.1365-2109.2011.03009.x

[63] Fotedar S, Evans L. Health management during handling and live transport of crustaceans: A review. Journal of Invertebrate Pathology. 2011;**106**:143-152. DOI: 10.1016/j. jip.2010.09.011

**65**

**Chapter 5**

**Abstract**

morphs in this species.

**1. Introduction**

Bateman Gradients and

in a Marine Isopod

Alternative Mating Strategies

The "Bateman gradient" provides a means for estimating the strength of sexual selection. Although widely used for this purpose, this approach has not been applied to examine the covariance between mate numbers and offspring numbers among alternative mating strategies. Differences in this covariance could exist if the average fitnesses of different mating phenotypes were unequal, as has been suggested for "alternative mating tactics." We tested this hypothesis in *Paracerceis sculpta*, a sexually dimorphic marine isopod in which three male morphs coexist. We found no significant differences in sexual competency and no significant differences in Bateman gradients among morphs, that is, the average morph fitnesses were equivalent. However, with data pooled among morphs, we found a significant sex difference in Bateman gradients, as expected for dimorphic species; females gained no additional fitness from mating with multiple males, whereas male fitness increased with increasing mate numbers. In nature, the fitnesses of the three morphs are variable due to differences in the availability of receptive females. Our results suggest that differences in mate availability, not differences in sexual competency, are responsible for observed variance in fitness within, and for the equality of fitnesses among, the three male

**Keywords:** measuring sexual selection, male polymorphism, Crustacea, Isopoda

By definition, females produce few, large ova, whereas males produce many, tiny sperm. This sex difference in initial parental investment is widely viewed as the primary cause of sexual selection and intersexual conflict [1–4]. However, Bateman ([1], p. 363) also argued that, "Variance in number of mates is…the only important cause of the sex difference in the variance in fertility," and therefore that a sex difference in the variance in fertility provides "a measure of the sex difference in intensity of selection." This statement implies that selection within each sex, rather than between the sexes is responsible for sexual selection as well as for the evolution of sexual differences. The magnitude of the sex difference in fitness variance can be specifically quantified, not through proxies for selection intensity,

*Katharine M. Saunders and Stephen M. Shuster*

#### **Chapter 5**

*Crustacea*

v16i2.1010

pp. 22-26

en el crecimiento y supervivencia de las especies [tesis]. Perú. Universidad

[59] Coyle SD, Tidwell JH, Yasharian DK, Caporelli A, Skudlarek NA. The effect of biomass density, temperature, and substrate on transport survival of market-size freshwater prawn, *Macrobrachium rosenbergii*. Journal of Applied Aquaculture. 2005;**17**(4):61-71.

DOI: 10.1300/J028v17n04\_04

[60] Escobar C, Pachamoro MA, Reyes W. Supervivencia y crecimiento de machos adultos del camarón de río *Cryphiops caementarius* Molina 1782 (Crustacea, Palaemonidae) expuestos a salinidades. Ecología Aplicada. 2017;**16**(2):75-82. DOI: 10.21704/rea.

[61] Ahmed N. Freshwater prawn hatcheries in Bangladesh: Concern of broodstock. Aquaculture Asia Magazine, July-September, 2008.

[62] Yang G, Frinsko M, Chen X, Wang J, Hu G, Gao Q. Current status of the giant freshwater prawn (*Macrobrachium rosenbergii*) industry in China, with special reference to live transportation. Aquaculture Research. 2012;**43**:1049-1055. DOI: 10.1111/j.1365-2109.2011.03009.x

[63] Fotedar S, Evans L. Health

jip.2010.09.011

management during handling and live transport of crustaceans: A review. Journal of Invertebrate Pathology. 2011;**106**:143-152. DOI: 10.1016/j.

Nacional del Santa; 2013

**64**

## Bateman Gradients and Alternative Mating Strategies in a Marine Isopod

*Katharine M. Saunders and Stephen M. Shuster*

#### **Abstract**

The "Bateman gradient" provides a means for estimating the strength of sexual selection. Although widely used for this purpose, this approach has not been applied to examine the covariance between mate numbers and offspring numbers among alternative mating strategies. Differences in this covariance could exist if the average fitnesses of different mating phenotypes were unequal, as has been suggested for "alternative mating tactics." We tested this hypothesis in *Paracerceis sculpta*, a sexually dimorphic marine isopod in which three male morphs coexist. We found no significant differences in sexual competency and no significant differences in Bateman gradients among morphs, that is, the average morph fitnesses were equivalent. However, with data pooled among morphs, we found a significant sex difference in Bateman gradients, as expected for dimorphic species; females gained no additional fitness from mating with multiple males, whereas male fitness increased with increasing mate numbers. In nature, the fitnesses of the three morphs are variable due to differences in the availability of receptive females. Our results suggest that differences in mate availability, not differences in sexual competency, are responsible for observed variance in fitness within, and for the equality of fitnesses among, the three male morphs in this species.

**Keywords:** measuring sexual selection, male polymorphism, Crustacea, Isopoda

#### **1. Introduction**

By definition, females produce few, large ova, whereas males produce many, tiny sperm. This sex difference in initial parental investment is widely viewed as the primary cause of sexual selection and intersexual conflict [1–4]. However, Bateman ([1], p. 363) also argued that, "Variance in number of mates is…the only important cause of the sex difference in the variance in fertility," and therefore that a sex difference in the variance in fertility provides "a measure of the sex difference in intensity of selection." This statement implies that selection within each sex, rather than between the sexes is responsible for sexual selection as well as for the evolution of sexual differences. The magnitude of the sex difference in fitness variance can be specifically quantified, not through proxies for selection intensity, such as the ratio of sexually mature males to receptive females at any time (the Operational Sex Ratio, OSR [5]) or the ratio of maximum potential reproductive rates for each sex (PRR; [6]), but rather from actual estimates of selection's strength [7–12].

Such measures include the opportunity for selection (*VW/W*<sup>2</sup> = *I*; [13]), the ratio of the variance in fitness to its squared average. This parameter, when measured using the mean and variance in mate numbers for each sex and adjusted by the sex ratio, quantifies the sex difference in the opportunity for selection, that is, the opportunity for sexual selection (*IM*, [7, 8]; *Imates* [9]; *Is* [14]). Despite an early focus on mate numbers, the opportunity for sexual selection can be measured more precisely using the mean and variance in offspring numbers for each sex [9, 15, 16]. The Bateman gradient, *β*ss [14, 16–19] provides a more specific estimator of the effect of mating success on fitness, by quantifying the standardized covariance between mate number and offspring number. Jones' Index, *β*ss√*Is*, combines these parameters and appears to provide a useful correction when the opportunity for sexual selection is expressed in terms of mate numbers rather than in terms of offspring numbers [14, 20].

The Bateman gradient is among the more precise methods for measuring sexual selection because it measures the slope, *β*ss, of the statistical relationship between mate numbers and offspring numbers for members of each sex [16]. Thus, it estimates the intensity of sexual selection on the trait or traits that influence the sex difference in the variance in offspring numbers, provided that such traits can be identified. Although now widely used to compare sex differences in selection intensity [16–19, 21], the Bateman gradient has not been used to examine the covariance between mate numbers and offspring numbers among polymorphic mating phenotypes, also known as alternative mating strategies [9, 22, 23].

Polymorphisms in mating phenotype are considered by many researchers to provide examples of *fitness satisficing*, a current explanation for why alternative adult morphs persist within populations despite their experience of average fitness that is less than the average fitness of the conventional adult morph. According to this hypothesis, alternative phenotypes appear to "make the best of a bad job" [22–24]. One mechanism by which alternative phenotypes could experience lessthan-average fitness is if Bateman gradients among the adult morphs are statistically distinct.

