**1. Introduction - Study species**

The Indian short-nosed fruit bat, *Cynopterus sphinx,* belongs to the Old-World fruit bats (Megachiroptera: Pteropodidae) (**Figure 1a**). It is a common plantvisiting bat that occurs throughout the Indo-Malayan region and roosts solitarily or in small groups in the foliage [1]. It weighs about 45–70 g and lives in small clusters of about 3–30 individuals [2–4]. Dog-shaped head, divergent nostril, large prominent eyes and short ears with white margin are the unique morphological characters by which one can easily identify this species. In males, the chin, anterior part of shoulders, sides of the chest, belly and thighs are characteristically orange tinted

#### **Figure 1.**

*The study species Indian short-nosed fruit bat (a) Cynopterus sphinx. A close view of (b) male and (c) female.*

(**Figure 1b**). In females, the collar is usually tawny brown, the rump is gray brown and the belly is paler gray with slightly lighter hair tips (**Figure 1c**).

These bats use several types of diurnal roosts and are known to alter different types of foliages (palm and mast trees) to construct tents and attract females (**Figure 2a** and **b**) [2, 4–6]. Although different types of altered plant structures are referred to as bat tents [7], the first account of tent making by a male bat came from observations on *C. sphinx* [2]. During the breeding season, most of these bats live in groups called "harems" (**Figure 2c** and **d**) consisting of a single male and more than one female [2–4, 6, 8]. Harem males defend such tents against other males and thereby enabling copulation with a large number of females which is the primary mating strategy adopted by *C. sphinx*. They follow polygynous mating system (prolonged association of one male with more than one female) based on resource, called resource defense polygyny. The recruited females are defended as harem by a single male [2, 6]. However, apart from such successful males, a number of adult males were also observed roosting solitarily [8–10].

*C. sphinx* is a polygynous-mating bat that has a polyestrous reproductive cycle with two well-defined and highly synchronous parturition periods per year [11, 12]. Typically, in India, parturition takes place during the month of March/April and July/ August. Females can reproduce a maximum of two pups in a year [11, 12]. Females endure a postpartum oestrus once the young ones are born during the month of

*Dispersal Patterns, Mating Strategy and Genetic Diversity in the Short Nosed Fruit Bat… DOI: http://dx.doi.org/10.5772/intechopen.100496*

#### **Figure 2.**

*The major roosting trees (a) Polyalthia longifolia (mast tree), (b) Borassus flabellifer (palm tree) commonly used by the Indian short-nosed fruit bat C. sphinx in South India. A closer view of group of C. sphinx roosting in tents of (c) mast and (d) palm tree. Arrows indicate the bat roosts.*

March/April [11, 13]. To wean the cohorts born during March/April, females lactate the young ones while they are pregnant. Females remain anoestrus until October after the birth of July/August cohort [14, 15]. Neonates weigh *ca.* 11 g at birth and begin to fly at approximately 40–50 days of age, although young may continue to suckle from their mothers for 10–15 days after they initiate flight [12, 16]. At weaning, young *C. sphinx* weight about 51% of adult body mass and achieve adult body dimensions at approximately two months of age [1]. In this chapter, we discuss dispersal patterns, mating strategy and genetic diversity in the short-nosed fruit bat *C. sphinx* (Chiroptera: Pteropodidae) in southern India.

## **2. Dispersal patterns**

#### **2.1 Introduction**

Displacement of a juvenile from its birth place to the first site of reproduction is termed as natal dispersal [17]. This natal dispersal is one of the factors contributing to the central evolutionary forces that affect the natural populations. Also, it is the key life history trait that is involved in both species persistence and evolution [18]. Understanding the patterns of dispersal is important in population ecology and conservation biology [17, 19]. Bats are known to exhibit varying degrees of dispersal and philopatry based on their social system [20, 21]. The short-nosed fruit bat *C. sphinx* is a group living, frugivorous, megachiropteran bat. In *C. sphinx*, the juveniles of both the sexes are believed to disperse completely from the natal harem [3]. However, their status after dispersion remained unanswered. Do they join established harems immediately or aggregate to form a new harem? Answering this question is the aim of this section.

