**2. Biology and ecology of topshells**

#### **2.1. Anatomy**

**1. Introduction**

142 Biological Resources of Water

Tethyan Seaway.

tive measures of the ecosystem.

anthropogenic impact on this ecosystem [4, 5].

Topshells are marine gastropods that inhabit the rocky shores. These marine snails together with limpets and winkles are the most successful algal grazers present in the intertidal of the Northeastern Atlantic and Mediterranean Sea [1]. Topshells occupy the rocky sea shores from the supratidal to the subtidal, one of the most extreme, heterogeneous, and dynamic environments in nature that expose these organisms to different levels of thermal and hydric stresses [2, 3]. These unpredictable environmental conditions are therefore responsible for many of their peculiar morphological and biological characteristics that can be perceived as adaptations to the intertidal environment [4]. The marine snails of the genus *Phorcus* are ecologically important algae grazers that play a major role in regulating the ecological balance of their habitat and have often been used as biological indicators in evaluating the consequences of

The diversity and ecological importance of the genus *Phorcus* prompted intensive research over the past years. Recently, this genus was redefined by Donald et al. [5] to include species previously under the genus *Monodonta* Lamarck, 1799, or *Osilinus* Philippi, 1847, allowing to trace the biogeographic history of this genus' origin to 40–20 Ma, prior to the closure of the

Intertidal invertebrates' life history traits vary inter- and intraspecifically because of genetic differences and environmental effects. Growth, reproductive strategy, and mortality depend on a complex combination of selective forces and are fundamental to understand the distribution and abundance of these species along the intertidal [6, 7]. As such, knowledge of life history traits of *Phorcus* populations provides important information required to understand how these species adapt to an ever-changing environment, whether because of human activities, such as fisheries, habitat disturbance, pollution and climate change, or natural causes.

One of the main causes of disturbance in the intertidal ecosystem is the harvest of gastropods in the rocky shores, which has occurred since prehistorical times, resulting in shifts in abundance and/or size structure of these species. Another cause of disturbance is the contamination of coastal waters, by the presence of unnatural chemicals, as a result of industrial spillage and sewage discharges among others. Gastropod molluscs are frequently used as bioindicators to assess the health status of the coast and determine the effect of marine pollution [8]. Walsh et al. [9] recorded that these sentinel species have the potential to act as a useful biomonitoring system of pollutants in the marine environment. As such, they act as pollution indicators by tracing metals, providing information required for the establishment of protec-

*Phorcus* species are recognized as good bioindicators of water quality due to their reduced mobility, easy sampling, adequate size for tissue analysis, widespread distribution, abundance all year-round, and ability to accumulate high metal concentration in their shell and

Global climate change also causes disturbance in the intertidal ecosystem that results in changes in the geographical distribution of marine gastropods. Intertidal invertebrates are

tissues, reflecting heavy metal availability in coastal waters [10, 11].

Gastropods are comprised essentially of two main parts: the shell and the body. These asymmetrical molluscs have a twisted, spirally coiled shell around its body, which protects them from biotic and abiotic factors present in their environment, and a corneous or calcareous operculum, a flat plate that rests on the upper dorsal side of the foot that acts as a supporting pad for the shell. When the snail actively moves or blocks the aperture, the body withdraws, protecting the animal from predators and preventing water leakage in exposed rocky shores [12, 13].

In topshells, the shell is complete and usually pyramidal, moderately large, conical to globose in shape, with rounded to angular body whorls and often with a flattened base and an interior consisting of mother-of-pearl. This structure is formed in the embryonic stage, with the secretion of protein fibres from the outer skin of the visceral mass and from the mantle, while they are free-swimming larvae and they are followed by the secretion of calcium carbonate from the same cells. Posterior to the embryonic phase, the shell continues to grow through the addition of a protein mesh and calcium carbonate mostly on its margins but also on its interior. Shell growth is not continuous and it frequently leaves different growth lines since maturity and adverse environmental conditions may cease growth. The shell offers refuge both from predators and from desiccation being impervious to gasses and liquids and resistant to crushing [12–14]. Colour patterns of the shell are usually highly variable in topshells and are mostly related to diet rather than to genetic control (**Figure 1**) [12].