The Gulf of California sphaeromatid isopod, *Paracerceis sculpta*, has three distinct male morphs and breeds within the spongocoels of the sponge, *Leucetta losangelensis*, (**Figure 1**). Alpha males are largest and possess enlarged uropods, used for defending breeding sites. Beta males are smaller than α-males and resemble females in behavior and body form. Gamma males are the smallest and use their small size and agility to "sneak" into spongocoels [25]. Previous results indicate that variance in fitness within each of the three male morphs is large, whereas fitness differences among morphs are minute, a necessary condition for the persistence of genetic polymorphism [26].

While the possible causes of variance in mating success within α-males are relatively well understood [27–32], the causes of within-morph fitness variance for β- and γ-males are less clear. Here, we measured Bateman gradients for α-, β-, and γ-males, and females in *P. sculpta* to determine if there is a significant difference in the covariance between mate numbers and offspring numbers for the four adult phenotypes in this species. Our results reveal the precision of this approach for measuring the difference in sexual selection intensity and suggest an alternative method for investigating fitness differences among morphs in species with sexual polymorphisms.

**67**

**2.2 Field collections**

**2. Materials and methods**

**Figure 1.**

**2.1 Sexual receptivity, mating, and gestation in** *P. sculpta*

*The α-, β-, and γ-male and female morphs in Paracerceis sculpta (redrawn from Shuster [30]).*

before being released as fully formed juveniles (mancas; [27–29]).

Females are attracted to breeding sites in sponges when their ovaries and brood pouches mature [29]. Sexual receptivity in these S1 females is initiated when they shed the posterior half of their cuticle and expose genital openings at the base of each fifth walking leg [27]. Females in S2 (half molted) condition remain receptive for 24 h before shedding their anterior cuticles, ovipositing into internal brood pouches and becoming non-receptive (S3). Females do not feed during gestation (S4–S7; [27]). Males complete a mating sequence with receptive females by inserting their appendix masculina and ejaculating into one, and then into the other of their mate's vaginas. Fertilization occurs and zygotes are brooded internally for 3 weeks

We collected several hundred isopods from the spongocoels of the intertidal sponge, *Leucetta losangelensis*, in the northern Gulf of California [30]. All individuals

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod*

*DOI: http://dx.doi.org/10.5772/intechopen.88956*

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod DOI: http://dx.doi.org/10.5772/intechopen.88956*

#### **Figure 1.**

*Crustacea*

strength [7–12].

strategies [9, 22, 23].

cally distinct.

genetic polymorphism [26].

sexual polymorphisms.

such as the ratio of sexually mature males to receptive females at any time (the Operational Sex Ratio, OSR [5]) or the ratio of maximum potential reproductive rates for each sex (PRR; [6]), but rather from actual estimates of selection's

ratio of the variance in fitness to its squared average. This parameter, when measured using the mean and variance in mate numbers for each sex and adjusted by the sex ratio, quantifies the sex difference in the opportunity for selection, that is, the opportunity for sexual selection (*IM*, [7, 8]; *Imates* [9]; *Is* [14]). Despite an early focus on mate numbers, the opportunity for sexual selection can be measured more precisely using the mean and variance in offspring numbers for each sex [9, 15, 16]. The Bateman gradient, *β*ss [14, 16–19] provides a more specific estimator of the effect of mating success on fitness, by quantifying the standardized covariance between mate number and offspring number. Jones' Index, *β*ss√*Is*, combines these parameters and appears to provide a useful correction when the opportunity for sexual selection is expressed in terms of mate numbers

The Bateman gradient is among the more precise methods for measuring sexual selection because it measures the slope, *β*ss, of the statistical relationship between mate numbers and offspring numbers for members of each sex [16]. Thus, it estimates the intensity of sexual selection on the trait or traits that influence the sex difference in the variance in offspring numbers, provided that such traits can be identified. Although now widely used to compare sex differences in selection intensity [16–19, 21], the Bateman gradient has not been used to examine the covariance between mate numbers and offspring numbers among polymorphic mating phenotypes, also known as alternative mating

Polymorphisms in mating phenotype are considered by many researchers to provide examples of *fitness satisficing*, a current explanation for why alternative adult morphs persist within populations despite their experience of average fitness that is less than the average fitness of the conventional adult morph. According to this hypothesis, alternative phenotypes appear to "make the best of a bad job" [22–24]. One mechanism by which alternative phenotypes could experience lessthan-average fitness is if Bateman gradients among the adult morphs are statisti-

The Gulf of California sphaeromatid isopod, *Paracerceis sculpta*, has three distinct male morphs and breeds within the spongocoels of the sponge, *Leucetta losangelensis*, (**Figure 1**). Alpha males are largest and possess enlarged uropods, used for defending breeding sites. Beta males are smaller than α-males and resemble females in behavior and body form. Gamma males are the smallest and use their small size and agility to "sneak" into spongocoels [25]. Previous results indicate that variance in fitness within each of the three male morphs is large, whereas fitness differences among morphs are minute, a necessary condition for the persistence of

While the possible causes of variance in mating success within α-males are relatively well understood [27–32], the causes of within-morph fitness variance for β- and γ-males are less clear. Here, we measured Bateman gradients for α-, β-, and γ-males, and females in *P. sculpta* to determine if there is a significant difference in the covariance between mate numbers and offspring numbers for the four adult phenotypes in this species. Our results reveal the precision of this approach for measuring the difference in sexual selection intensity and suggest an alternative method for investigating fitness differences among morphs in species with

= *I*; [13]), the

Such measures include the opportunity for selection (*VW/W*<sup>2</sup>

rather than in terms of offspring numbers [14, 20].

**66**

*The α-, β-, and γ-male and female morphs in Paracerceis sculpta (redrawn from Shuster [30]).*

#### **2. Materials and methods**

#### **2.1 Sexual receptivity, mating, and gestation in** *P. sculpta*

Females are attracted to breeding sites in sponges when their ovaries and brood pouches mature [29]. Sexual receptivity in these S1 females is initiated when they shed the posterior half of their cuticle and expose genital openings at the base of each fifth walking leg [27]. Females in S2 (half molted) condition remain receptive for 24 h before shedding their anterior cuticles, ovipositing into internal brood pouches and becoming non-receptive (S3). Females do not feed during gestation (S4–S7; [27]). Males complete a mating sequence with receptive females by inserting their appendix masculina and ejaculating into one, and then into the other of their mate's vaginas. Fertilization occurs and zygotes are brooded internally for 3 weeks before being released as fully formed juveniles (mancas; [27–29]).

#### **2.2 Field collections**

We collected several hundred isopods from the spongocoels of the intertidal sponge, *Leucetta losangelensis*, in the northern Gulf of California [30]. All individuals were sexed, scored by reproductive condition, measured to the nearest 0.125 mm, and identified by unique cuticular pigmentation patterns [27, 28]. We retained unmolted, sexually mature (S1) females (N = 92), as well as α-, β-, and γ-males (N = 41) from samples and placed these individuals into 225-ml plastic cups containing seawater. All other individuals were returned to collection sites within 24 h.

