Bats (Mammalia: Chiroptera) are among the most successful mammals and likely display the widest range of mating systems within the Class. One mating system that is underrepresented in the Chiroptera is lek breeding, which is characterized by aggregations of sexually displaying males that are visited by receptive females who appraise male displays and actively choose mates, yet receive no direct benefits such as assistance in parenting. Leks are thought to form when males can defend neither resources nor females, making it more economical to establish small breeding territories and self-advertise through sexual displays. Lekking is rare in mammals, and it has been suggested that a lack in the mobility required by females to economically seek out aggregations of sexually displaying males may explain this rarity. Bats, like birds, do not suffer reduced mobility and yet out of over a thousand described species, only one has been confirmed to breed in leks. We examine the rarity of lekking in bats by providing an overview on the current state of knowledge of their mating systems and discuss the ecological and social determinants for the observed trends, contrasted with the prerequisites of lek-breeding behaviour. We use the breeding behaviour of New Zealand's lesser short-tailed bat Mystacina tuberculata, which is believed to be a lek breeder, as a case study for the examination of potential lekking behaviour in bats, and highlight the importance of such research for the development of effective conservation strategies.

Introduction

Lek breeding has been referred to as one of the most bizarre mating systems (Wiley, 1991), with males aggregating and establishing resource-free territories (‘leks’) and producing sexual displays for visiting females. Females visit leks solely to appraise male displays and select mates, receiving no direct benefits in the process. For these reasons, lekking species have long been used by evolutionary biologists for studying sexual selection in free-living animals, as mate choice can be investigated independently from the influence of resources and the clustering of males ensures that multiple males can be assessed by females (Höglund & Alatalo, 1995; Morales, Jiguet & Arroyo, 2001). Female selection is typified by an often extreme skew in male reproductive success, with a small proportion of males receiving the majority of copulations (e.g. Bradbury & Gibson, 1983; Bradbury, Vehrencamp & Gibson, 1985; Alatalo et al., 1992; but see Höglund & Alatalo, 1995; Johnstone & Earn, 1999).

Lekking is generally defined by four characteristics: (1) males aggregate to display within a specific area of their habitat; (2) females gain no direct benefits from males when mating (if females gain benefits from mate choice, they can only be indirect genetic benefits); (3) males provide no parental care to offspring; (4) females are free to select the males they mate with (Bradbury, 1977a, 1981). Leks may be further split into two broad categories: ‘classic’ leks involve males clustered within sight of one another, typically within a particular part of the suitable display habitat (Bradbury, 1981); or ‘exploded’ leks wherein males are separated by large distances and aggregations may only be determined statistically (Bradbury, 1981; Foster, 1983). There is no clear level of distinction between the two categories and it is important to remember when considering the criteria of mating systems that one is dealing with continuums rather than discrete categories (Bradbury, 1981).

Despite being intensively studied for over 50 years, leks remain one of the least-understood mating systems, particularly with respect to their evolution. In spite of this, five ecological and physiological prerequisites are thought to be necessary for lek formation (Höglund & Alatalo, 1995): (1) males are emancipated from parental care; (2) resources used by females are indefensible; (3) fertilization is internal (or there is no association between the chosen male and the site of oviposition in species with external fertilization); (4) high mobility allows females to accept the cost for searching for male aggregations (and for males to avoid predation attempts while displaying); (5) females have the ability to discriminate between males. Under these conditions, lek breeding has independently evolved a number of times in both vertebrates and invertebrates.

Within invertebrates, lekking is almost exclusively found in insects (particularly in highly volant groups such as swarm-forming Diptera; e.g. Spieth, 1978), but has also been described in fiddler crabs (Uca spp.; Croll & McClintock, 2000) (see Höglund & Alatalo, 1995). Among vertebrates, lekking appears to be most common in birds with the most recent review listing 148 known lek-breeding species (see Jiguet, Arroyo & Bretagnolle, 2000). Lekking behaviour has also been documented in other vertebrate taxa including amphibians (e.g. Hedlund & Robertson, 1989), fish (e.g. Clavijo, 1983) and reptiles (e.g. Wikelski, Carbone & Trillmich, 1996). In mammals, lek breeding appears to be comparatively rare compared with birds, with just over a dozen confirmed species, most of which are ungulates and pinnipeds (Table 1). While many mammals share most of the prerequisites for lek breeding, such as the absence of male parental care (Woodroffe & Vincent, 1994), the evolution of leks is likely constrained by relatively low mobility (compared with birds), apparently limiting it to predominantly large, free-roaming species.