#### **2.2 Materials and methods**

In order to understand the dispersal pattern in *C. sphinx*, the mark-recapture study was carried out in the day-roosting places in and around Palayamkottai, Tamil Nadu, South India (lat: 8° 44′ S; long: 77° 42′ E). We spotted day roosts by citing the accumulation of leaf pellets, rejected fruits, seeds, and leaves under trees especially *Borassus flabellifer, Polyalthia longifolia Washigtonia filifera, Caryota urens,* and *Vernonia scandens.* When any of these accumulations are seen, it is very likely that *C. sphinx* bats roost. Randomly 4–6 day roosts were censused every week. Bats were captured just before emergence with the help of a hoop net attached to an extendable aluminum pole. The entire tree was enveloped with a 6 m x 9 m nylon mist net (Avinet-Dryden, New York, USA) to prevent bats from escaping. The mouth of the hoop net was placed at the entrance of day roosts. A minor disturbance was caused to the trap the bats inside the tent. For each bat, sex, age, forearm length and body mass were recorded [16]. After processing, the bats were held in net cages and were released at their roosts on the evening of the same day they were captured. Only those colonies, which were captured completely, were included in the present study. The proportion of males and females in different age classes viz. pups, juveniles and subadults were estimated and their roosting patterns were recorded.

#### **2.3 Results and discussion**

Our results showed that female proportion in harem increases considerably from pups to subadults. Both the sexes are equal in number (1:1) in the pup stage, whereas the sex ratio was female biased in the juvenile (1:1.8) and subadult stage (1:4.2). In mammals, dispersal is usually male biased and this also holds true for most bat species studied to date [17, 22, 23]. However, several studies on tropical species indicate that there may be cases where females also disperse [24]. Our study suggests that the juveniles of both the sexes disperse from their natal group before entering the subadult stage. We mostly captured dispersed juveniles and harems in which post-lactating females were present without the young ones. In many of the day roosts, the number of juvenile bats were disproportionate to the number of post-lactating females, especially when the juvenile bats were predominant.

The capture rate of juvenile females outnumbered the juvenile males, which suggest that the males dispersed early from the natal roost. One could suggest that maternal neglect could be playing a strong role in the altered sex ratio in *C. sphinx*. If mortality is a factor at the pre-weaning stage, both the sexes are expected to suffer equally: whereas if adults eject the males by force, then there may not be any juvenile males in their parental roosts. Contrarily we observed some juvenile males roosting in the natal roost though the number was much less when compared to females. Similar studies in other bats show that young females of short-tailed fruit bat *Carollia perspiscillata* are more likely to disperse away from the natal roosts than the young males [25]. In *Nycticeius humeralis,* all juvenile male bats deserted the roost faster than females and they were neither seen again in the roost nor foraging nearby. Contrary to this, juvenile females remained in the foraging area with their mothers after recruitment. They evidently continued to nurse for about three weeks longer, since milk could be expressed from the mammary glands of captured adult females until mid-July [26]. In a Neotropical bat *Lophostoma silvicolum* both male and female offsprings disperse before maturity and the polygynous mating system may lead to all-offspring dispersal more often than previously assumed in mammals [27].

In accordance with the general mammalian pattern the females of most group-living bats, including some harem-forming species and all temperate zone *Dispersal Patterns, Mating Strategy and Genetic Diversity in the Short Nosed Fruit Bat… DOI: http://dx.doi.org/10.5772/intechopen.100496*

species, are strongly philopatric which includes evening bat *N. humeralis* [17, 26, 28], vampire bat *Desmodus rotundus* [29], the brown long-eared bat *Plecotus auritus* [30, 31], Bechstein's bat *Myotis bechsteinii* [32–34], greater horseshoe bat *Rhinolophus ferrumequinum* [35], mouse-eared bat *Myotis myotis* [22] and northern long-eared bat *Myotis septentrionalis* [36]. A typical female philopatry was not observed in the group living *C. sphinx*. In this study, juveniles of both the sexes were found to disperse completely from their natal harems. Several reasons for female dispersal have been postulated [37]. It is often assumed that dispersal costs are higher for females than for males, whereas the benefits are thought to be higher for males. Moreover, absence of female philopatry is not uncommon among harem forming Neotropical bats [25, 29].