#### **2.3 Matings for males**

To examine the relationship between mate number and fertility for the three male morphs, and to compare the fertility of females mated to each of the three male morphs (see below), we allowed α-males (N = 14), β-males (N = 14), and γ-males (N = 13) to mate with 1–5 females in succession (Nfemales = 86). We allowed each male to remain with each female for the duration of her 24-h period of receptivity. We then separated individuals and placed them in separate 225-ml cups containing seawater. Males were then placed with another S2 female, allowed to mate for 24 h, and the sequence was continued until males either died or mated five times. All S3 females were maintained in containers until parturition when we counted all mancas and undeveloped zygotes, if present.

To determine whether the fertility of males differed or decreased with increasing mating frequency, as well as to determine whether the fertility of the females mated by α-, β-, and γ-males was statistically distinguishable, we first calculated the residuals for the regression of offspring number on female body size to account for the positive effect female body size has on fertility (F[1,85] = 98.14, P < 0.0001). Then, we analyzed these residuals using a two-way ANOVA to examine the influences of male morph (MORPH), the order of females in the mating queue (ORDER), and their interaction (MORPH\*ORDER) on the number of offspring produced by individual females mated by α-, β-, and γ-males. We performed a similar analysis on the number of undeveloped zygotes per female but did not calculate residuals for this analysis because there was no significant relationship between female body length and the number of undeveloped zygotes (F[1,68] = 0.67, P = 0.42).

#### **2.4 Matings for females**

To examine the relationship between mate number and fertility for females, we allowed S2 females to complete one mating sequence each with either 1 (N = 2), 3 (N = 1), or 5 (N = 3) α-males in succession. Pairs of isopods were given a maximum of 20 min to begin mating. To prevent re-mating, we removed males after mating, changed the water in the cup, and allowed each female to recover for 5 min before the next male was introduced. The entire mating sequence for each female never exceeded 2 h. S3 females were maintained in their containers until parturition, when all mancas were counted. Again, the numbers of undeveloped zygotes, if present, were also counted.

To investigate whether the fertility of females who mated 1–5 times over 2 h, was different from each other as well as from the fertility of the 86 females, we allowed unlimited matings with males over 24 h (see "Matings for males" section), we first calculated the residuals for the regression of offspring number on female body size to account for the positive relationship between female size and fertility (F[1,5] = 15.98, P = 0.02). Next, because of the small sample size of females mated within 2 h (N = 6), we compared the residuals of the fertility of females mated 1, 3 and 5 times using a Kruskal-Wallis test. Because this test was non-significant (*X*<sup>2</sup> [2,6] = 0.86, P = 0.65), we pooled these females for our analysis and compared their fertility as a group, with those of females who were allowed unlimited matings for 24 h. Note that these latter females (Nfemales = 86) were the same females whose fertility was compared when mated with α-, β-, and γ-males above.

**69**

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod*

Using two-way ANOVA, we then examined the influences of female body length (FBLENG), the time available for mating (DURATION; 1–5 matings in 2 h; unlimited matings in 24 h), and their interaction (FBLENG\*DURATION) on the number of offspring produced by females. We performed a similar analysis on the number of undeveloped zygotes per female. As in the previous analysis of undeveloped zygotes, we did not calculate residuals for this analysis because there was no significant relationship between female body length and the number of undeveloped

We used two-way ANOVA to examine the influences of adult phenotype (ADULTP), mate number (NMATES), and their interaction (ADULTP\*NMATES) on the number of offspring produced by α-, β-, and γ-males, and females. We then subdivided our data by sex and used two-way ANOVA to examine the influence of male morph (MORPH), mate number (NMATES), and their interaction (MORPH\*NMATES) on the number of offspring produced by α-, β-, and γ-males. Because males were analyzed separately from females, we used a Bonferroni correction to reduce our criterion for significance, α = 0.05/2 = 0.025. Lastly, we pooled the data for all males and used two-way ANOVA to examine the influences of sex (SEX), mate numbers (NMATES), and their interaction (SEX\*NMATES) on the number of offspring produced by all males and all females. For individual Bateman gradients, we calculated the least squares regression of offspring numbers on mate

Our two-way ANOVA of the residuals for offspring number on female body length, to determine whether the fertility of the three male morphs differed or decreased with increasing mating frequency, was non-significant overall (F[5,85] = 0.25, P = 0.94) with non-significant effects of male morph (F[MORPH] = 0.42, P = 0.66) and mate order (F[ORDER] = 2.21, P = 0.64) and a nonsignificant interaction between these factors (F[MORPH\*ORDER] = 0.15, P = 0.86). This result indicated that the three male morphs did not differ in their sexual competency with multiple matings. This result also confirmed that there were no significant differences in the fertility of females mated with α-, β-, and γ-males, and confirmed that there were no significant differences in the numbers of undeveloped zygotes among females mated by α-, β-, and γ-males (F[5,67] = 0.18, P = 0.97; F[MORPH] = 0.31, P = 0.73; F[ORDER] = 0.01, P = 0.95; F[MORPH\*ORDER] = 0.18, P = 0.83). Our two-way ANOVA to compare the fertility of females who mated 1–5 times over 2 h vs. the fertility of females allowed unlimited matings over 24 h was significant overall (F[3,81] = 34.56, P < 0.0001) with a significant effect of body length (F[FBLENG] = 7.34, P = 0.008), but no significant effect of the time available for mating (F[DURATION] = 1.03, P = 0.31) and no significant interaction between female body length and the time available for mating (F[FBLENG\*DURATION] = 0.35, P = 0.55). This result indicated that the size-adjusted fertility of females allowed to mate 1–5 times was no different from those of females allowed unlimited access to matings over 24 h. This result was corroborated by our finding that there were no significant differences in the numbers of undeveloped zygotes among females mated 1–5 times compared with females allowed unlimited matings over 24 h. (F[3,73] = 0.63, P = 0.60; F[FLENG] = 1.07, P = 0.30; F[DURATION] = 0.04, P = 0.84;

*DOI: http://dx.doi.org/10.5772/intechopen.88956*

zygotes (F[1,73] = 1.27, P = 0.26).

numbers for each adult morph [16].

F[FBLENG\*DURATION] = 0.33, P = 0.57).

**3. Results**

**2.5 Bateman gradients**

Using two-way ANOVA, we then examined the influences of female body length (FBLENG), the time available for mating (DURATION; 1–5 matings in 2 h; unlimited matings in 24 h), and their interaction (FBLENG\*DURATION) on the number of offspring produced by females. We performed a similar analysis on the number of undeveloped zygotes per female. As in the previous analysis of undeveloped zygotes, we did not calculate residuals for this analysis because there was no significant relationship between female body length and the number of undeveloped zygotes (F[1,73] = 1.27, P = 0.26).

#### **2.5 Bateman gradients**

*Crustacea*

**2.3 Matings for males**

**2.4 Matings for females**

were sexed, scored by reproductive condition, measured to the nearest 0.125 mm, and identified by unique cuticular pigmentation patterns [27, 28]. We retained unmolted, sexually mature (S1) females (N = 92), as well as α-, β-, and γ-males (N = 41) from samples and placed these individuals into 225-ml plastic cups containing seawater. All other individuals were returned to collection sites within 24 h.