Table 1. Mammals with reported lek or lek-like breeding behaviour

Taxa	Common name	Source	Notes
Pteropodidae
Hypsignathus monstrosus	Hammer-headed bat	Bradbury, 1977a	Classic lek
Ursidae
Ursos arctos	Brown bear	Steyaert et al., 2012	Some populations use lek-like ‘mating areas’
Dasyuridae
Antechinus stuartii	Brown antechinus	Lazenby-Cohen & Cockburn, 1988	Has since been refuted; likely to be scramble polygyny (Fisher et al., 2011)
Procyonidae
Nasua narica	White-nosed coati	Booth-Binczik, Binczik & Labisky, 2004	Described as a ‘mobile lek’ as male aggregations follow female bands
Caviidae
Galea spixii	Spix's yellow-toothed cavy	Lacher, 1981	Unconfirmed. Likely a ‘lek-like male-dominance polygyny’ (see Emlen & Oring, 1977), but would require genetic studies to confirm (T. E. Lacher Jr, pers. comm.).
Dugongidae
Dugong dugon	Dugong	Anderson, 1997	Classic lek
Otariidae
Otaria flavescens	South American sea lion	Soto & Trites, 2011	Classic lek
Zalophus californianus	California sea lion	Robertson et al., 2008	Described as a ‘modified lek’ as male display grounds become enveloped by females and pups during the whelping period (Boness, 1991)
Zalophus wollebaeki	Galapagos sea lion	Kunc & Wolf, 2008	Male behaviour resembles a lek, but likely a resource defence as females rest within male territories
Phocarctos hookeri	New Zealand sea lion	Boness, 1991	Originally described as a ‘modified lek’ but has since been reported as a harem defence polygyny (Gales, 2002)
Phocidae
Phoca vitulina richardii	Pacific harbour seal	Hayes et al., 2004	Classic lek
Odobenidae
Odobenus rosmarus divergens	Pacific walrus	Fay, Ray & Kibal'chich, 1984	Mating behaviour resembles a lek, but has characteristics of harem defence. Höglund & Alatalo (1995) suggest lek breeding is unlikely.
Cervidae
Dama dama	Fallow deer	Pemberton & Balmford, 1987	Classic lek
Cervus nippon	Sika deer	Balmford et al., 1993	Classic lek
Cervus elaphus	Red deer	Carranza, Garcia-Muñoz & Vargas, 1995	Experimentally induced via food supplementation
Rangifer tarandus	Reindeer	Leader-Williams, 1988	Höglund & Alatalo (1995) suggest lek breeding is unlikely
Bovidae
Antilope cervicapra	Blackbuck	Isvaran & Jhala, 2000	Classic lek
Kobus kob kob	Buffon's kob	Wanzie, 1988	Classic lek
Kobus kob leucotis	White-eared kob	Fryxell, 1987	Classic lek
Kobus kob thomasi	Uganda kob	Buechner & Schloeth, 1965	Classic lek
Kobus leche	Lechwe	Schuster, 1976	Classic lek
Connochaetes taurinus	Blue wildebeest	Estes, 1969	Male territories are likely too large to be classified as a classic lek (Höglund & Alatalo, 1995)
Damaliscus korrigum	Topi	Gosling, Petrie & Rainy, 1987	Classic lek
Pantholops hodgsonii	Chiru	Buzzard et al., 2008	Classic lek
Procapra przewalskii	Przewalski's gazelle	You & Jiang, 2005	Classic lek
Balaenopteridae
Megaptera novaeangliae	Humpback whale	Clapham, 1996	Described as a ‘floating lek’ as there are no clearly defined male territories and males travel freely

Bats appear to satisfy all prerequisites for lek breeding as: male parental care is yet to be conclusively described in any species (McCracken & Wilkinson, 2000); defence of roosting sites or females may be impossible in several species (e.g. McWilliam, 1990; Happold & Happold, 1996); female mate choice is likely more important for male reproductive success than in most mammals (McCracken & Wilkinson, 2000); and they are not limited by mobility. However, despite these traits lek breeding is virtually undescribed in the Order. In this paper, we discuss reasons for the apparent rarity with respect to the ecological determinants of bat mating systems while also highlighting the limited knowledge we have of these mating systems as a call for further research.

Bat mating systems and lek-like behaviour

Bats are among the most successful mammals on the planet; the evolution of flight and echolocation are thought to have contributed to rapid diversification since the Eocene (Altringham & Senior, 2005), with an estimated 1116 species extant today (Simmons, 2005). Flight has allowed bats to exploit a range of roost sites and roosting behaviours and develop a wide range of feeding habits, resulting in the greatest niche differentiation of any mammalian order (Krutzsch, 2000; Altringham & Senior, 2005). This has resulted in the evolution of numerous reproductive strategies to meet their various seasonal, ecological and social requirements. As such, bats likely show the greatest range of reproductive behaviours of all mammals (Altringham, 2011).

Most mammals (>90%) use some form of polygynous mating system (Clutton-Brock, 1989) and bats appear to follow this general pattern. Harem polygyny (one male roosting with multiple females) is likely the most common mating system, but there are a range of others including a surprising number of species that use facultative monogamy (24% of species listed by McCracken & Wilkinson, 2000), which is rare in mammals (Clutton-Brock, 1989). Also reported are species that use resource defence polygyny (e.g. Bradbury & Vehrencamp, 1977), swarming (e.g. Furmankiewicz & Altringham, 2007) and mating territories (e.g. Gerell & Lundberg, 1985) (for a review, see McCracken & Wilkinson, 2000; Altringham, 2011).

To date, the hammer-headed bat Hypsignathus monstrosus of equatorial Africa is the only species of bat confirmed to form classic leks (Bradbury, 1977a). Hammer-headed bats are the largest bats in continental Africa and display one of the most marked examples of sexual dimorphism among mammals; males are nearly twice as heavy as females and the larynx is nearly three times larger in males than females, occupying half of their body cavity (Bradbury, 1977a; Langevin & Barclay, 1990). The large larynxes of males produce the vocal displays used in courtship, consisting of loud, low-frequency honking. During the breeding season, upwards of 130 males will arrange themselves along stretches of river (spaced c. 10 m apart) and vocalize rapidly while wing-flapping. Females fly through these aggregations and hover in front of males in quick succession before selecting a male to copulate with. There appears to be high stereotypy in female selection of males with 6% of males receiving 79% of observed copulations in 1 year of study (Bradbury, 1977a).