In this study, the female proportion in harems increases considerably from pups to subadults. Compared to juveniles (1:1.8), sex ratio was highly skewed towards females in the subadult stage (1:4.2). From the total of 52 subadults, only 10 were males. Moreover, not a single subadult male bat was found to be roosting in a harem. This explains that the males disperse from the natal roost before subadult stage. From the 42 captured subadult females, it was observed that four subadult females were pregnant showing that the females matured earlier and were engaged in reproductive activities during the subadult stage itself. Lower rate of juvenile survivorship maybe one of the reasons for the low capture of adult males [12], which remains unclear. The probability of censusing these bats remain low because the male bats preferred to roost in dense, unmodified and previously unoccupied foliages. During the capture, the number of subadult females were larger as they joined established harems, formed a new harem of subadult females with an adult male or they remained alone in the roost.

However, we were not able to find out whether the dispersed juvenile bats return back to their natal harems. The probability of making local migrations even during the breeding season is rare in both *Rhinopoma hardwickei* and *P. auritus* and hence they show greater fidelity towards their roost sites when compared to other bat species [38, 39]. However, the degrees of roost fidelity differ according to the sex and age in different bat species. During the nursing season female *Miniopterus schreibersii* bats strongly exhibit philopatric behavior since they returned to their place of birth to produce young ones [40]. Also, it was observed that the males extended greater level of connection to their birth site and also the juvenile female bats showed higher fidelity to their natal roost than did males and bats of other ages [41]. Moreover a particular population of *C. sphinx* from Pune, there were no recruitment of females to natal harems and also these females did not join other harems in the same or neighboring colonies [3]. Young females joining harems have been documented in bats like *Artibeus jamaicensis* and *Phyllostomus hastatus.* Though, technically the mating system of both these species appears to be a form of polygyny similar to *C. sphinx,* all three species seem to differ in the way young females are recruited in to a harem. In *A. jamaicensis*, it was observed that harems contained females of all ages, which suggests that subadult females join established harems [21], whereas, harem of the greater spear-nosed bat *P. hastatus* forms a new generation of subadult females [20]. However, in *C. sphinx* the harems consist of all age groups of harem females as well as the harems with only subadult females were in common.

#### **2.4 Conclusion**

We identify that young female *C. sphinx* become member of a harem group much earlier than the male. The reason for nonharem young females staying near to the established harems is not known. But this roosting pattern may improve the chances of breeding attempts made by young females as they attain sexual maturity earlier (*ca.* 7 months) compared to males (*ca*. 18 months) [12, 42].

### **3. Mating strategy**

Factors responsible for the occurrence of nonharem males and mechanisms used to acquire harem male status.

### **3.1 Introduction**

Polygynous mating is one of the most salient features of mammalian social structure and has potentially far-reaching consequences for a diverse array of evolutionary processes [43]. Male reproductive success in polygynous mammals is largely attributed to the spatial and temporal patterns of female aggregation [43, 44]. Receptive females are reliant on variation in resource distribution, predation pressure, costs of social living and activities of males [43]. One of the major factors that affect the mating success of resource-based polygynous mating animals is the resource distribution. Females choose males indirectly by mating with males that defend the highest quality resource when the males control access to the resources that these females require for reproduction [44]. Males that can make the greatest genetic contribution to the fitness of their offspring are chosen by the females [45].