To examine the relationship between mate number and fertility for the three male morphs, and to compare the fertility of females mated to each of the three male morphs (see below), we allowed α-males (N = 14), β-males (N = 14), and γ-males (N = 13) to mate with 1–5 females in succession (Nfemales = 86). We allowed each male to remain with each female for the duration of her 24-h period of receptivity. We then separated individuals and placed them in separate 225-ml cups containing seawater. Males were then placed with another S2 female, allowed to mate for 24 h, and the sequence was continued until males either died or mated five times. All S3 females were maintained in containers until parturition when we

To determine whether the fertility of males differed or decreased with increasing mating frequency, as well as to determine whether the fertility of the females mated by α-, β-, and γ-males was statistically distinguishable, we first calculated the residuals for the regression of offspring number on female body size to account for the positive effect female body size has on fertility (F[1,85] = 98.14, P < 0.0001). Then, we analyzed these residuals using a two-way ANOVA to examine the influences of male morph (MORPH), the order of females in the mating queue (ORDER), and their interaction (MORPH\*ORDER) on the number of offspring produced by individual females mated by α-, β-, and γ-males. We performed a similar analysis on the number of undeveloped zygotes per female but did not calculate residuals for this analysis because there was no significant relationship between female body

counted all mancas and undeveloped zygotes, if present.

length and the number of undeveloped zygotes (F[1,68] = 0.67, P = 0.42).

To examine the relationship between mate number and fertility for females, we allowed S2 females to complete one mating sequence each with either 1 (N = 2), 3 (N = 1), or 5 (N = 3) α-males in succession. Pairs of isopods were given a maximum of 20 min to begin mating. To prevent re-mating, we removed males after mating, changed the water in the cup, and allowed each female to recover for 5 min before the next male was introduced. The entire mating sequence for each female never exceeded 2 h. S3 females were maintained in their containers until parturition, when all mancas were counted. Again, the numbers of undeveloped zygotes, if present, were also counted. To investigate whether the fertility of females who mated 1–5 times over 2 h, was different from each other as well as from the fertility of the 86 females, we allowed unlimited matings with males over 24 h (see "Matings for males" section), we first calculated the residuals for the regression of offspring number on female body size to account for the positive relationship between female size and fertility (F[1,5] = 15.98, P = 0.02). Next, because of the small sample size of females mated within 2 h (N = 6), we compared the residuals of the fertility of females mated 1, 3 and 5 times using a Kruskal-Wallis test. Because this test was non-significant

[2,6] = 0.86, P = 0.65), we pooled these females for our analysis and compared their fertility as a group, with those of females who were allowed unlimited matings for 24 h. Note that these latter females (Nfemales = 86) were the same females whose

fertility was compared when mated with α-, β-, and γ-males above.

**68**

(*X*<sup>2</sup>

We used two-way ANOVA to examine the influences of adult phenotype (ADULTP), mate number (NMATES), and their interaction (ADULTP\*NMATES) on the number of offspring produced by α-, β-, and γ-males, and females. We then subdivided our data by sex and used two-way ANOVA to examine the influence of male morph (MORPH), mate number (NMATES), and their interaction (MORPH\*NMATES) on the number of offspring produced by α-, β-, and γ-males. Because males were analyzed separately from females, we used a Bonferroni correction to reduce our criterion for significance, α = 0.05/2 = 0.025. Lastly, we pooled the data for all males and used two-way ANOVA to examine the influences of sex (SEX), mate numbers (NMATES), and their interaction (SEX\*NMATES) on the number of offspring produced by all males and all females. For individual Bateman gradients, we calculated the least squares regression of offspring numbers on mate numbers for each adult morph [16].

#### **3. Results**

Our two-way ANOVA of the residuals for offspring number on female body length, to determine whether the fertility of the three male morphs differed or decreased with increasing mating frequency, was non-significant overall (F[5,85] = 0.25, P = 0.94) with non-significant effects of male morph (F[MORPH] = 0.42, P = 0.66) and mate order (F[ORDER] = 2.21, P = 0.64) and a nonsignificant interaction between these factors (F[MORPH\*ORDER] = 0.15, P = 0.86). This result indicated that the three male morphs did not differ in their sexual competency with multiple matings. This result also confirmed that there were no significant differences in the fertility of females mated with α-, β-, and γ-males, and confirmed that there were no significant differences in the numbers of undeveloped zygotes among females mated by α-, β-, and γ-males (F[5,67] = 0.18, P = 0.97; F[MORPH] = 0.31, P = 0.73; F[ORDER] = 0.01, P = 0.95; F[MORPH\*ORDER] = 0.18, P = 0.83).

Our two-way ANOVA to compare the fertility of females who mated 1–5 times over 2 h vs. the fertility of females allowed unlimited matings over 24 h was significant overall (F[3,81] = 34.56, P < 0.0001) with a significant effect of body length (F[FBLENG] = 7.34, P = 0.008), but no significant effect of the time available for mating (F[DURATION] = 1.03, P = 0.31) and no significant interaction between female body length and the time available for mating (F[FBLENG\*DURATION] = 0.35, P = 0.55). This result indicated that the size-adjusted fertility of females allowed to mate 1–5 times was no different from those of females allowed unlimited access to matings over 24 h. This result was corroborated by our finding that there were no significant differences in the numbers of undeveloped zygotes among females mated 1–5 times compared with females allowed unlimited matings over 24 h. (F[3,73] = 0.63, P = 0.60; F[FLENG] = 1.07, P = 0.30; F[DURATION] = 0.04, P = 0.84; F[FBLENG\*DURATION] = 0.33, P = 0.57).

#### **Figure 2.**

*Bateman gradients estimated for each adult phenotype in P. sculpta: α-males (βss ± SE = 87.60 ± 25.33, N = 14; P = 0.005; black diamonds, dashed line); β-males (βss ± SE = 80.46 ± 11.96, N = 14, P < 0.0001; dark gray triangles, dashed and dotted line); γ-males (βss ± SE = 69.48 ± 26.16, N = 13, P = 0.022; light gray squares, dotted line); females (βss ± SE = 1.78 ± 4.48, N = 6, P = 0.64; open circles, solid line); and pooled males (βss ± SE = 78.92 ± 12.23, N = 41, P < 0.0001; open circles); details of this analysis are described in the text.*

Our two-way ANOVA comparing the relationship between mate numbers and offspring numbers for each of the three male morphs and females (**Figure 2**) was significant (F[7, 39] = 8.71, P < 0.001), with a significant effect of adult phenotype (F[ADULTP] = 5.13, P = 0.004), a significant effect of mate numbers (F[NMATES] = 32.60, P < 0.0001), and with a significant interaction between adult phenotype and mate numbers (F[ADULTP\*NMATES] = 3.25, P = 0.032). This result indicated that a phenotype difference in Bateman gradients does exist for *P. sculpta*, but it did not reveal the source of the difference.

That source was revealed by two successive tests. Our two-way ANOVA of males alone, to identify the source of the difference in Bateman gradients among the adult phenotypes, was significant overall (F[5, 35] = 8.91, P < 0.0001), with a significant effect of mate numbers (F[NMATES] = 40.66, P < 0.0001). However, we found no significant effect of male morph (F[MORPH] = 1.59, P = 0.22) and no significant interaction between male morph and mate numbers (F[MORPH\*NMATES] = 0.17, P = 0.85), indicating that Bateman gradients for the three male morphs were indistinguishable. This result justified pooling all males for re-analysis of the relationship between mate numbers and offspring numbers for males and females.

This pooled-male analysis was significant overall (F[3,38] = 19.09, P < 0.001) with a significant effect of sex (F[SEX] = 11.81, P = 0.001), a significant effect of mate numbers (F[NMATES] = 10.14, P = 0.003), and a significant interaction between sex and mate numbers (F[SEX\*NMATES] = 9.26, P = 0.004), a result confirming that a sex difference in Bateman gradients exists for *P. sculpta* (**Figure 2**). In this analysis, the sex difference in the covariance between mate numbers and offspring numbers was over 40-fold larger for males than for females (**Figure 2**).