Further descriptions of lek-like behaviour (i.e. male display clusters) in bats are rare, and either do not represent classic lek mating or remain to be confirmed as such. To date, only seven bat species other than H. monstrosus have been observed with lek-like characteristics in their breeding behaviour (Table 2). The least long-fingered bat Miniopterus minor represents perhaps the best case of unconfirmed classic lek breeding in bats. A population in coastal Kenya was observed across 2 years by McWilliam (1990), and an aggregation of 5–19 males was described occupying a ‘mating dome’ (a small erosion hollow in the roof of the colony's cave) during the breeding season. These males were both older and heavier than males outside the mating dome, and residency in the dome across three breeding seasons was limited to c. 30 males (out of a population of over 300 males), suggesting intense competition between males to retain their positions within it. Display behaviour in the dome appeared to be primarily olfactory, with males covering themselves in urine resulting in a pungent odour (McWilliam, 1988). While McWilliam (1990) argued that the male display behaviour in the mating dome suggested a lek mating system, no copulations were ever observed at this display site. Lek breeding therefore cannot be confirmed because male aggregations and display behaviour do not necessarily translate into a female preference for those males, and mating could be a random scramble.

Table 2. Bat species where lek-like breeding characteristics have been suggested in literature

	Absence of ♂ parental care	♂ Clumping (No. of males per aggregation)	No resources obtained by ♀♀	♀ Selection of ♂♂	Likely mating system	Additional explanation	Source
	Lekking criteria				Likely mating system	Additional explanation	Source
Pteropodidae
Epomops franqueti	✓a	✓¹	✓	✓a	Exploded lek	¹Male-calling territories are fairly large (0.6–0.9 ha). Copulations not observed but females show similar appraisal behaviour as female Hypsignathus monstrosus.	Bradbury, 1977a, 1981
Epomophorus wahlbergi	✓a	?²	?	?	Resource defence polygyny	²Males call from perches estimated to be c. 50 m apart. Size of aggregations not reported. Likely does not lek (Bradbury, 1977a).	Wickler & Seibt, 1976
Vespertilionidae
Pipistrellus pipistrellus	✓	✓³	?	?	Mating territories or resource defence polygyny	³Males hold large (1.2–10 ha) courtship territories located near communal roosts.	Sachteleben & von Helversen, 2006
Pipistrellus pipistrellus	✓	✓³	?	?	Mating territories or resource defence polygyny	Copulations were not observed, and it is unknown if females gain access to male day roosts.	Sachteleben & von Helversen, 2006
Pipistrellus nathusii	✓	✓ (2–3)	✗	?	Variable	Male aggregations are very small in size, and many males do not form aggregations but appear to adopt resource defence polygyny, among other strategies.	Jahelková & Horáček, 2011
Miniopteridae
Miniopterus minor	✓	✓ (5–19)	✓	?	Unknown	Copulations not observed at male aggregations	McWilliam, 1990
Phyllostomidae
Erophylla sezekorni	✓	✓ (2–9)	✗	✓	Resource defence polygyny	Females roost within the male display sites	Murray & Fleming, 2008
Mystacinidae
Mystacina tuberculata	✓	✓ (∼39)	?	?	Unknown	Currently undergoing study	C. A. Toth, unpubl. data

^a Assumed but either not reported or tested.

Franquet's epauletted fruit bat Epomops franqueti, which occurs sympatrically with H. monstrosus, is another species with lek-like breeding behaviour. Male E. franqueti establish territories of 100–200 m in diameter and produce whistle-like calls from four or five perches situated within the territories (Bradbury, 1977a). Like H. monstrosus, female E. franqueti visit male territories and hover in front of calling males to appraise them, even engaging in vocal duets with males (although copulations were not observed) (Bradbury, 1977a). The relatively large size of male territories means E. franqueti are not classic lek breeders, but would be consistent with exploded leks (Bradbury, 1981).

Determinants of bat mating systems

In mammals, polygynous mating systems appear to be largely influenced by four characteristics: (1) parental care required for offspring survival; (2) female home range size; (3) female group size and stability; (4) the density and distribution of females (Clutton-Brock, 1989; Clutton-Brock, Deutsch & Nefdt, 1993). If male assistance is required for offspring survival, obligate monogamy will result. If female home ranges are small enough, males commonly defend territories encompassing one or more female territories. If female groups are small and have stable membership, males individually defend these groups (or multiple males may defend female groups if they are large). If neither females nor their home ranges can be defended by males, males will defend mating territories within female home ranges. In areas of low female density, these territories will be relatively large and spaced far apart, but in areas of high-density male territories will be relatively small and clustered, giving rise to leks and similar mating systems (Emlen & Oring, 1977). Additional theoretical (Bradbury, Gibson & Tsai, 1986) and empirical (e.g. Bradbury et al., 1989) work has highlighted the importance of factors such as female home range size in further determining the attributes of resulting leks, such as the dispersion of male territories.

With respect to bats, the determinants of mating systems are poorly studied but are thought to operate on the same basic assumptions listed above (Altringham, 2011). Male parental care is largely absent in bats (but see Vehrencamp, Stiles & Bradbury, 1977) and the high mobility of females promotes polygyny and promiscuity (McCracken & Wilkinson, 2000). Additionally, the roosting behaviour of bats is a unique characteristic that further influences their reproductive strategies (see Kunz & Lumsden, 2003); some species roost solitarily while others form the largest aggregations of mammals on earth, numbering in millions (e.g. Davis, Herreid & Short, 1962). Roosting structures are as varied as abandoned bird, ant and termite nests; exposed tree limbs; ‘tents’ constructed from leaves; anthropogenic structures such as bridges, tombs, mines and buildings; caves; or cavities in trees. These can serve as sites for mating, hibernating, rearing offspring, and protection from predators and the elements (see Kunz & Lumsden, 2003; Altringham, 2011). Thus, the influence roosting behaviour has on the evolution of bat mating systems is significant (e.g. see Happold & Happold, 1996).