The soft body consists of two compartments connected by a waist and present a dark ash colour with a greenish tint [15]. The lower compartment encompasses the muscular foot and the head. The foot is used for locomotion over the substrate, swimming, jumping, and returning the animal to an upright position when overturned. Also, it helps to detect food. The upper compartment is used for respiration, digestion, excretion, gamete production, and shell secretion. The body of these organisms comprises a head with a short snout, a pair of conical

**Figure 1.** Shell phenotypic variability of *Phorcus sauciatus*. A – Portugal mainland, B – Madeira Island, C – Gran Canaria Island.

and papillate tentacles, cup-shaped open eyes on distinct stalks, a foot, a muscular ventral organ with a flattened base used for locomotion, and a visceral mass, which fills dorsally the spire of the shell and contains most organ systems and the mantle, a collar-like tegument, which lines and secretes the shell, and forms a mantle cavity normally provided with respiratory gills for breathing in water and a well-vascularised mantle cavity, which allows the animals to breathe in air [13, 14].

#### **2.2. Taxonomy and geographic distribution**

*Phorcus* Risso, 1826, are herbivorous marine snails (Gastropoda: Prosobranchia) belonging to the family Trochidae Rafinesque, 1815, that inhabit rocky shores from the Mediterranean Sea through the Northeastern Atlantic Ocean including the Macaronesian Archipelagos of Madeira, Canaries, Azores, and Cape Verde [14].

the Macaronesian archipelagos of Madeira, Canary, and Azores with its northern boundary in the Iberian Peninsula and its southern limit in the African mainland, with negligible genetic differentiation between them, suggesting either recent or continuing dispersal among these

**Figure 2.** Shells of the nine species of the genus *Phorcus*. A – *Phorcus sauciatus* from Madeira archipelago, B – *Phorcus lineatus* from mainland Portugal, C – *Phorcus atratus* from Selvagens Islands, D – *Phorcus mariae* from Cape Verde archipelago, E – *Phorcus punctulatus* from Senegal (NMR 36429) [17], F *– Phorcus articulatus* from Spain (NMR 36447) [17], G – *Phorcus mutabilis* from Greece (NMR 36658) [17], H – *Phorcus richardi* from Greece (NMR 36669) [17], I – *Phorcus turbinatus* from Greece (NMR 36606) [17]. Images E, F, G, H, and I by Joop Trausel and Frans Slieker and available online

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Concerning the geographic distribution of the genus *Phorcus* in the Mediterranean Sea, *P. turbinatus* occurs from Spain to Cyprus, *P. articulatus* from Spain to Tunisia, *P. richardi*

Topshells as limpets are subject to an array of environmental stresses due to their extended vertical distribution, which ranges from the upper to the lower shore levels. Thus, these organisms can exhibit varying degrees of structural adaptations since their position relative to the shore influences their exposure to desiccation, hydrodynamic action of the waves, temperature variation, and tidal width [20–23], resulting in a wide array of intraspecific pheno-

Marine snails of the genus *Phorcus* have a gill for water breathing and a well-vascularised mantle cavity, which allows the animal to breathe in the air [14]. The mantle cavity placed between the body and its overhanging mantle skirt is constituted by a single gill in the front part of the mantle cavity and thin-walled organs that absorb oxygen from the sea water [12]. The marine snails' blood, the haemolymph, contains haemocyanin, a copper-containing protein that can fix and transport two to three times more oxygen, from the gills to the heart, than organisms without this protein. The heart pulsations push the oxygen-rich blood over a closed system of arteries that lead the blood to a system of open arteries, without epithelial

from Spain to Croatia, and *P. mutabilis* from Italy to Turkey [5].

areas [5, 18, 19].

at NMR – Natural History Museum Rotterdam [17].

typic variability.

**2.3. Respiratory system**

This genus of gastropod grazers is currently represented by nine recognized living species [5, 6] and is comprised of *Phorcus articulatus* (Lamarck, 1822)*, Phorcus atratus* (Wood, 1828), *Phorcus lineatus* (da Costa, 1778), *Phorcus mariae* Templado & Rolán, 2012, *Phorcus mutabilis* (Philippi, 1851), *Phorcus punctulatus* (Lamarck, 1822), *Phorcus richardi* (Payraudeau, 1826), *Phorcus sauciatus* (Koch, 1845), and *Phorcus turbinatus* (Born, 1778) [1, 5].