#### **4. Discussion**

Our results showed that although they appear to invest different amounts of energy toward somatic and gametic functions [27, 28], the three male morphs in *P. sculpta* do not differ in their sexual competencies with multiple matings. This result also demonstrated that individual females mated with α-, β-, or γ-males do

**71**

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod*

not differ in their fertility when allowed to mate with these males *a bene placito* over a 24-h period. Here, we confirmed this finding using the number of live young produced, *as well as* the number of undeveloped zygotes remaining within female brood pouches, thus considering the possibility of the positive, as well as the negative influences that multiple mating may have on female fertility. We also showed that the size-adjusted fertility of females allowed to mate 1–5 times was no different from those of females allowed unlimited access to matings over 24 h. This result justified our comparison of multiple matings by females with multiple matings by males of each of the three male phenotypes in our analysis of Bateman gradients. Our results further showed that while the three male morphs do not exhibit distinct Bateman gradients, a sex difference in Bateman gradients does exist for *P. sculpta* when adult male and female phenotypes are compared. α-, β-, and γ-males coexist at different population frequencies in nature (α: 0.81; β: 0.15; γ: 0.04; N = 555; [26]) and appear to differ in their mating success in different social circumstances [28, 29]. However, the fact that their Bateman gradients are statistically indistinguishable indicates that under our experimental conditions the fitnesses of the three male morphs were equal. Although the sample size for the females was small relative to females who mated once, as many as five matings had no effect on the number of offspring females in our study produced. Moreover, the fertility of these females, with variable numbers of matings, was no different from the fertility

of a larger sample of females (N = 86) with unlimited numbers of matings.

no evidence of that females were negatively affected by multiple matings.

cess, such as mate guarding or repeated inseminations, than α-males [26].

If this is indeed the case, then as is widely acknowledged, the number of matings individual males acquire need not translate linearly toward that male's overall fitness. More specifically, in nature, multiple Bateman gradients among male morphs may exist that each depend on the number of available mates *as well as* the number of different mating males representing each morph that are present within breeding sites at any given time. Such variation is likely to be widespread among species exhibiting reproductive polymorphisms (reviews in [17, 22, 33–40]). Under

The significant sex difference in Bateman gradients for *P. sculpta* suggests that sexual selection acts much more intensely on males than it does on females in this species. However, this result also indicates that sexual selection does not act differentially among the three male morphs through differences in mate number alone. This result corroborates other results [9, 26] indicating that fitness satisficing does not occur among the male morphs in *P. sculpta* in this context, and that differences in mate availability, not differences in sexual competency, are responsible for observed variance in fitness within, and for the equality of fitnesses among the three male morphs in this species. When β- and γ-males are present with α-males in the spongocoels in which these isopods breed, they tend to be more successful than α-males, particularly when harem sizes are large [9, 26, 28]. These results suggest that β- and γ-males may be more effective in tactics that enhance fertilization suc-

In contrast, within each of the three morphs, male fitness increased linearly with increasing numbers of matings (**Figure 2**). The large difference between the sexes in the number of offspring produced with increased numbers of mates suggests that intersexual conflict (c.f., [1–4, 12]) *could* exist within this species. Indeed in this study, the sex difference in the intensity of selection was over 40 times greater in males than in females (see also [10]). However, the magnitude of this difference also suggests that while intersexual conflict could exist, natural selection on females is considerably weaker than sexual selection on males. An evolutionary response by females to possible sexual exploitation by males, that is, an intersexual arms race of the sort envisioned in intersexual conflict scenarios [1–4, 12], might therefore be undetectable [9]. Despite the possibility of sexual exploitation by males, we found

*DOI: http://dx.doi.org/10.5772/intechopen.88956*

#### *Bateman Gradients and Alternative Mating Strategies in a Marine Isopod DOI: http://dx.doi.org/10.5772/intechopen.88956*

*Crustacea*

**Figure 2.**

Our two-way ANOVA comparing the relationship between mate numbers and offspring numbers for each of the three male morphs and females (**Figure 2**)

*Bateman gradients estimated for each adult phenotype in P. sculpta: α-males (βss ± SE = 87.60 ± 25.33, N = 14; P = 0.005; black diamonds, dashed line); β-males (βss ± SE = 80.46 ± 11.96, N = 14, P < 0.0001; dark gray triangles, dashed and dotted line); γ-males (βss ± SE = 69.48 ± 26.16, N = 13, P = 0.022; light gray squares, dotted line); females (βss ± SE = 1.78 ± 4.48, N = 6, P = 0.64; open circles, solid line); and pooled males (βss ± SE = 78.92 ± 12.23, N = 41, P < 0.0001; open circles); details of this analysis are described in the text.*

That source was revealed by two successive tests. Our two-way ANOVA of males alone, to identify the source of the difference in Bateman gradients among the adult phenotypes, was significant overall (F[5, 35] = 8.91, P < 0.0001), with a significant effect of mate numbers (F[NMATES] = 40.66, P < 0.0001). However, we found no significant effect of male morph (F[MORPH] = 1.59, P = 0.22) and no significant interaction between male morph and mate numbers (F[MORPH\*NMATES] = 0.17, P = 0.85), indicating that Bateman gradients for the three male morphs were indistinguishable. This result justified pooling all males for re-analysis of the relationship between mate numbers and offspring numbers for males and females.

This pooled-male analysis was significant overall (F[3,38] = 19.09, P < 0.001) with

a significant effect of sex (F[SEX] = 11.81, P = 0.001), a significant effect of mate numbers (F[NMATES] = 10.14, P = 0.003), and a significant interaction between sex and mate numbers (F[SEX\*NMATES] = 9.26, P = 0.004), a result confirming that a sex difference in Bateman gradients exists for *P. sculpta* (**Figure 2**). In this analysis, the sex difference in the covariance between mate numbers and offspring numbers was

Our results showed that although they appear to invest different amounts of energy toward somatic and gametic functions [27, 28], the three male morphs in *P. sculpta* do not differ in their sexual competencies with multiple matings. This result also demonstrated that individual females mated with α-, β-, or γ-males do

was significant (F[7, 39] = 8.71, P < 0.001), with a significant effect of adult phenotype (F[ADULTP] = 5.13, P = 0.004), a significant effect of mate numbers (F[NMATES] = 32.60, P < 0.0001), and with a significant interaction between adult phenotype and mate numbers (F[ADULTP\*NMATES] = 3.25, P = 0.032). This result indicated that a phenotype difference in Bateman gradients does exist for *P. sculpta*,

but it did not reveal the source of the difference.

over 40-fold larger for males than for females (**Figure 2**).

**70**

**4. Discussion**

not differ in their fertility when allowed to mate with these males *a bene placito* over a 24-h period. Here, we confirmed this finding using the number of live young produced, *as well as* the number of undeveloped zygotes remaining within female brood pouches, thus considering the possibility of the positive, as well as the negative influences that multiple mating may have on female fertility. We also showed that the size-adjusted fertility of females allowed to mate 1–5 times was no different from those of females allowed unlimited access to matings over 24 h. This result justified our comparison of multiple matings by females with multiple matings by males of each of the three male phenotypes in our analysis of Bateman gradients.

Our results further showed that while the three male morphs do not exhibit distinct Bateman gradients, a sex difference in Bateman gradients does exist for *P. sculpta* when adult male and female phenotypes are compared. α-, β-, and γ-males coexist at different population frequencies in nature (α: 0.81; β: 0.15; γ: 0.04; N = 555; [26]) and appear to differ in their mating success in different social circumstances [28, 29]. However, the fact that their Bateman gradients are statistically indistinguishable indicates that under our experimental conditions the fitnesses of the three male morphs were equal. Although the sample size for the females was small relative to females who mated once, as many as five matings had no effect on the number of offspring females in our study produced. Moreover, the fertility of these females, with variable numbers of matings, was no different from the fertility of a larger sample of females (N = 86) with unlimited numbers of matings.