Given the importance of roosting behaviour, bat researchers must reconcile several factors to elucidate the ecological determinants of mating systems. Moreover, additional features of bat life histories may facilitate or hinder the evolution of particular mating strategies. Corrected for body size, bats are the longest-lived mammals, averaging three times longer lifespans than non-flying eutherians (Austad & Fischer, 1991); several species have been recorded with lifespans of over 30 years (Barclay & Harder, 2003). Additionally, many species of bat show female philopatry with females remaining in the area in which they were born and males dispersing (Burland & Wilmer, 2001). The combination of these characteristics promotes social systems involving female groups inhabiting the same roost (Kerth, 2008). Based on the work of Clutton-Brock (1989), we would expect harem mating systems to be common under such conditions where females are easily defended, and this appears to be the case with bats as harem polygyny is a common mating system in the Order (McCracken & Wilkinson, 2000). It should be noted, however, that not all harem-forming bats have stable female group composition (McCracken & Wilkinson, 2000) and one – Saccopteryx bilineata – exhibits female dispersal rather than male dispersal (Nagy et al., 2007), and so the lack of these features does not necessarily preclude the evolution of harems. Regardless, many species of bats are apparently predisposed to harem polygyny, rather than other strategies such as leks, due to common life history characteristics that promote this mating system. To identify lekking bats, we must then examine species that are unable to form harems due to one or more factors.

Some clues to help explain the adoption of male display clusters in bats can come from the comparison of closely related species that differ in their reproductive strategies, such as M. minor (discussed above) and Miniopterus australis. Miniopterus australis exhibits a harem polygyny system with individual males defending unstable groups of up to six females (Medway, 1971). An important difference in the life histories of the two species is their roosting behaviour; female M. minor migrate seasonally, leaving little opportunity for males to monopolize them (McWilliam, 1990). For female M. australis, the required roosting sites in small erosion domes in cave roofs are limiting and they must remain in these sites annually (Medway, 1971), thus promoting the formation of harems by males (McWilliam, 1990).

Climate also plays a large role in the evolution of bat mating systems and may provide the greatest insight on where leks are likely to evolve. In temperate regions, ecological factors promote large home ranges, seasonal migration and low population densities (Barclay & Harder, 2003; Kunz & Lumsden, 2003), all of which restrict the formation of harems (McCracken & Wilkinson, 2000; Jahelková & Horáček, 2011). In some species, males may completely avoid courtship by simply copulating with hibernating females (Bradbury, 1977b). In other cases, the conditions imposed by temperate climates require males to establish territories and attract females through self-advertisement, resulting in mating systems such as resource (i.e. roost) defence, mating territories or lek mating systems (McCracken & Wilkinson, 2000).

In summary, bat mating systems are controlled by the same factors as most other mammals, with additional factors such as complex roosting behaviour, long lifespans and a so-far universal lack of male parental care further influencing their evolution. In tropical species, this appears to translate to a tendency towards harem defence by males. Harems, however, are rarer in temperate regions, and it is therefore surprising that so few lek-breeding bat species have been documented in these regions. This is likely due in large part to a lack of studies that examine the reproductive behaviours of bats.

Mystacina tuberculata

Currently we are investigating the possibility of lek breeding in the temperate New Zealand lesser short-tailed bat M. tuberculata, as their life history and ecology make them a good candidate species for the evolution of a lek mating system. Mystacina tuberculata are medium-sized (10–20 g), tree-roosting bats associated with large (>1000 ha), old-growth native forests across New Zealand. From September to May, males individually occupy and defend small cracks and holes in trees and sing from within the cavity, presumably to attract passing females. These songs are audible to humans (although they contain ultrasonic components). In areas of high population density male ‘singing roosts’ have been reported to be clustered in space leading to the suggestion that M. tuberculata employ a lek mating system (Daniel, 1990; Lloyd, 2001). However, the breeding behaviour of M. tuberculata has never been formally investigated and so this assertion remains unconfirmed.

Mystacina tuberculata colonies are some of the largest among cavity-roosting bats (Kunz & Lumsden, 2003), with the largest communal roost trees containing upwards of 6000 individuals (Lloyd, 2001). In addition to high population densities, females possess large home ranges. Individuals radio-tracked from a population in the Eglington Valley in Fiordland ranged the entire length of the valley (26.5 km), covering an area of over 130 km², with individual home ranges covering between 3.2 and 69.3 km² (O'Donnell et al., 1999). Preliminary data from a population of M. tuberculata in the Pikiariki Ecological Area in the central North Island further suggest that males may have little opportunity to monopolize females despite the occurrence of large communal roosts, as females frequently roost away from the main colony. Of nine adult females radio-tracked across the summer of 2011–2012, eight had solitary day roosts in which they roosted an average of 57% of days tracked (range: 20–100%) (C. A. Toth, unpubl. data). The combination of high female densities, large home ranges, and frequent roost changes provide an excellent environment for the evolution of leks.

Further study will be required to reveal the level of female choice via female visits to male roosts and male reproductive success (through paternity analyses), and whether females gain access to male singing roosts as day roosts (i.e. resources). If lek breeding can be confirmed in M. tuberculata, it will be the first temperate bat conclusively demonstrated to use this mating system, allowing future research to help determine some of the appropriate ecological conditions necessary for the evolution of lek breeding in temperate bats.

Conservation implications and the need for research

Despite a lack of direct evidence, the numbers of lek breeding temperate bat species may be relatively high. Cryan (2008) has hypothesized that the high numbers of bats killed by wind turbines each year are a consequence of behaviours associated with lek breeding. Many of the species killed in North America and Europe are tree or foliage roosting, with peaks in fatalities coming in late summer and autumn. Cryan (2008) reasons that some bats could be mistaking turbines for the tallest and most mature trees in the forest, which would serve as ideal landmarks (and thus display sites) for lekking bats mating on migration. Fatalities of two species killed by wind turbines – La. borealis and La. cinereus – are largely adult males (Arnett et al., 2008), suggesting display aggregations (although the trend may also be due to separate habitat use by males and females, as sexual segregation is common in bats; Altringham & Senior, 2005).