There is a clear separation between the species of *Phorcus* that occur in the Atlantic and the Mediterranean. This split distribution is thought to result from the barrier imposed by the Strait of Gibraltar, since there is no species overlap in the adjacent area, and the nearby Alboran front that act as biogeographic breaks for animals with short larval stages, such as *P. lineatus*, whose lecithotrophic veliger larvae remain in the water column for, at the most, 6–7 days [5, 14, 16]. As such, four species of this genus are restricted to the Mediterranean Sea, specifically *P. turbinatus*, *P. mutabilis*, *P. articulatus* and *P. richardi* and the remaining five species occur in the Northeastern Atlantic Ocean, namely *P. lineatus*, *P. sauciatus*, *P. atratus*, *P. punctulatus*, and *P. mariae* (**Figure 2**) [5].

In the North Atlantic Ocean, *P. lineatus* is the species that reaches the northernmost geographic limits of the genus *Phorcus* in North Wales and Ireland and *P. punctulatus* the southernmost limits in Senegal. *P. mariae* is restricted to Cape Verde archipelago, *P. atratus* to the Canaries archipelago and Selvagens Islands, and *P. punctulatus* to Senegal [1, 5, 14]. *P. lineatus* has a wide distribution ranging from North Wales and Ireland to Morocco and *P. sauciatus* includes Marine Snails of the Genus *Phorcus*: Biology and Ecology of Sentinel Species for Human Impacts… http://dx.doi.org/10.5772/intechopen.71614 145

**Figure 2.** Shells of the nine species of the genus *Phorcus*. A – *Phorcus sauciatus* from Madeira archipelago, B – *Phorcus lineatus* from mainland Portugal, C – *Phorcus atratus* from Selvagens Islands, D – *Phorcus mariae* from Cape Verde archipelago, E – *Phorcus punctulatus* from Senegal (NMR 36429) [17], F *– Phorcus articulatus* from Spain (NMR 36447) [17], G – *Phorcus mutabilis* from Greece (NMR 36658) [17], H – *Phorcus richardi* from Greece (NMR 36669) [17], I – *Phorcus turbinatus* from Greece (NMR 36606) [17]. Images E, F, G, H, and I by Joop Trausel and Frans Slieker and available online at NMR – Natural History Museum Rotterdam [17].

the Macaronesian archipelagos of Madeira, Canary, and Azores with its northern boundary in the Iberian Peninsula and its southern limit in the African mainland, with negligible genetic differentiation between them, suggesting either recent or continuing dispersal among these areas [5, 18, 19].

Concerning the geographic distribution of the genus *Phorcus* in the Mediterranean Sea, *P. turbinatus* occurs from Spain to Cyprus, *P. articulatus* from Spain to Tunisia, *P. richardi* from Spain to Croatia, and *P. mutabilis* from Italy to Turkey [5].

Topshells as limpets are subject to an array of environmental stresses due to their extended vertical distribution, which ranges from the upper to the lower shore levels. Thus, these organisms can exhibit varying degrees of structural adaptations since their position relative to the shore influences their exposure to desiccation, hydrodynamic action of the waves, temperature variation, and tidal width [20–23], resulting in a wide array of intraspecific phenotypic variability.

#### **2.3. Respiratory system**

and papillate tentacles, cup-shaped open eyes on distinct stalks, a foot, a muscular ventral organ with a flattened base used for locomotion, and a visceral mass, which fills dorsally the spire of the shell and contains most organ systems and the mantle, a collar-like tegument, which lines and secretes the shell, and forms a mantle cavity normally provided with respiratory gills for breathing in water and a well-vascularised mantle cavity, which allows the

**Figure 1.** Shell phenotypic variability of *Phorcus sauciatus*. A – Portugal mainland, B – Madeira Island, C – Gran Canaria

*Phorcus* Risso, 1826, are herbivorous marine snails (Gastropoda: Prosobranchia) belonging to the family Trochidae Rafinesque, 1815, that inhabit rocky shores from the Mediterranean Sea through the Northeastern Atlantic Ocean including the Macaronesian Archipelagos of

This genus of gastropod grazers is currently represented by nine recognized living species [5, 6] and is comprised of *Phorcus articulatus* (Lamarck, 1822)*, Phorcus atratus* (Wood, 1828), *Phorcus lineatus* (da Costa, 1778), *Phorcus mariae* Templado & Rolán, 2012, *Phorcus mutabilis* (Philippi, 1851), *Phorcus punctulatus* (Lamarck, 1822), *Phorcus richardi* (Payraudeau, 1826),