In contrast, within each of the three morphs, male fitness increased linearly with increasing numbers of matings (**Figure 2**). The large difference between the sexes in the number of offspring produced with increased numbers of mates suggests that intersexual conflict (c.f., [1–4, 12]) *could* exist within this species. Indeed in this study, the sex difference in the intensity of selection was over 40 times greater in males than in females (see also [10]). However, the magnitude of this difference also suggests that while intersexual conflict could exist, natural selection on females is considerably weaker than sexual selection on males. An evolutionary response by females to possible sexual exploitation by males, that is, an intersexual arms race of the sort envisioned in intersexual conflict scenarios [1–4, 12], might therefore be undetectable [9]. Despite the possibility of sexual exploitation by males, we found no evidence of that females were negatively affected by multiple matings.

The significant sex difference in Bateman gradients for *P. sculpta* suggests that sexual selection acts much more intensely on males than it does on females in this species. However, this result also indicates that sexual selection does not act differentially among the three male morphs through differences in mate number alone. This result corroborates other results [9, 26] indicating that fitness satisficing does not occur among the male morphs in *P. sculpta* in this context, and that differences in mate availability, not differences in sexual competency, are responsible for observed variance in fitness within, and for the equality of fitnesses among the three male morphs in this species. When β- and γ-males are present with α-males in the spongocoels in which these isopods breed, they tend to be more successful than α-males, particularly when harem sizes are large [9, 26, 28]. These results suggest that β- and γ-males may be more effective in tactics that enhance fertilization success, such as mate guarding or repeated inseminations, than α-males [26].

If this is indeed the case, then as is widely acknowledged, the number of matings individual males acquire need not translate linearly toward that male's overall fitness. More specifically, in nature, multiple Bateman gradients among male morphs may exist that each depend on the number of available mates *as well as* the number of different mating males representing each morph that are present within breeding sites at any given time. Such variation is likely to be widespread among species exhibiting reproductive polymorphisms (reviews in [17, 22, 33–40]). Under

#### *Crustacea*

such circumstances, it is unlikely that any given subset of fitness gradients among morphs accurately represents the entire population, particularly if that subset focuses on males who are successful at mating and tends to ignore males who are unsuccessful. Field samples that disproportionately focus on successfully mating males tend to overestimate the fitness of males in the mating class, making it easier to conclude that males expressing alternative mating phenotypes are "making the best of a bad job [9, 40]."

For this reason, we recommend, when male polymorphisms exist, that the fitness for a large number of males of each morph be measured, and their relative fitness outcomes be considered in proportion to the average fitness that all males in the population achieve. This approach is consistent with studies of this and other species [26, 40], in which equal average fitnesses exist among male morphs over multiple generations.

#### **Acknowledgements**

This research was supported by NSF REU Site grant DBI-0552644, Research Experience for Undergraduates in Behavioral and Conservation Sciences at Northern Arizona University, and by NSF grants DEB-9726504 and OCE 84-01067 to SMS. We are grateful to D. S. Smith, R. Beresic-Perrins, and J. C. Boothroyd for their comments on earlier drafts of this manuscript. We also thank the summer 2007 REU students and G.P. Shuster for help in collecting *Paracerceis sculpta*. Permission to study *P. sculpta* populations in the Gulf of California was granted by Mexican Government, permits 412.2.1.3.0.2315, A00-702-06296, and DAN 02384.

#### **Author details**

Katharine M. Saunders1 and Stephen M. Shuster2 \*

1 School of Biological Sciences, University of Texas, Austin, TX, United States

2 Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, United States

\*Address all correspondence to: stephen.shuster@nau.edu

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

**73**

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod*

Journal of Evolutionary Biology.

[12] Kokko H, Klug H, Jennions MD. Unifying cornerstones of sexual selection: Operational sex ratio, Bateman gradient and the scope for competitive investment. Ecology Letters. 2012;**15**:1340-1351

[13] Crow JF. Some possibilities for measuring selection intensities in man.

[14] Jones AG. On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution. 2009;**63**:1673-1684

[15] Moorad JA, Wade MJ. Selection gradients, the opportunity for selection and the coefficient of determination.

[16] Arnold SJ, Duvall D. Animal mating systems: A synthesis based on selection theory. American Naturalist.

[17] Jones AG, Rosenqvist G, Anders B, Arnold SJ, Avise JC. The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proceedings of the Royal Society of London B. 2000;**267**:677-680

[18] Jones AG, Arguello JR, Arnold SJ. Molecular parentage analysis in experimental newt populations: The response of mating system measures to variation in the operational sex ratio. American Naturalist. 2004;**164**:444-456

[19] Jones AG, Rosenqvist G, Berglund A, Avise JC. The measurement of sexual selection using Bateman's Principles: An experimental test in the sex-role reversed pipefish *Syngnathus typhle*. Integrative and Comparative Biology.

The American Naturalist.

2013;**181**:291-300

1994;**143**:317-348

2005;**45**:874-884

Human Biology. 1958;**30**:1-13

2011;**24**:2064-2071

*DOI: http://dx.doi.org/10.5772/intechopen.88956*

[1] Bateman AJ. Intra-sexual selection in *Drosophila*. Heredity. 1948;**2**:349-368

[3] Trivers RL. Parental investment and sexual selection. In: Campbell B, editor. Sexual Selection and the Descent of Man. Chicago, IL: Aldine Press; 1972.

[4] Rubenstein DR, Alcock J. Animal Behavior. 11th ed. New York, Oxford: Sinauer Associates, Oxford University

[5] Emlen ST, Oring LW. Ecology, sexual selection, and the evolution of mating systems. Science. 1977;**197**:215-223

[6] Clutton-Brock TH, Vincent ACJ. Sexual selection and the potential reproductive rates of males and females.

[7] Wade MJ. Sexual selection and variance in reproductive success. American Naturalist. 1979;**114**:742-764

[8] Wade MJ, Arnold SJ. The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence. Animal Behaviour.

[9] Shuster SM, Wade MJ. Mating Systems and Strategies. Princeton, NJ: Princeton University Press; 2003

[11] Krakauer AH, Webster MS, DuVal EH, Jones AG, Shuster SM. The opportunity for sexual selection: Not mismeasured, just misunderstood.

[10] Wade MJ, Shuster SM. Don't throw Bateman out with the bathwater! Integrative and Comparative Biology.

Nature. 1991;**351**:58-60.7

1980;**28**:446-461

2005;**45**:261-268

[2] Williams GC. Adaptation and Natural Selection. Princeton, NJ: Princeton University Press; 1966

**References**

pp. 136-179

Press; 2019. 548pp

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod DOI: http://dx.doi.org/10.5772/intechopen.88956*

#### **References**

*Crustacea*

best of a bad job [9, 40]."

multiple generations.