The swarming behaviour of many temperate bats may also represent lek-like breeding. Swarming behaviour typically takes place in late summer to autumn (but has also been reported in spring; Furmankiewicz, 2008), with large groups briefly visiting potential hibernacula (caves and mines; e.g. Parsons et al., 2003). Swarms can contain thousands of individuals from several species and mating is known to occur during these events (e.g. Rivers, Butlin & Altringham, 2006). Mating in swarms appears to be superficially random with males making no obvious displays to attract females (e.g. Thomas, Fenton & Barclay, 1979); however, genetic evidence in the little brown bat Myotis lucifugus has shown that fertilizations are actually skewed towards certain males or male lineages (although this pattern could be caused by males mating during hibernation) (Watt & Fenton, 1995). Such large aggregations of mating individuals provide the opportunity for lek-like behaviour (Altringham, 2011), but swarms are poorly understood and would require further study to determine if males are displaying to females in some way and if females are actively selecting males based on these displays.

In tropical species, nightly calling behaviour similar to that observed in H. monstrosus and E. franqueti has been reported in closely related species (e.g. Wickler & Seibt, 1976; Boulay & Robbins, 1989; McCracken & Wilkinson, 2000), although there are no detailed studies describing male spacing or female choice. Thus, it is likely that several other epomophorine bats display lek-like breeding behaviour analogous to the gradients of lekking behaviour observed within several families of birds (J. W. Bradbury, pers. comm.), ranging from classic leks to exploded leks to more widely spaced mating territories (Jiguet et al., 2000). This remains to be shown, however, given the absence of detailed research.

The above examples bring us to an important point about the current state of knowledge of bat mating systems. The last comprehensive review on breeding behaviour was compiled by McCracken & Wilkinson (2000), and at that time information of reproductive behaviours was known for less than 7% of all species. The nocturnal habits of bats, their high mobility and the difficulty in reaching their roosts make it challenging to study their social interactions, particularly reproduction. The numbers of lekking bat species may be relatively high with respect to other mammals (or perhaps even to birds), but this will remain unknown without further research. Modern molecular techniques are a useful tool that could be used to overcome the difficulty in directly observing copulations that has hindered past studies (e.g. McWilliam, 1990), although the effort required in gaining such data may still be prohibitive for some species.

Leks not only offer interesting research opportunities for behavioural ecologists, but also present unique conservation considerations for species at risk. Determining the mating system of a species implicitly requires an understanding of sexually mature male and female distributions, male display site requirements, and female mate selection criteria – all of which provide information necessary for conservation (Morales et al., 2001). As of 2002, almost a quarter of known bat species were considered threatened due to factors such as habitat loss, persecution and roost site disturbance (Mickleburgh, Hutson & Racey, 2002). In the intervening time, white-nose syndrome has devastated populations of bats across eastern North America (Blehert et al., 2009). For potential lek breeding species, such as M. tuberculata (which is considered critically endangered across its range; O'Donnell et al., 2010) and other yet-described lekking bats, conservation strategies must take this distinct mating system into account. Important factors such as male display site requirements, traditional display grounds and resource distributions must all be considered when designing holistic rescue policies.

Summary and conclusions

The evolutionary origins of leks and the ecological determinants of bat mating systems are both poorly understood, and so reconciling the two is difficult without further research. It appears as though the evolution of lek breeding may be limited in bats (at least in tropical species) by life history characteristics that promote the use of harem defence by males. Because ecological constraints in temperate regions restrict the evolution of harems, males must instead focus on self-advertisement, potentially leading to the use of leks under the ideal conditions (e.g. high population densities with large home ranges, as observed in M. tuberculata). However, as Höglund & Alatalo (1995) note, given the degree to which species differ in their habitat use, ecology and life history, it should not be surprising if leks form under several different conditions. This is particularly likely in an order as successful and diverse as Chiroptera.

Any inferences on the adoption of lekking behaviour in bats are hamstrung, however, by the unfortunate lack of knowledge on bat reproduction. It is likely that the best explanation for the apparent rarity of lek breeding in bats is simply the difficulty in studying their reproduction, and we hope this paper highlights the need for further research. For example, when contrasted with birds, studies of bats have lagged in both the use of genetic tools to determine levels of polygyny and of experimentation to clarify causal factors influencing mating systems (McCracken & Wilkinson, 2000). Further research will not only provide benefits for the understanding of mating systems, but will aid in the conservation of the many species of bats at risk.

Acknowledgements

We would like to thank C. Rodgers, L. Dewell, G. Holwell, C. Jones and J. Bradbury for helpful comments and suggestions. We also thank G. Cummings and T. Dennis for assistance in the field and with analyses, as well as T. Thurley, D. Smith and the New Zealand Department of Conservation. Funding was provided by the Australasian Society for the Study of Animal Behaviour, the Australasian Bat Society, Bat Conservation International, and the University of Auckland.