There is a clear separation between the species of *Phorcus* that occur in the Atlantic and the Mediterranean. This split distribution is thought to result from the barrier imposed by the Strait of Gibraltar, since there is no species overlap in the adjacent area, and the nearby Alboran front that act as biogeographic breaks for animals with short larval stages, such as *P. lineatus*, whose lecithotrophic veliger larvae remain in the water column for, at the most, 6–7 days [5, 14, 16]. As such, four species of this genus are restricted to the Mediterranean Sea, specifically *P. turbinatus*, *P. mutabilis*, *P. articulatus* and *P. richardi* and the remaining five species occur in the Northeastern Atlantic Ocean, namely *P. lineatus*, *P. sauciatus*, *P. atratus*,

In the North Atlantic Ocean, *P. lineatus* is the species that reaches the northernmost geographic limits of the genus *Phorcus* in North Wales and Ireland and *P. punctulatus* the southernmost limits in Senegal. *P. mariae* is restricted to Cape Verde archipelago, *P. atratus* to the Canaries archipelago and Selvagens Islands, and *P. punctulatus* to Senegal [1, 5, 14]. *P. lineatus* has a wide distribution ranging from North Wales and Ireland to Morocco and *P. sauciatus* includes

*Phorcus sauciatus* (Koch, 1845), and *Phorcus turbinatus* (Born, 1778) [1, 5].

animals to breathe in air [13, 14].

Island.

144 Biological Resources of Water

**2.2. Taxonomy and geographic distribution**

Madeira, Canaries, Azores, and Cape Verde [14].

*P. punctulatus*, and *P. mariae* (**Figure 2**) [5].

Marine snails of the genus *Phorcus* have a gill for water breathing and a well-vascularised mantle cavity, which allows the animal to breathe in the air [14]. The mantle cavity placed between the body and its overhanging mantle skirt is constituted by a single gill in the front part of the mantle cavity and thin-walled organs that absorb oxygen from the sea water [12].

The marine snails' blood, the haemolymph, contains haemocyanin, a copper-containing protein that can fix and transport two to three times more oxygen, from the gills to the heart, than organisms without this protein. The heart pulsations push the oxygen-rich blood over a closed system of arteries that lead the blood to a system of open arteries, without epithelial walls, that surround the viscera and the muscles covering all organs with oxygen-rich blood. The body organs receive the oxygen from the haemolymph and release carbon dioxide into it, which then returns to the gills, via a system of veins, where it releases the carbon dioxide and again receives oxygen [12].

Contrary to limpets, topshells are active at low tide and respond very rapidly to changes in weather conditions, moving out into the open when the sun shines and hiding from rain or cold winds in crevices or under boulders [26]. These species are limited in their vertical zonation by their tolerance to temperature variation; as such, they undertake vertical migrations

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Wave action also acts as a limiting factor on suspension feeders and on semisessile and sessile organisms that are favoured on exposed conditions, since the water movement allows the flow of food, propagules, nutrients, and preys to these organisms. However, in these habitats, the increase of exposure to wave action involves an increase on the risk of dislodgement and physical damage, limiting the range of susceptible and physically fragile species [2]. In order to overcome the adverse conditions of the exposed areas, intertidal gastropods inhabiting these areas have a thin and smooth shell with large aperture due to the large foot required to cope with the higher risk of wave displacement and to be able to maintain a firm hold on rocky surfaces [28, 29]. In dangerous circumstances, a snail withdraws into its shell and adheres firmly to the substrate, so as to not be detached by waves or predators [12]. In the Northeastern Atlantic, *P. lineatus* is usually used as an indicator of sheltered rocky shores [30] contrary to *P. sauciatus* that seems to be more tolerant to wave action being found lower on the shore but also able to establish on sheltered zones [18]. The anatomic features of these two species corroborate this hypothesis since *P. sauciatus'* thinner shell, larger foot, and consequently large aperture imply that this species is more tolerant to wave action than *P. lineatus* with thicker shell and smaller aperture. On the other hand, these anatomic differences result

Growth is a key variable in determining the survivability of any given animal, and it is important to understand the factors that drive it [31]. Biological parameters such as growth rate, asymptotic length, longevity, and age structure reflect the overall state of health of a population and are commonly used as stock assessment tools of exploited marine organisms [4]. In gastropods, growth rates have been determined through several features such as growth lines and rings in shells [32, 33], opercula [34], and statoliths [35]. Size and age of topshells are