**Acknowledgements**

**Author details**

United States

Katharine M. Saunders1

such circumstances, it is unlikely that any given subset of fitness gradients among morphs accurately represents the entire population, particularly if that subset focuses on males who are successful at mating and tends to ignore males who are unsuccessful. Field samples that disproportionately focus on successfully mating males tend to overestimate the fitness of males in the mating class, making it easier to conclude that males expressing alternative mating phenotypes are "making the

For this reason, we recommend, when male polymorphisms exist, that the fitness for a large number of males of each morph be measured, and their relative fitness outcomes be considered in proportion to the average fitness that all males in the population achieve. This approach is consistent with studies of this and other species [26, 40], in which equal average fitnesses exist among male morphs over

This research was supported by NSF REU Site grant DBI-0552644, Research

Northern Arizona University, and by NSF grants DEB-9726504 and OCE 84-01067 to SMS. We are grateful to D. S. Smith, R. Beresic-Perrins, and J. C. Boothroyd for their comments on earlier drafts of this manuscript. We also thank the summer 2007 REU students and G.P. Shuster for help in collecting *Paracerceis sculpta*. Permission to study *P. sculpta* populations in the Gulf of California was granted by Mexican Government, permits 412.2.1.3.0.2315, A00-702-06296, and DAN 02384.

Experience for Undergraduates in Behavioral and Conservation Sciences at

and Stephen M. Shuster2

\*Address all correspondence to: stephen.shuster@nau.edu

provided the original work is properly cited.

1 School of Biological Sciences, University of Texas, Austin, TX, United States

2 Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ,

© 2019 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

\*

**72**

[1] Bateman AJ. Intra-sexual selection in *Drosophila*. Heredity. 1948;**2**:349-368

[2] Williams GC. Adaptation and Natural Selection. Princeton, NJ: Princeton University Press; 1966

[3] Trivers RL. Parental investment and sexual selection. In: Campbell B, editor. Sexual Selection and the Descent of Man. Chicago, IL: Aldine Press; 1972. pp. 136-179

[4] Rubenstein DR, Alcock J. Animal Behavior. 11th ed. New York, Oxford: Sinauer Associates, Oxford University Press; 2019. 548pp

[5] Emlen ST, Oring LW. Ecology, sexual selection, and the evolution of mating systems. Science. 1977;**197**:215-223

[6] Clutton-Brock TH, Vincent ACJ. Sexual selection and the potential reproductive rates of males and females. Nature. 1991;**351**:58-60.7

[7] Wade MJ. Sexual selection and variance in reproductive success. American Naturalist. 1979;**114**:742-764

[8] Wade MJ, Arnold SJ. The intensity of sexual selection in relation to male sexual behaviour, female choice, and sperm precedence. Animal Behaviour. 1980;**28**:446-461

[9] Shuster SM, Wade MJ. Mating Systems and Strategies. Princeton, NJ: Princeton University Press; 2003

[10] Wade MJ, Shuster SM. Don't throw Bateman out with the bathwater! Integrative and Comparative Biology. 2005;**45**:261-268

[11] Krakauer AH, Webster MS, DuVal EH, Jones AG, Shuster SM. The opportunity for sexual selection: Not mismeasured, just misunderstood.

Journal of Evolutionary Biology. 2011;**24**:2064-2071

[12] Kokko H, Klug H, Jennions MD. Unifying cornerstones of sexual selection: Operational sex ratio, Bateman gradient and the scope for competitive investment. Ecology Letters. 2012;**15**:1340-1351

[13] Crow JF. Some possibilities for measuring selection intensities in man. Human Biology. 1958;**30**:1-13

[14] Jones AG. On the opportunity for sexual selection, the Bateman gradient and the maximum intensity of sexual selection. Evolution. 2009;**63**:1673-1684

[15] Moorad JA, Wade MJ. Selection gradients, the opportunity for selection and the coefficient of determination. The American Naturalist. 2013;**181**:291-300

[16] Arnold SJ, Duvall D. Animal mating systems: A synthesis based on selection theory. American Naturalist. 1994;**143**:317-348

[17] Jones AG, Rosenqvist G, Anders B, Arnold SJ, Avise JC. The Bateman gradient and the cause of sexual selection in a sex-role-reversed pipefish. Proceedings of the Royal Society of London B. 2000;**267**:677-680

[18] Jones AG, Arguello JR, Arnold SJ. Molecular parentage analysis in experimental newt populations: The response of mating system measures to variation in the operational sex ratio. American Naturalist. 2004;**164**:444-456

[19] Jones AG, Rosenqvist G, Berglund A, Avise JC. The measurement of sexual selection using Bateman's Principles: An experimental test in the sex-role reversed pipefish *Syngnathus typhle*. Integrative and Comparative Biology. 2005;**45**:874-884

[20] Henshaw JM, Kahn AT, Fritzche K. A rigorous comparison of sexual selection indexes via simulations of diverse mating systems. Proceedings of the National Academy of Sciences. 2016;**113**:E300-E308

[21] Bjork A, Pitnick S. Intensity of sexual selection along the anisogamyisogamy continuum. Nature. 2006;**441**:742-748

[22] Gross MR. Alternative reproductive strategies and tactics: Diversity within sexes. Trends in Ecology & Evolution. 1996;**11**:92-97

[23] Tomkins JL, Hazel W. The status of the conditional evolutionary stable strategy. Trends in Ecology & Evolution. 2007;**22**:522-528

[24] Dawkins R. Good strategy or evolutionary stable strategy? In: Barlow GW, Silverberg J, editors. Sociobiology: Beyond Nature/ Nurture? Boulder, CO: Westview; 1980. pp. 331-367

[25] Shuster SM. Alternative reproductive behaviors: three discrete male morphs in *Paracerceis sculpta*, an intertidal isopod from the northern Gulf of California. Journal of Crustacean Biology. 1987;**7**(2):318-327

[26] Shuster SM, Wade MJ. Equal mating success among male reproductive strategies in a marine isopod. Nature. 1991;**350**:608-610

[27] Shuster SM. Female sexual receptivity associated with molting and differences in copulatory behavior among the three male morphs in *Paracerceis sculpta* (Crustacea: Isopoda). Biological Bulletin. 1989;**177**:331-337

[28] Shuster SM. Male alternative reproductive behaviors in a marine isopod crustacean (*Paracerceis sculpta*): The use of genetic markers to measure

differences in fertilization success among α-, β- and γ-males. Evolution. 1989;**34**:168-169

[29] Shuster SM. Courtship and female mate selection in a semelparous isopod crustacean (*Paracerceis sculpta*). Animal Behaviour. 1990;**40**:390-399

[30] Shuster SM. The reproductive behaviour of α-, β- and γ-males in *Paracerceis sculpta*, a marine isopod crustacean. Animal Behaviour. 1992;**121**:231-258

[31] Shuster SM, Arnold EM. The effect of females on male-male competition in atypical breeding habitats in the marine isopod, *Paracerceis sculpta*: A reaction norm approach to behavioral plasticity. Journal of Crustacean Biology. 2007;**27**(3):417-424

[32] Shuster SM. The expression of crustacean mating strategies. In: Brockmann HJ, Olivieri R, Taborsky M, editors. Alternative Mating Tactics. Cambridge, UK: Cambridge University Press; 2008

[33] Gross MR, Charnov EL. Alternative male life histories in bluegill sunfish. Proceedings of the National Academy of Science, USA. 1980;**77**:6937-6948

[34] Thornhill R. Panorpa (Mecoptera: Panorpidae) scorpionflies: Systems for understanding resourcedefense polygyny and alternative male reproductive efforts. Annual Review of Ecology and Systematics. 1981;**12**:355-386

[35] Lank DB, Smith CM, Hanotte O, Burke T, Cooke F. Genetic polymorphism for alternative mating behaviour in lekking male ruff. Nature. 1995;**378**:59-62

[36] Sinervo B. Selection in local neighborhoods, graininess of social environments, and the ecology of

**75**

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod*

*DOI: http://dx.doi.org/10.5772/intechopen.88956*

alternative strategies. In: Dugatkin LA, editor. Model Systems in Behavioral Ecology. Princeton, NJ: Princeton University Press; 2001. pp. 191-226

[37] Tomkins JL, Brown GS. Population density drives the local evolution of a threshold dimorphism. Nature.