Bats exhibit various forms of mating behavior ranging from simple monogamy to resource and female defense polygyny, as well as leks [46, 47]. Among these, resource defense polygyny is the most commonly observed mating pattern [48]. Bats establish a harem by defending critical resources such as food, shelter or mates [46]. Males potentially gaining favored access to several females is considered as one of the main benefits in resource defense polygyny and a healthy male inseminates the females [43, 46]. It is observed that several Neotropical fruit bats such as *Uroderma bilobatum* [49, 50], *Vampyressa nymphaea* [51], *Ectophylla alba* [52], *A. jamaicensis* [53–55] and *C. sphinx* [2] follow this type of mating strategy. Most of the bat species often spend the day and a large portion of the night in the roost which shows their attachment to their roosts [7]. However, it was observed that out of 1,300 bat species, only about 20 species are known to make their own roosts [56]. A striking feature of some polygynous bat species is that they often alter different types of foliage to create tents [2, 3, 57].

*C. sphinx* is known to exhibit polygynous mating system (i.e. prolonged association of one male with more than one female) based on resource defense polygyny [4]. In *C. sphinx,* the adult males are categorized into two groups, harem and nonharem males. Males construct and defend tents (resource) and recruit females to gain mating access and this organization is called a harem. In order to attract females, the harem males defend critical resources during the breeding season and this type of system is called harem-polygynous mating. Though, several studies suggest that the breeding population of *C. sphinx* also consists of nonharem males which dwell in roosts adjacent to harems [3, 4].

If this is true, what is the role of such nonharem males in the population or colony? What are the factors that cause the occurrence of nonharem males in a colony of *C. sphinx*? Are trees and foliage suitable for tent-making a scarce resource? Are solitary males less competitive and so remain isolated from the breeding activities? However, the factors responsible for the occurrence of nonharem males and mechanisms used to acquire harem male status are not understood fully.

*Dispersal Patterns, Mating Strategy and Genetic Diversity in the Short Nosed Fruit Bat… DOI: http://dx.doi.org/10.5772/intechopen.100496*

### **3.2 Materials and methods**

The study involves understanding the mating status of solitary males, bat captures were confined to day roosting places. Captures at roosting places indicated whether a male was solitary or a harem holder. Every week, we inspected trees and censused day roosts regardless of the number of incumbents (solitary or harem). Roosting groups with a single adult male with one or more adult females were considered as harems [46]. However, apart from such successful males, a number of adult males were also observed roosting solitarily. All the individuals of harems and the solitary males, which roost adjacent to the harems, were captured just before emergence using a hoop net with an extensible aluminum pole.

All the bats of harem groups and nonharem males were tagged with a colorcoded bead necklace. We used beads of ten different colors, each color denoting a number from 0 to 9. We loaded each necklace with 1–3 beads. Thus, there were 999 possible sequential arrangements of the color beads. We have used this type of tagging for various studies and have observed no apparent detrimental effects on bats. After marking, all individuals were released at the site of capture. These color coded bead necklace markings allowed us to identify individuals and determine their previous roosting locations. The census, mark-recapture and radio-telemetry studies data were used to assess the reproductive condition, mobility, roosting pattern and status of adult males (harem/nonharem).

#### **3.3 Results and discussion**

One of the striking features of tent-making male bats is that they use tents as a resource to recruit large numbers of females and copulate with them [46, 51]. Although experimental evidence supporting causal factors for resource-defense polygyny is lacking, scarcity of resources is thought to be one of the factors for aggregation of females [58]. Solitary roosting existence of some adult males is one of the main consequences of resource-defense polygyny as the males fail to defend a resource. We attempted to study the resource-defense polygyny in *C. sphinx*. We observed that there were no shortage of roosting sites and these solitary males remained reproductively active. Similar, results have been reported in a Jamaican fruit-eating bat *A. jamaicensis* [59, 60].

Our results suggest that the male success in female recruitment was not due to shortage of tents. We found that, nearly 39% of adult males were roosting alone. This observation was based on >90% of nonharem males roosting adjacent to harems and also 50% of nonharem males had scrotal testes. In addition, the mark recapture study showed that the transition status of males from nonharem to harem was possibly due to previously unobserved mode and the female recruitment is associated with resource (roost). It indicates that the solitary males are involved actively in female recruitment to their roosts and also in the process of mating. During our study we observed that many solitary males recruited females within a short period of time. A nonharem male's effort to gain access to adult female cannot be hindered by the solitary nature *per se*, which is found reliable based on expectation. Since it is a choice of every animal to represent itself genetically superior among a population, we believe that the breeding behavior of the animal is not restricted by the resource.

