SPECIAL SECTION: ANIMAL BEHAVIOUR Midnight’s children?: Solitary primates and gregarious chiropterans Sindhu Radhakrishna National Institute of Advanced Studies, Indian Institute of Science Campus, Bangalore 560 012, India than arboreal, folivorous (leaf-eating) and nocturnal pri- Some primate species exhibit a solitary social organi- zation. Among several ecological and biological para- mates. meters that have been forwarded as correlates of a Amidst the diversity of social organizations displayed solitary lifestyle, a nocturnal activity cycle is considered by primates, the solitary lifestyle adopted by some of the an important determinant. However, several species of species has excited enormous debate. Many reasons have megachiropterans, a mammalian group that is com- been propounded to explain this; chiefly, they are (i) a pletely nocturnal, live in large multimale–multifemale nocturnal activity cycle, (ii) small body size, (iii) a dietary groups. A comparative review of primate and megachi- reliance on substances that occur in small patches, like ropteran behavioural adaptations shows that megachi- animal prey and gum, and (iv) lack of predator pressure4. ropterans do not exhibit the expected correlates of a None of these reasons are completely satisfactory4; they nocturnal lifestyle. It is suggested that detailed studies appear even less so when compared with the megachirop- of megachiropteran social structures may reveal impor- terans, a group of bats that are nocturnal, fairly large in tant pointers to the adaptive bases of a solitary social life. size, and frugivorous, and mostly tend to live in large multimale–multifemale groups. The following sections Keywords: Bats, gregarious, nocturnal, primates, social briefly review the two orders and compare the two groups organization, solitary. in order to discern similarities or differences in their behav- ioural adaptations. MEMBERS of the mammalian orders Chiroptera (bats) and Primates (primates) compel attention on account of their singular morphological and behavioural adaptations. Chi- Chiropterans ropterans are one of the most successful and diverse of mammalian orders and the only mammals capable of The chiropterans are the second largest mammalian order 1,2 powered flight . Echolocation or orientation by analysis and certainly the most diverse. More than 900 species are of echoes from emitted sound pulses, reaches an evolu- recognized that inhabit the tropical and temperate zones tionary peak of development in bats and the majority of of the world2. Bats come in many sizes, shapes and col- the species forage and orient using echolocation. Chirop- ours and possess the most amazing facial features in the terans also possess another interesting adaptation – torpor, form of extravagant noseleaves and protuberances2. They or the ability to reduce body temperature and save energy roost in all possible places – in caves, rock crevices, behind when insect availability is low and later return to full oper- tree bark, in the open against tree trunks, in man-made ating body temperature. The variety in dietary specializa- structures like mines and tunnels and even inside the tions that occurs here is unseen in any other mammalian flowers of the water arum!1. Sophisticated physiological order – from fruits, nectar, pollen, and insects to fish, adaptations accompany the diverse dietary specializations 1 amphibians, reptiles, birds, mammals and blood . found in many of the species, for example, the fish-eating The most unusual aspect that secerns the primate order is species have long, sharp claws for gaffing fish, vampire 3 the remarkable sociality of its member species . Not only bats have efficient kidneys that switch modes from water- do the majority of the species live in large stable groups expelling to water conserving during and after feeding, that are maintained by complex interactions between and the nectar feeders have long and bristly tongues that group members, many elaborate sets of behaviours medi- are useful for pollen grooming and nectar extraction1. ate long-term social relationships between individuals. Bats roost individually, in small groups or in large colo- However, this sociality is not exhibited uniformly, but nies that may include up to 20 million bats1. shows differences in expression depending on the activity Taxonomically two suborders exist – Megachiroptera or cycle (diurnal, nocturnal or cathemeral) and ecology of frugivorous megabats, and Microchiroptera or the insec- 3 the species . For example, terrestrial, frugivorous (fruit- tivorous microbats. The megachiropterans feed on flowers, eating) and diurnal primates tend to live in larger groups fruit, nectar and pollen and are confined in their distribution to the Old World