References

Alatalo, R.V., Höglund, J., Lundberg, A. & Sutherland, W.J. (1992). Evolution of black grouse leks: female preferences benefit males in larger leks. Behav. Ecol. 3, 53–59.
Altringham, J.D. (2011). Bats: from evolution to conservation. 2nd edn. New York: Oxford University Press.
Altringham, J.D. & Senior, P. (2005). Social systems and ecology of bats. In Sexual segregation in vertebrates: ecology of the two sexes: 280–302. K.E. Ruckstuhl & P. Neuhaus (Eds). Cambridge: Cambridge University Press.
Anderson, P.K. (1997). Shark Bay dugongs in summer. I: lek mating. Behaviour 134, 433–462.
Arnett, E.B., Brown, W., Erickson, W.P., Fiedler, J.K., Hamilton, B.L., Henry, T.H., Jain, A., Johnson, G.D., Kerns, J. & Koford, R.R. (2008). Patterns of bat fatalities at wind energy facilities in North America. J. Wildl. Manage. 72, 61–78.
Austad, S.N. & Fischer, K.E. (1991). Mammalian aging, metabolism, and ecology: evidence from the bats and marsupials. J. Gerontol. 46, B47–B53.
Balmford, A., Bartoš, L., Brotherton, P., Herrmann, H., Lancingerova, J., Mika, J. & Zeeb, U. (1993). When to stop lekking: density-related variation in the rutting behaviour of sika deer. J. Zool. (Lond.) 231, 652–656.
Barclay, R.M.R. & Harder, L.D. (2003). Life histories of bats: life in the slow lane. In Bat ecology: 209–253. T. Kunz & M. Fenton (Eds). Chicago: University of Chicago Press.
Blehert, D.S., Hicks, A.C., Behr, M., Meteyer, C.U., Berlowski-Zier, B.M., Buckles, E.L., Coleman, J.T.H., Darling, S.R., Gargas, A. & Niver, R. (2009). Bat white-nose syndrome: an emerging fungal pathogen? Science 323, 227.
Boness, D. (1991). Determinants of mating systems in the Otariidae (Pinnipedia). In The behaviour of pinnipeds: 1–44. D. Renouf (Ed.). London: Chapman and Hall.
Booth-Binczik, S., Binczik, G. & Labisky, R. (2004). Lek-like mating in white-nosed coatis (Nasua narica): socio-ecological correlates of intraspecific variability in mating systems. J. Zool. (Lond.) 262, 179–185.
Boulay, M.C. & Robbins, C.B. (1989). Epomophorus gambianus. Mamm. Species 344, 1–5.
Bradbury, J., Vehrencamp, S. & Gibson, R. (1985). Leks and the unanimity of female choice. In Evolution: essays in honour of John Maynard Smith: 301–314. P.J. Greenwood, P.H. Harvey & M. Slatkin (Eds). Cambridge: Cambridge University Press.
Bradbury, J., Gibson, R. & Tsai, I.M. (1986). Hotspots and the evolution of leks. Anim. Behav. 34, 1694–1709.
Bradbury, J.W. (1977a). Lek mating behavior in the hammer-headed bat. Z. Tierpsychol. 45, 225–255.
Bradbury, J.W. (1977b). Social organization and communication. In The biology of bats: 1–72. W. Wimsatt (Ed.). New York: Academic Press.
Bradbury, J. & Vehrencamp, S.L. (1977). Social organization and foraging in emballonurid bats, III. mating systems. Behav. Ecol. Sociobiol. 2, 1–17.
Bradbury, J.W. (1981). The evolution of leks. In Natural selection and social behaviour: 138–169. R.D. Alexander & D.W. Tinkle (Eds). New York: Chiron Press.
Bradbury, J.W. & Gibson, R.M. (1983). Leks and mate choice. In Mate choice: 109–138. P. Bateson (Ed.). Cambridge: Cambridge University Press.
Bradbury, J.W., Gibson, R.M., McCarthy, C.E. & Vehrencamp, S.L. (1989). Dispersion of displaying male sage grouse: II. The role of female dispersion. Behav. Ecol. Sociobiol. 24, 15–24.
Buechner, H.K. & Schloeth, R. (1965). Ceremonial mating behavior in Uganda kob (Adenota kob thomasi Neumann)*. Z. Tierpsychol. 22, 209–225.
Burland, T.M. & Wilmer, J.W. (2001). Seeing in the dark: molecular approaches to the study of bat populations. Biol. Rev. Camb. Philos. Soc. 76, 389–409.
Buzzard, P., Bleisch, W., Xü, D. & Zhang, H. (2008). Evidence for lekking in chiru. J. Zool. (Lond.) 276, 330–335.
Carranza, J., Garcia-Muñoz, A.J. & Vargas, J.D. (1995). Experimental shifting from harem defence to territoriality in rutting red deer. Anim. Behav. 49, 551–554.
Clapham, P.J. (1996). The social and reproductive biology of humpback whales: an ecological perspective. Mamm. Rev. 26, 27–49.
Clavijo, I.E. (1983). Pair spawning and formation of a lek-like mating system in the parrotfish Scarus vetula. Copeia 1983, 253–256.
Clutton-Brock, T. (1989). Mammalian mating systems. Proc. R. Soc. Lond., B, Biol. Sci. 236, 339–372.
Clutton-Brock, T., Deutsch, J. & Nefdt, R. (1993). The evolution of ungulate leks. Anim. Behav. 46, 1121–1138.
Croll, G.A. & McClintock, J.B. (2000). An evaluation of lekking behavior in the fiddler crab Uca spp. J. Exp. Mar. Biol. Ecol. 254, 109–121.
Cryan, P.M. (2008). Mating behavior as a possible cause of bat fatalities at wind turbines. J. Wildl. Manage. 72, 845–849.
Daniel, M. (1990). Report on a visit to Codfish Island and Poutama Island to study short-tailed bats 28 February–28 March 1990. Unpublished report. Invercargill, Department of Conservation.
Davis, R.B., Herreid, C.F. & Short, H.L. (1962). Mexican free-tailed bats in Texas. Ecol. Monogr. 32, 311–346.