The mode of attaining harem male status differs from species to species. For e.g. young males of *P. hastatus* are known to gain access with harem females if the harem male dies or gets displaced [61]. It was observed that under captive conditions, two adult *C. sphinx* males, competing with each other to take control of a tent resulted in the harem male turnover. However, the turnover of harem male did not have any impact

on the cohesion of harem females [62]. In other harem forming bats, males exhibit a typical pattern during their ascendance to the dominant status. A size-based hierarchy for males in the social system was observed in *A. jamaicensis* [59, 63], with some larger harems being occupied by a small sized subordinate male apart from a dominant male. In *S. bilineata*, some individuals are associated in harems over several years and the non-territorial males build up site-specific dominant hierarchies [64] and for coalitions of male manikins (*Chiroxiphia linearis*). In order to attract females, the subordinate males perform costly displays by playing a satellite role. But they do not obtain reward immediately because the dominant male practically fathers all the young bats [65].

However, subordinate manakin males readily take the place of the dominant males in order to obtain a long term benefit from the association. Subordinate males' relationship with dominant males adds an extra benefit to the subordinate males by increasing the inclusive fitness thereby leading to higher reproductive output [66]. Our efforts to identify the morphological differences between harem males and nonharem males were not successful as we did not find substantial differences in the forearm length and body mass. This is surprising because an individual's body condition is often the most important determinant for alternative mating tactics [67, 68]. Larger and heavier males are typically dominant in male–male contests and reproduce more often [69]. In male common shrews *Sorex araneus,* the differences in body weight may vary with age [70]. Body weight of the males that differed in mate-searching behavior varied during the early stage of maturation while no significant difference was observed in the body size of both the types of adult males. In the present study, it was observed that most of the adults with T3 tooth-wear class were harem males, while the ones with T1 tooth-wear were found to be in the group where nonharem males existed. Therefore, among the first breeders, a strong competition for mates takes place. Observation made it evident that approximately 50% of males with T2 tooth-wear class were harem males while the remainders were found to be nonharem males. Also, these results suggest that harem males and nonharem males differ in age slightly.

Individuals with territory and resource, typically have a higher reproductive success than the males without territories due to strong competition for mates in a polygynous mating system. Males with territories usually monopolize and probably fertilize many females [71]. The males which does not possess any territory follow alternative mating strategy either as satellites [72, 73] or as sneakers [74, 75]. Similarly, among polygynous bats such as *Parasenecio hastatus* [20], *D. rotundus* [76] and *Saccopteryx bilineata* [77] it has been observed that the harem males monopolized the females incompletely. Chances of nonharem males fertilizing the harem females increased due to the incomplete monopolization of harem females by harem males. However, the mode of nonharem males gaining access to harem females was not clearly known to determine the "alternative strategy" [58].

The roosting preference of females seems more likely to increase the chances for nonharem males fertilizing some of the females. Apart from the mating success of nonharem males, low paternity for harem males can also occur as a result of female choice. *S. bilineata* are highly mobile and actively select their roosting location. During the course of a day, some females are found to shift their roosting territories while others disperse to other colonies. Importance of female choice specifically in highly mobile animals with harem system was reported [77]. Our radio-telemetry studies suggest that 3-postpartum *C. sphinx* females were found to be visiting a nonharem male especially during the night hours and also were involved in mating. Females were periodically shifting their tents since fluctuations were observed in the harem size on a day-to-day basis [2]. Similarly, movement of females between harems has also been observed among the polygynous bats such as *A. jamaicensis* [60, 78], *P. hastatus* [20, 24], *D. rotundus* [76] and *S. bilineata* [77, 79].