Size and growth rates in the species of the genus *Phorcus* are influenced by fluctuations in food supply [26, 37], competition [38], and wave action [39], while population density is mainly controlled by the successful settlement of larvae and predation [26, 38]. The oceanographic current systems are known to be largely responsible for the water temperature and nutrients of the coastal ecosystems, which mark the distribution and behaviour of organisms throughout the coastlines [2]. As such, temperature also influences growth in the species of the genus *Phorcus*. For instance, Crothers [14] and Mannino et al. [40] observed that a decrease in water temperature promotes a metabolic deceleration, resulting in the interruption of growth during the winter in *P. lineatus*. However, after this season, growth continues rapidly through the year, slowing only in the next winter. In general, in the first year, the growth rate of this species is high and decreases thereafter [14] as a possible result of achieving sexual maturity.

up and down the shore over the seasons [27].

in *P. sauciatus* being less tolerant to desiccation than *P. lineatus*.

positively related, thus allowing to investigate population structure [36].

**2.5. Growth**

#### **2.4. Feeding habits, behaviour, and ecological importance**

Molluscan grazers are known to have an important influence on the overall structure of benthic marine communities, because of the influence and control they exert on algae [24, 25]. Removal of grazers often leads to an imbalance on the population dynamics of the species involved on the rocky shores ecosystem, due to a dramatic development of seaweed beds [25].

Topshells, winkles, and limpets form a guild of microphagous herbivores that feed on microbial biofilms, by grazing the rocky substrate with the radula, a specialized rasping organ unique to molluscs, on which successive rows upon rows of backwards-pointing teeth are placed. The teeth crack, break, and wear away during use, by the food or the hard substrate from which the sea snail scrapes [12]. Marine snails can all be found together, grazing on the open shore, and it is probable that these various snail species do not feed in exactly the same place, at the same time, in the same manner, or on exactly the same food [14] in order to avoid interspecific competition. The feeding adaptations between these species can be behavioural through spatial differentiation or anatomical through adaptations in the radula. Among these species, radulae show different hardness and patterns, being multi–fine-toothed rhipidoglossan in topshells, less complex taenioglossan in winkles, and simple docoglossan in pattelid limpets; therefore, it is easy to conclude they feed in different ways [14].

In several species of sea snails, the digestive fluids contain the cellulase enzyme that breaks down cellulose. This is one of the very few cases throughout the animal kingdom of an animal producing an enzyme capable of breaking down cellulose [12]. Feeding behaviour in topshells is assumed to occur at night or during high tide as stated by Crothers [14] for *P. lineatus*. Food particles are gathered by the radula, squashed by the jaws, and then transported inward into the mouth where the digestive track begins, in the front of the body, and then transported back along the body through the oesophagus to the stomach where most of digestion occurs, and finally, digested food loops and descends forwards to the intestine where faeces are formed and expelled by the anus, which drains into the mantle cavity, at the front of the body [12].

Common topshells and edible winkles swing their head from side to side while crawling and may leave grazing tracks on the rock surface and visible slime trails. Usually, the more active species secrete a thicker layer on which to crawl and this may show up as a pale band over the rock surface. Trail-following, namely the crawling over existing mucus trails, will reduce the expense of producing a mucus trail. These trails might also be used to locomote back home, to find mates, and to assist in feeding, by trapping food particles from the water column [12]. Marine snails crawl by squeezing the front end of the foot against the substrate and by means of a ripple of muscle contraction, pass that point of contact forcing the mass of the snail forwards. In topshells, the two halves of the foot work independently of each other, out of phase, producing a characteristic slime trail [26].

Contrary to limpets, topshells are active at low tide and respond very rapidly to changes in weather conditions, moving out into the open when the sun shines and hiding from rain or cold winds in crevices or under boulders [26]. These species are limited in their vertical zonation by their tolerance to temperature variation; as such, they undertake vertical migrations up and down the shore over the seasons [27].