tropics. Although considerable variation e-mail: [email protected] in size occurs within the suborder (from 20 g to 1.5 kg), 1208 CURRENT SCIENCE, VOL. 89, NO. 7, 10 OCTOBER 2005 SPECIAL SECTION: ANIMAL BEHAVIOUR as a group they tend to be larger than the microchiropterans. order is vertically divided into the suborders Strepsirrhini The microchiropterans, as the name implies, are much (lemurs, lorises and bushbabies) and Haplorrhini (tarsiers, smaller in size (1.5–150 g), but they far exceed the megachi- monkeys, apes and humans). Strepsirrhines are restricted ropterans in number and distribution. There are about 757 in distribution to the tropics and sub-tropics of Madagascar, extant species and 17 families (in comparison, the megachi- Africa, south and south-east Asia10, while the Haplor- ropterans number about 159 species, all belonging to one rhines inhabit the tropical areas of Asia, Africa, Europe, family) and they are found on every continent in the world, South and Central America. except Antartica. The microbat dietary adaptations are equally varied – they feed on insects, fruit, nectar, pollen, Cheirogaleidae dwarf, mouse and fork-crowned lemurs Lemuridae ring-tailed, bamboo and ruffed lemurs vertebrates and blood. Megaladapidae sportive lemurs Strepsirrhini Indridae indris, avahis and sifakas Daubentoniidae aye-aye Loridae angwantibos, pottos, slender and slow lorises Megachiroptera Pteropodidae Old World fruit bats Galagonidae bushbabies Rhinopomatidae mouse-tailed bats Primates Tarsiidae tarsiers Craseonycteridae bumblebee bat Cebidae marmosets, tamarins, capuchins, and squirrel Emballonuridae sheath-tailed bats monkeys Aotidae night monkeys Chiroptera Rhinolophidae horseshoe bats Pitheciidae sakis, uakaris and titis Hipposideridae Old World leaf-nosed bats Haplorrhini Atelidae howlers, muriquis, spider and woolly monkeys Nycteridae slit-faced bats Cercopithecidae talapoins, vervets, guenons, macaques, Megadermatidae false vampire bats mangabeys, baboons, colobus monkeys and langurs Mystacinidae short-tailed bats Hylobatidae gibbons Microchiroptera Noctilionidae bulldog bats Hominidae orangutans, chimpanzees, gorillas and humans Mormoopidae naked-backed bats Phyllostomidae New World leaf-nosed bats Vespertilionidae vesper bats Natalidae funnel-eared bats Furipteridae smoky bats Many morphological and behavioural differences sepa- Thyropteridae disc-winged bats rate the two suborders. The strepsirrhines are distinguished by Myzopodidae sucker-footed bat Molossidae free-tailed bats the retention of many primitive anatomical adaptations, for example, they possess a moist rhinarium, toothcomb, grooming claws, tapetum lucidum and an unfused mandible. In addition, they also largely nocturnal and small-sized, The most striking difference between megachiropterans possess shorter life history parameters, a relatively smaller and microchiropterans is that the former orient primarily brain and rely more on olfaction. In comparison, the hap- by vision, and the latter primarily by echolocation. Only a lorrhines have retinal fovea, nails instead of claws, more few megabat species, belonging to the genus Rousettus, conservative dentition and a fused mandibular symphasis. produce tongue-clicking orientation sounds. Other, less They are also largely diurnal, bigger in size, possess conspicuous differences exist between the two suborders longer life history parameters and relatively larger brains, – microbat pinnae are often complex, with a cartilaginous and rely more on vision. projection called the tragus present inside the pinna; megabat pinnae on the other hand, are simple and the tragus is never present. Again, the structure of the teeth in microchi- Chiropterans–primates relationship ropterans is clear proof for insectivorous ancestry, while The association of chiropterans and primates dates back megabat teeth show no such evidence. All these differ- to 1758, when Linnaeus originally classified chiropterans ences, discussed exhaustively by Pettigrew et al.5, led as primates, after studying megachiropterans1. Subsequently, many authors5–7 to propose that chiropterans are actually chiropterans were classified in a separate order and in- diphyletic in origin, i.e. megachiropterans and microchi- cluded with primates, tree shrews and dermopterans in the ropterans evolved separately. super order Archonta12. The chiropterans–primates rela- tionship was first suggested by Smith and Madkour7 who Primates pointed out that megachiropterans shared morphological characteristics of the penis with primates that were not seen Living primates fall into a naturally ordered hierarchical in microchiropterans. Hence, megachiropterans evolved scale – from the smallest primate, the pygmy mouse lemur, from primates, while microchiropterans