*Dispersal Patterns, Mating Strategy and Genetic Diversity in the Short Nosed Fruit Bat… DOI: http://dx.doi.org/10.5772/intechopen.100496*

Similarly, pallid bats *Antrozous pallidus* switch roosts without respect to group structure during pregnancy, but invest energy in communication to move as part of a cohesive group during lactation [80]. Storz et al. [4] reported that in *C. sphinx,* new harems are formed when parous females from an established harem join a previously solitary male in a different roost within the same colony. Reproductive success of male *C. sphinx* depends on colony structure during the previous postpartum estrus rather than current parturition [58]. Similar results have been reported in round-eared bat, *L. silvicolum* [47].

In the Bechstein's bat *M. bechsteinii* female bats frequently change between many different roosts [32]. In *M. myotis*, 16% of 435 ringed females appeared at least once in foreign colonies and about 6% switched colonies permanently [81]. Furthermore, in *P. auritus* [39] and in *R. ferrumequinum* [82] females occasionally switch colonies. Moreover, the permanence of roost sites like caves, mines and buildings, in contrast to the ephemeral nature of sites like trees, could account for patterns of roost switching observed in free-ranging bats [80]. It is well known that tree-roosting bats switch roost sites every few days, but the motivation underlying roost switching is not well understood [83]. The roost switching may reflect the maintenance of long-term social relationships between individuals of the larger colony [84]. We observed that the females of *C. sphinx* move between two or more roosts and also, many harems were completely abandoned the tents. In response to changes in access to diurnal roosts with suitable microclimates or the availability of fruit and nectar resources, female *C. sphinx* may alternate between different roosting habitats in the same local area [4], although they do not undergo seasonal migration. A similar pattern has been observed in a breeding population of the Neotropical fruit bat *C. perspicillata* and *Pteropus poliocephalus* [85].

*C. sphinx* has two well-defined parturition periods per year [11, 12, 86]. A huge difference was found between these two parturition periods while assessing the paternity of harem males [58]. The authors attributed this difference between the parturition periods to the availability of roosting sites associated with seasons. The survey also showed that average size of harem was found to be slightly higher during the dry season than during the wet season. However, we observed little correlation between harem size and availability of roost sites. In the study area, during both wet and dry seasons, bats abundantly roosted in both mast trees and palm trees. Shortage of roosting sites were rarely observed in our year long survey. Throughout the year, more than 90% of the day roosts were occupied by *C. sphinx*. Similarly, food resources in the area were also very vast to influence harem size [87].

During July and August, the frequency of nonharem males were found to be highest. Timing of sexual maturity of young males might be a probable reason, though no reports on timing of sexual maturity of young male bats in southern India. Reports from central India suggest that males born during the June–July parturition and February–March parturition were able to mate during September– October of the following year [88]. The number of nonharem males censused during August to October was relatively high in the study area. This can be attributed to the competition among first time breeding males to establish a day roost to recruit females before securing mating in October–November.

Our radio-telemetry observations suggest that females aggregated with a solitary male. Interestingly, aggregation occurred only after the male occupying a tent which was probably constructed by another male. Our tagging efforts might have probably disturbed the harem but the exciting aspect of this observation is the subsequent female aggregation and the way by which a solitary male succeeded in recruiting females. In a short span of time it may not be possible for a male to succeed in mating, if it followed the primary strategy involving construction and defense of tent leading to female recruitment. In addition, we observed that the

solitary male spent less time away from the roost at night after female recruitment by frequently visiting the roost throughout the night and by making several short foraging flights spaced randomly throughout the night [10]. This behavior is consistent with the earlier reports on the activity of harem males in *C. sphinx*, *A. jamaicensis, P. hastatus*, *C. perspicillata* and *Balionycteris maculata* [2, 24, 25, 54, 89]. This suggests that in *C. sphinx,* some type of territoriality is associated with shelter [61]. Situations under natural conditions like displacement or death of harem male can also occur though, roost abandonment of harem appears to be artificial. Among the species, the mode of attaining harem male status differs. In *A. jamaicensis* [59], *S. bilineata* [64] and *P. hastatus* [61], a size based hierarchy was observed. However, in *C. sphinx,* no such pattern has been reported*.* In order to attract maximum number of females (extreme variation in the group size) and hold them together, some recognizable factors should be considered. But, morphological features of males [90] and the characteristics of tents [2], does not influence in female recruitment.