Wave action also acts as a limiting factor on suspension feeders and on semisessile and sessile organisms that are favoured on exposed conditions, since the water movement allows the flow of food, propagules, nutrients, and preys to these organisms. However, in these habitats, the increase of exposure to wave action involves an increase on the risk of dislodgement and physical damage, limiting the range of susceptible and physically fragile species [2]. In order to overcome the adverse conditions of the exposed areas, intertidal gastropods inhabiting these areas have a thin and smooth shell with large aperture due to the large foot required to cope with the higher risk of wave displacement and to be able to maintain a firm hold on rocky surfaces [28, 29]. In dangerous circumstances, a snail withdraws into its shell and adheres firmly to the substrate, so as to not be detached by waves or predators [12]. In the Northeastern Atlantic, *P. lineatus* is usually used as an indicator of sheltered rocky shores [30] contrary to *P. sauciatus* that seems to be more tolerant to wave action being found lower on the shore but also able to establish on sheltered zones [18]. The anatomic features of these two species corroborate this hypothesis since *P. sauciatus'* thinner shell, larger foot, and consequently large aperture imply that this species is more tolerant to wave action than *P. lineatus* with thicker shell and smaller aperture. On the other hand, these anatomic differences result in *P. sauciatus* being less tolerant to desiccation than *P. lineatus*.

#### **2.5. Growth**

walls, that surround the viscera and the muscles covering all organs with oxygen-rich blood. The body organs receive the oxygen from the haemolymph and release carbon dioxide into it, which then returns to the gills, via a system of veins, where it releases the carbon dioxide and

Molluscan grazers are known to have an important influence on the overall structure of benthic marine communities, because of the influence and control they exert on algae [24, 25]. Removal of grazers often leads to an imbalance on the population dynamics of the species involved on the rocky shores ecosystem, due to a dramatic development of seaweed beds [25]. Topshells, winkles, and limpets form a guild of microphagous herbivores that feed on microbial biofilms, by grazing the rocky substrate with the radula, a specialized rasping organ unique to molluscs, on which successive rows upon rows of backwards-pointing teeth are placed. The teeth crack, break, and wear away during use, by the food or the hard substrate from which the sea snail scrapes [12]. Marine snails can all be found together, grazing on the open shore, and it is probable that these various snail species do not feed in exactly the same place, at the same time, in the same manner, or on exactly the same food [14] in order to avoid interspecific competition. The feeding adaptations between these species can be behavioural through spatial differentiation or anatomical through adaptations in the radula. Among these species, radulae show different hardness and patterns, being multi–fine-toothed rhipidoglossan in topshells, less complex taenioglossan in winkles, and simple docoglossan in pattelid

In several species of sea snails, the digestive fluids contain the cellulase enzyme that breaks down cellulose. This is one of the very few cases throughout the animal kingdom of an animal producing an enzyme capable of breaking down cellulose [12]. Feeding behaviour in topshells is assumed to occur at night or during high tide as stated by Crothers [14] for *P. lineatus*. Food particles are gathered by the radula, squashed by the jaws, and then transported inward into the mouth where the digestive track begins, in the front of the body, and then transported back along the body through the oesophagus to the stomach where most of digestion occurs, and finally, digested food loops and descends forwards to the intestine where faeces are formed and expelled by the anus, which drains into the mantle cavity, at

Common topshells and edible winkles swing their head from side to side while crawling and may leave grazing tracks on the rock surface and visible slime trails. Usually, the more active species secrete a thicker layer on which to crawl and this may show up as a pale band over the rock surface. Trail-following, namely the crawling over existing mucus trails, will reduce the expense of producing a mucus trail. These trails might also be used to locomote back home, to find mates, and to assist in feeding, by trapping food particles from the water column [12]. Marine snails crawl by squeezing the front end of the foot against the substrate and by means of a ripple of muscle contraction, pass that point of contact forcing the mass of the snail forwards. In topshells, the two halves of the foot work independently of each other, out of phase,

again receives oxygen [12].

146 Biological Resources of Water

the front of the body [12].

producing a characteristic slime trail [26].

**2.4. Feeding habits, behaviour, and ecological importance**

limpets; therefore, it is easy to conclude they feed in different ways [14].

Growth is a key variable in determining the survivability of any given animal, and it is important to understand the factors that drive it [31]. Biological parameters such as growth rate, asymptotic length, longevity, and age structure reflect the overall state of health of a population and are commonly used as stock assessment tools of exploited marine organisms [4]. In gastropods, growth rates have been determined through several features such as growth lines and rings in shells [32, 33], opercula [34], and statoliths [35]. Size and age of topshells are positively related, thus allowing to investigate population structure [36].