Emlen, S.T. & Oring, L.W. (1977). Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223.
Estes, R. (1969). Territorial behaviour of the wildebeest (Connochaetes taurinus Burchell, 1823). Z. Tierpsychol. 26, 284–370.
Fay, F., Ray, G. & Kibal'chich, A. (1984). Time and location of mating and associated behavior of the Pacific walrus, Odobenus rosmarus divergens Illiger. In Society of American Cooperative Research on Marine Mammals, Vol. 1: Pinniped: 89–99. F. Fay & G. Fedoseev (Eds). Fairbanks, Alaska: NOAA Technical Report NMFS 12.
Fisher, D.O., Nuske, S., Green, S., Seddon, J.M. & McDonald, B. (2011). The evolution of sociality in small, carnivorous marsupials: the lek hypothesis revisited. Behav. Ecol. Sociobiol. 65, 593–605.
Foster, M.S. (1983). Disruption, dispersion, and dominance in lek-breeding birds. Am. Nat. 122, 53–72.
Fryxell, J.M. (1987). Lek breeding and territorial aggression in white-eared kob. Ethology 75, 211–220.
Furmankiewicz, J. & Altringham, J. (2007). Genetic structure in a swarming brown long-eared bat (Plecotus auritus) population: evidence for mating at swarming sites. Conserv. Genet. 8, 913–923.
Furmankiewicz, J. (2008). Population size, catchment area, and sex-influenced differences in autumn and spring swarming of the brown long-eared bat (Plecotus auritus). Can. J. Zool. 86, 207–216.
Gales, N.J. (2002). New Zealand sea lion Phocarctos hookeri. In Encyclopedia of marine mammals: 763–765. F.P. William, B. Würsig & J. Thewissen (Eds). Amsterdam: Academic Press.
Gerell, R. & Lundberg, K. (1985). Social organization in the bat Pipistrellus pipistrellus. Behav. Ecol. Sociobiol. 16, 177–184.
Gosling, L., Petrie, M. & Rainy, M. (1987). Lekking in topi: a high cost, specialist strategy. Anim. Behav. 40, 616–618.
Happold, D. & Happold, M. (1996). The social organization and population dynamics of leaf-roosting banana bats, Pipistrellus nanus (Chiroptera, Vespertilionidae), in Malawi, east-central Africa. Mammalia 60, 517–544.
Hayes, S.A., Costa, D.P., Harvey, J.T. & Boeuf, B.J. (2004). Aquatic mating strategies of the male Pacific harbor seal (Phoca vitulina richardii): are males defending the hotspot? Mar. Mamm. Sci. 20, 639–656.
Hedlund, L. & Robertson, J.G.M. (1989). Lekking behaviour in crested newts, Triturus cristatus. Ethology 80, 111–119.
Höglund, J. & Alatalo, R.V. (1995). Leks. Princeton: Princeton University Press.
Isvaran, K. & Jhala, Y. (2000). Variation in lekking costs in blackbuck (Antilope cervicapra): relationship to lek-territory location and female mating patterns. Behaviour 137, 547–563.
Jahelková, H. & Horáček, I. (2011). Mating system of a migratory bat, Nathusius' Pipistrelle (Pipistrellus nathusii): different male strategies*. Acta Chiropt. 13, 123–137.
Jiguet, F., Arroyo, B. & Bretagnolle, V. (2000). Lek mating systems: a case study in the Little Bustard Tetrax tetrax. Behav. Processes 51, 63–82.
Johnstone, R.A. & Earn, D.J.D. (1999). Imperfect female choice and male mating skew on leks of different sizes. Behav. Ecol. Sociobiol. 45, 277–281.
Kerth, G. (2008). Causes and consequences of sociality in bats. Bioscience 58, 737–746.
Krutzsch, P. (2000). Anatomy, physiology and cyclicity of the male reproductive tract. In Reproductive biology of bats: 91–155. E.G. Crichton & P.H. Krutzsch (Eds). New York: Academic Press.
Kunc, H.P. & Wolf, J.B.W. (2008). Seasonal changes of vocal rates and their relation to territorial status in male Galápagos sea lions (Zalophus wollebaeki). Ethology 114, 381–388.
Kunz, T.H. & Lumsden, L.F. (2003). Ecology of cavity and foliage roosting bats. In Bat ecology: 3–89. T.H. Kunz & L.F. Lumsden (Eds). Chicago: The University of Chicago Press.
Lacher, T.E. (1981). The comparative social behavior of Kerodon rupestris and Galea spixii and the evolution of behavior in the Caviidae. Bull. Carnegie Mus. Nat. Hist. 17, 1–71.
Langevin, P. & Barclay, R.M.R. (1990). Hypsignathus monstrosus. Mammal. Species 357, 1–4.
Lazenby-Cohen, K.A. & Cockburn, A. (1988). Lek promiscuity in a semelparous mammal, Antechinus stuartii (Marsupialia: Dasyuridae)? Behav. Ecol. Sociobiol. 22, 195–202.
Leader-Williams, N. (1988). Reindeer on South Georgia. Cambridge: Cambridge University Press.
Lloyd, B.D. (2001). Advances in New Zealand mammalogy 1990–2000: short-tailed bats. J. R. Soc. N. Z. 31, 59–81.
McCracken, G.F. & Wilkinson, G.S. (2000). Bat mating systems. In Reproductive biology of bats: 321–362. E.G. Crichton & P.H. Krutzsch (Eds). New York: Academic Press.
McWilliam, A.N. (1988). The reproductive cycle of male long-fingered bats, Miniopterus minor (Chiroptera: Vespertilionidae), in a seasonal environment of the African Tropics. J. Zool. (Lond.) 216, 119–129.
McWilliam, A.N. (1990). Mating system of the bat Miniopterus minor (Chiroptera: Vespertilionidae) in Kenya, East Africa: a lek? Ethology 85, 302–312.