[38] Isvaran K. Variation in male mating behaviour within ungulate populations: Patterns and processes. Current Science.

[39] Beveridge M, Simmons LW, Alcock J. Genetic breeding system and investment patterns within the nests of Dawson's burrowing bee (*Amegilla dawsoni*) (Hymenoptera: Anthophorini). Molecular Ecology.

[40] Shuster SM, Willen RM, Keane B, Solomon NG. Alternative mating tactics in socially monogamous prairie voles (*Microtus ochrogaster*). Frontiers in Ecology and Evolution. 2019;**7**(7):1-19

2004;**431**:1099-1103

2005;**89**:1192-1199

2006;**15**:3459-3467

*Bateman Gradients and Alternative Mating Strategies in a Marine Isopod DOI: http://dx.doi.org/10.5772/intechopen.88956*

alternative strategies. In: Dugatkin LA, editor. Model Systems in Behavioral Ecology. Princeton, NJ: Princeton University Press; 2001. pp. 191-226

*Crustacea*

2016;**113**:E300-E308

2006;**441**:742-748

1996;**11**:92-97

2007;**22**:522-528

pp. 331-367

[20] Henshaw JM, Kahn AT, Fritzche K. A rigorous comparison of sexual selection indexes via simulations of diverse mating systems. Proceedings of the National Academy of Sciences.

differences in fertilization success among α-, β- and γ-males. Evolution.

[29] Shuster SM. Courtship and female mate selection in a semelparous isopod crustacean (*Paracerceis sculpta*). Animal

Behaviour. 1990;**40**:390-399

[30] Shuster SM. The reproductive behaviour of α-, β- and γ-males in *Paracerceis sculpta*, a marine isopod crustacean. Animal Behaviour.

[31] Shuster SM, Arnold EM. The effect of females on male-male competition in atypical breeding habitats in the marine isopod, *Paracerceis sculpta*: A reaction norm approach to behavioral plasticity. Journal of Crustacean Biology.

[32] Shuster SM. The expression of crustacean mating strategies. In: Brockmann HJ, Olivieri R, Taborsky M, editors. Alternative Mating Tactics. Cambridge, UK: Cambridge University

[33] Gross MR, Charnov EL. Alternative male life histories in bluegill sunfish. Proceedings of the National Academy of Science, USA. 1980;**77**:6937-6948

[34] Thornhill R. Panorpa (Mecoptera: Panorpidae) scorpionflies: Systems

Hanotte O, Burke T, Cooke F. Genetic polymorphism for alternative mating behaviour in lekking male ruff. Nature.

[36] Sinervo B. Selection in local neighborhoods, graininess of social environments, and the ecology of

for understanding resourcedefense polygyny and alternative male reproductive efforts. Annual Review of Ecology and Systematics.

[35] Lank DB, Smith CM,

1981;**12**:355-386

1995;**378**:59-62

1989;**34**:168-169

1992;**121**:231-258

2007;**27**(3):417-424

Press; 2008

[21] Bjork A, Pitnick S. Intensity of sexual selection along the anisogamy-

[22] Gross MR. Alternative reproductive strategies and tactics: Diversity within sexes. Trends in Ecology & Evolution.

[23] Tomkins JL, Hazel W. The status of the conditional evolutionary stable strategy. Trends in Ecology & Evolution.

[24] Dawkins R. Good strategy or evolutionary stable strategy? In: Barlow GW, Silverberg J, editors. Sociobiology: Beyond Nature/

[25] Shuster SM. Alternative

Biology. 1987;**7**(2):318-327

[27] Shuster SM. Female sexual receptivity associated with molting and differences in copulatory behavior among the three male morphs in *Paracerceis sculpta* (Crustacea: Isopoda). Biological Bulletin. 1989;**177**:331-337

[28] Shuster SM. Male alternative reproductive behaviors in a marine isopod crustacean (*Paracerceis sculpta*): The use of genetic markers to measure

1991;**350**:608-610

Nurture? Boulder, CO: Westview; 1980.

reproductive behaviors: three discrete male morphs in *Paracerceis sculpta*, an intertidal isopod from the northern Gulf of California. Journal of Crustacean

[26] Shuster SM, Wade MJ. Equal mating success among male reproductive strategies in a marine isopod. Nature.

isogamy continuum. Nature.

**74**

[37] Tomkins JL, Brown GS. Population density drives the local evolution of a threshold dimorphism. Nature. 2004;**431**:1099-1103

[38] Isvaran K. Variation in male mating behaviour within ungulate populations: Patterns and processes. Current Science. 2005;**89**:1192-1199

[39] Beveridge M, Simmons LW, Alcock J. Genetic breeding system and investment patterns within the nests of Dawson's burrowing bee (*Amegilla dawsoni*) (Hymenoptera: Anthophorini). Molecular Ecology. 2006;**15**:3459-3467

[40] Shuster SM, Willen RM, Keane B, Solomon NG. Alternative mating tactics in socially monogamous prairie voles (*Microtus ochrogaster*). Frontiers in Ecology and Evolution. 2019;**7**(7):1-19

**77**

**Chapter 6**

**Abstract**

and Belize)

*and Oscar Frausto-Martínez*

The Habitat Types of Freshwater

*Macrobrachium*) with Abbreviated

Mesoamerica (Mexico, Guatemala

*Luis M. Mejía-Ortíz, Jesús E. Cupul-Pool, Marilú López-Mejía,* 

*Jair G. Valladarez, Keith A. Crandall, Marcos Pérez-Losada* 

The freshwater prawns of genus *Macrobrachium* with abbreviated larval development have been reported from a diversity of freshwater habitats (caves, springs and primary streams from so-long basins). Here we analysed 360 sites around the Mesoamerican region (Mexico, Guatemala and Belize). At each site, we measured temperature, salinity oxygen dissolved, pH, altitude and water flow velocity values. We documented the riparian vegetation and occurrence and abundance of *Macrobrachium* populations. All these values were analysed by multi-dimensional scaling and principal components analysis in order to identify key features of the environmental data that determine the habitat types and habitat diversity. The results show that there are *Macrobrachium* populations in 70 sites inhabiting two main habitats: Lotic and Lentic; and each one have fours subhabitat types. All are defined by altitude range and water velocity that involve the temperature and oxygen variables. In some specific areas, the karstic values on salinity and pH defined some groups. Within the lentic habitats, we identified the following subhabitats: (1) temperate streams, (2) neutral streams, (3) high dissolved oxygen, (4) multifactorial; and for lotic habitats, we identified: (5) water high carbonate, (6) moderate dissolved oxygen, (7) low dissolved oxygen, and (8) high altitude streams. All these subhabitats are located on the drainage basin to the Atlantic Sea, including places from 50 to 850 meters above sea levels and have specifically ranges from temperature, water velocity, pH and salinity for some cases. Also, the geological analysis from the basins where the *Macrobrachium* inhabit is located showed that the geological faults align with these habitat subdivisions. In this chapter, we discuss the environmental heterogeneity, morphological plasticity and their relationship to physiographic regions across the species ranges.

**Keywords:** *Macrobrachium*, abbreviated larval development, Mesoamerica, habitat

*Alfredo G. Baez-Meléndres, Juan C. Tejeda Mazariegos,* 

Prawns (Palaemonidae:

Larval Development in

## **Chapter 6**