Size and growth rates in the species of the genus *Phorcus* are influenced by fluctuations in food supply [26, 37], competition [38], and wave action [39], while population density is mainly controlled by the successful settlement of larvae and predation [26, 38]. The oceanographic current systems are known to be largely responsible for the water temperature and nutrients of the coastal ecosystems, which mark the distribution and behaviour of organisms throughout the coastlines [2]. As such, temperature also influences growth in the species of the genus *Phorcus*. For instance, Crothers [14] and Mannino et al. [40] observed that a decrease in water temperature promotes a metabolic deceleration, resulting in the interruption of growth during the winter in *P. lineatus*. However, after this season, growth continues rapidly through the year, slowing only in the next winter. In general, in the first year, the growth rate of this species is high and decreases thereafter [14] as a possible result of achieving sexual maturity. In the first six months postsettlement, specimens can grow up to 8 mm diameter, reaching 11–15 mm by the end of the year [41]. Although the growth rates slow down dramatically after the achievement of sexual maturity, since energy is mostly directed towards reproduction, growth continues throughout the life cycle of this species. In habitats with low abundance, *P. lineatus* grows rapidly to a large size and reaches maturity early but has lower longevity. While individuals that live in habitats where they are more abundant grow slowly, they do not achieve great size and may live to an older age. These differences in growth are likely related to different levels of food availability depending on population density, which in turn is related to settlement success and predation evasion [26]. The specimens of this species have been known to reach a size of 34 mm in shell height and a longevity of 15 years of age in southern Britain [36]. *P. sauciatus* have approximately the same size range of *P. lineatus.* For instance, in the Madeira archipelago, *P. sauciatus* size ranges from 2 to 28 mm (pers. obs.); in the Canary Islands, this species size ranges from 5 to 26 mm [42]; and in the Portuguese mainland coast, its size ranges from 7 to 24 mm (pers. obs.). There is, however, a great gap in knowledge concerning life history parameters of *Phorcus* species. Most studies focused on *P. lineatus* due to their wide geographical distribution spanning from Morocco to North Wales/ Ireland. Life history parameters such as growth rates, asymptotical length, size at first maturity, recruitment patterns, and mortality of *Phorcus* species are likely to differ inter- and intraspecifically as a result of different biotic and abiotic factors. Further studies on the biology and population dynamics of *Phorcus* are therefore required in order to guarantee the implementation of successful conservation strategies and a sustainable exploitation based on effective management measures.

the northernmost range limit, breeding seasons are shorter with a single spawning period, while in southern regions, the breeding season is longer with multiple spawning events [46, 47]. For instance, in *P. lineatus* from Austurias, Spain, the gonadal development occurs from November to June and the breeding stages from June to September and may last until November in some specimens [46]. Spawning occurs between May and August [48]. Further north in Wales, the same species is reported to have a shorter spawning season, lasting from July to August [14]. On the other hand, *P. turbinatus* that occurs in the Mediterranean Sea appears to have a longer

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Fertilisation is external, with both sexes releasing their gametes into the sea and the whole process occurs directly in the water. During the reproductive season, males and females approach each other and then females send out chemical signals, leading to sperm being discharged in the water by males, which in turn stimulates females to release the oocytes [12]. According to Desai [44], males discharge clouds of spermatozoa that become very active 2 or 3 minutes after being released, and females liberate oocytes separately, a few at each spasm. This process of external fertilisation, regarded as a primitive trait in snails, becomes a high-risk strategy and improbable to succeed unless the species is locally common [14]. The fertilised egg develops within approximately a day and becomes trochophore larvae, which are capable of independent locomotion. The veliger larvae enclosed in a tiny shell develop in one or two days. At metamorphosis, the veliger turns upside down with the foot becoming ventral and the shell dorsal. Posterior to the snail's development, the back dorsal rotates in 180° anticlockwise in relation to the head and foot. Veliger larvae remain in the water column for at most 6–7 days [5, 14, 16], and at settlement, the shell measures a little over 1 mm across [14]. According to Heller [12], the trochophores of the genus *Phorcus* hatch down shore, within approximately one day and the veliger settles 4–5 days with about 1 mm. For *P. lineatus* in the United Kingdom, the recruits achieve 5–6 mm shell length by the first autumn and are detected on the bare rock between September and November and recognized, with 6–14 mm,

The gap in size at settlement and size at first capture reported for topshells may be understood as a potential argument for the existence of nursery areas, underneath boulders or fissures, in which small juveniles are much commoner, but there appears to be no uniform pattern [14]. For instance, in Madeira archipelago, the juveniles of *P. sauciatus* are commonly found under boulders, with the smallest individuals having 2 mm in diameter (pers. obs.). These boulders may function as a nursery for topshell juveniles as they provide protection against abiotic factors, such as wave action and desiccation, and biotic factors, such as predation and substrate competition.