Medway, L. (1971). Observations of social and reproductive biology of the bent-winged bat Miniopterus australis in northern Borneo. J. Zool. (Lond.) 165, 261–273.
Mickleburgh, S.P., Hutson, A.M. & Racey, P.A. (2002). A review of the global conservation status of bats. Oryx 36, 18–34.
Morales, M.B., Jiguet, F. & Arroyo, B. (2001). Exploded leks: what bustards can teach us. Ardeola 48, 85–98.
Murray, K.L. & Fleming, T.H. (2008). Social structure and mating system of the Buffy flower bat, Erophylla sezekorni (Chiroptera, Phyllostomidae). J. Mammal. 89, 1391–1400.
Nagy, M., Heckel, G., Voigt, C.C. & Mayer, F. (2007). Female-biased dispersal and patrilocal kin groups in a mammal with resource-defence polygyny. Proc. Biol. Sci. 274, 3019–3025.
O'Donnell, C.F.J., Christie, J., Corben, C., Sedgeley, J.A. & Simpson, W. (1999). Rediscovery of short-tailed bats (Mystacina sp.) in Fiordland, New Zealand: preliminary observations of taxonomy, echolocation calls, population size, home range, and habitat use. N.Z. J. Ecol. 23, 21–30.
O'Donnell, C.F.J., Christie, J.E., Hitchmough, R.A., Lloyd, B. & Parsons, S. (2010). The conservation status of New Zealand bats, 2009. N.Z. J. Zool. 37, 297–311.
Parsons, K.N., Jones, G., Davidson-Watts, I. & Greenaway, F. (2003). Swarming of bats at underground sites in Britain – implications for conservation. Biol. Conserv. 111, 63–70.
Pemberton, J. & Balmford, A. (1987). Lekking in fallow deer. J. Zool. (Lond.) 213, 762–765.
Rivers, N.M., Butlin, R.K. & Altringham, J.D. (2006). Autumn swarming behaviour of Natterer's bats in the UK: population size, catchment area and dispersal. Biol. Conserv. 127, 215–226.
Robertson, K.L., Runcorn, C.W., Young, J.K. & Gerber, L.R. (2008). Spatial and temporal patterns of territory use of male California sea lions (Zalophus californianus) in the Gulf of California, Mexico. Can. J. Zool. 86, 237–244.
Sachteleben, J. & Von Helversen, O. (2006). Songflight behaviour and mating system of the pipistrelle bat (Pipistrellus pipistrellus) in an urban habitat. Acta Chiropt. 8, 391–401.
Schuster, R.H. (1976). Lekking behavior in Kafue lechwe. Science 192, 1240–1242.
Simmons, N.B. (2005). Order chiroptera. In Mammal species of the world: a taxonomic and geographic reference: 312–529. D.E. Wilson & D.M. Reeder (Eds). Baltimore: Johns Hopkins University Press.
Soto, K.H. & Trites, A.W. (2011). South American sea lions in Peru have a lek-like mating system. Mar. Mamm. Sci. 27, 306–333.
Spieth, H.T. (1978). Courtship patterns and evolution of the Drosophila adiastola and planitibia species subgroups. Evolution 32, 435–451.
Steyaert, S.M.J., Endrestøl, A., Hackländer, K., Swenson, J.E. & Zedrosser, A. (2012). The mating system of the brown bear Ursus arctos. Mamm. Rev. 42, 12–34.
Thomas, D.W., Fenton, M.B. & Barclay, R.M.R. (1979). Social behavior of the little brown bat, Myotis lucifugus. I. Mating behavior. Behav. Ecol. Sociobiol. 6, 129–136.
Vehrencamp, S.L., Stiles, F.G. & Bradbury, J.W. (1977). Observations on the foraging behavior and avian prey of the neotropical carnivorous bat, Vampyrum spectrum. J. Mammal. 58, 469–478.
Wanzie, C. (1988). Sociability of Buffon's kob (Kobus kob kob Erxleben) in Waza national park, Cameroon. Mammalia 52, 21–33.
Watt, E.M. & Fenton, M.B. (1995). DNA fingerprinting provides evidence of discriminate suckling and non-random mating in little brown bats Myotis lucifugus. Mol. Ecol. 4, 261–264.
Wickler, W. & Seibt, U. (1976). Field studies on the African fruit bat Epomophorus wahlbergi (Sundevall), with special reference to male calling. Z. Tierpsychol. 40, 345–376.
Wikelski, M., Carbone, C. & Trillmich, F. (1996). Lekking in marine iguanas: female grouping and male reproductive strategies. Anim. Behav. 52, 581–596.
Wiley, R.H. (1991). Lekking in birds and mammals: behavioral and evolutionary issues. Adv. Study Behav. 20, 201–291.
Woodroffe, R. & Vincent, A. (1994). Mother's little helpers: patterns of male care in mammals. Trends Ecol. Evol. 9, 294–297.
You, Z.Q. & Jiang, Z.G. (2005). Courtship and mating behaviors in Przewalski's gazelle Procapra przewalskii. Curr. Zool. 52, 187–194.

Citing Literature

Volume291, Issue1

September 2013

Pages 3-11

Is lek breeding rare in bats?

Abstract

Introduction

Bat mating systems and lek-like behaviour

Determinants of bat mating systems

Mystacina tuberculata

Conservation implications and the need for research

Summary and conclusions

Acknowledgements

References

Citing Literature

References

Information

About Wiley Online Library

Help & Support

Opportunities

Connect with Wiley

Is lek breeding rare in bats?

Abstract

Introduction

Bat mating systems and lek-like behaviour

Determinants of bat mating systems

Mystacina tuberculata

Conservation implications and the need for research

Summary and conclusions

Acknowledgements

References

Citing Literature

References

Related

Information