Intertidal and shallow-water grazers are extremely vulnerable organisms because of their limited habitat and their accessibility to human activity [50]. Hunter-gatherers have exploited intertidal grazers, since prehistoric times, and there are evidences that the densities and the

**3. Anthropogenic impacts on the genus** *Phorcus*

breeding period with two spawning events in spring and autumn [49].

through their first year [33].

**3.1. Harvesting**

#### **2.6. Reproduction**

Topshells' reproductive system is usually strikingly simple, with a genital duct opening into the mantle cavity through the right kidney. Sea snails commonly have separate sexes but these species are not externally sexually dimorphic and sex determination is only possible through macroscopic observation of the gonads. Internally, the most reliable character for sorting them is the appearance of the urogenital aperture. In males, the lips of this organ are unpigmented and smaller, while in females, the lips are yellow and swollen. Nevertheless, in the ripe state, males have cream testis and females greyish-green ovary covering the digestive gland and viscera [43, 44], being therefore easily differentiated in the breeding state. The lobes of the gonad, whether ovary or testis, lie near the apex of the visceral hump, among the lobes of the digestive tube, and they drain into the pericardium [12].

Prior to the breeding season, adults migrate up shore to the high eulittoral zone. It seems that this migration brings the animals into a region of higher temperature required for spawning. An increase in temperature may stimulate spawning as suggested by Desai [44] who observed that adults that have migrated furthest up shore were the first to spawn.

In fact, spawning in intertidal organisms seems to be promoted by environmental triggers such as temperature, high wind speed, and wave action. Biological factors as an increase in phytoplankton concentration may also stimulate spawning as occurs in limpets [38, 45]. As such, breeding stages of a given species may differ according to their geographical position. In fact, in the northernmost range limit, breeding seasons are shorter with a single spawning period, while in southern regions, the breeding season is longer with multiple spawning events [46, 47]. For instance, in *P. lineatus* from Austurias, Spain, the gonadal development occurs from November to June and the breeding stages from June to September and may last until November in some specimens [46]. Spawning occurs between May and August [48]. Further north in Wales, the same species is reported to have a shorter spawning season, lasting from July to August [14]. On the other hand, *P. turbinatus* that occurs in the Mediterranean Sea appears to have a longer breeding period with two spawning events in spring and autumn [49].

Fertilisation is external, with both sexes releasing their gametes into the sea and the whole process occurs directly in the water. During the reproductive season, males and females approach each other and then females send out chemical signals, leading to sperm being discharged in the water by males, which in turn stimulates females to release the oocytes [12]. According to Desai [44], males discharge clouds of spermatozoa that become very active 2 or 3 minutes after being released, and females liberate oocytes separately, a few at each spasm. This process of external fertilisation, regarded as a primitive trait in snails, becomes a high-risk strategy and improbable to succeed unless the species is locally common [14]. The fertilised egg develops within approximately a day and becomes trochophore larvae, which are capable of independent locomotion. The veliger larvae enclosed in a tiny shell develop in one or two days. At metamorphosis, the veliger turns upside down with the foot becoming ventral and the shell dorsal. Posterior to the snail's development, the back dorsal rotates in 180° anticlockwise in relation to the head and foot. Veliger larvae remain in the water column for at most 6–7 days [5, 14, 16], and at settlement, the shell measures a little over 1 mm across [14]. According to Heller [12], the trochophores of the genus *Phorcus* hatch down shore, within approximately one day and the veliger settles 4–5 days with about 1 mm. For *P. lineatus* in the United Kingdom, the recruits achieve 5–6 mm shell length by the first autumn and are detected on the bare rock between September and November and recognized, with 6–14 mm, through their first year [33].

The gap in size at settlement and size at first capture reported for topshells may be understood as a potential argument for the existence of nursery areas, underneath boulders or fissures, in which small juveniles are much commoner, but there appears to be no uniform pattern [14]. For instance, in Madeira archipelago, the juveniles of *P. sauciatus* are commonly found under boulders, with the smallest individuals having 2 mm in diameter (pers. obs.). These boulders may function as a nursery for topshell juveniles as they provide protection against abiotic factors, such as wave action and desiccation, and biotic factors, such as predation and substrate competition.
