Reproductive biology of the slender loris (Loris lydekkerianus lydekkerianus)

The slender loris (Loris lydekkerianus lydekkerianus), a nocturnal prosimian, was studied for 21 months in its natural habitat of scrub jungle in Dindigul, south India. Here we report on its reproductive biology. Identified and unidentified lorises were observed for a total of 2,656 h. Reproductive seasonality was seen, with births and oestrus observed to be highest in April-June and October-December. The mating system was promiscuous with 1 female mating successively with 3-4 males. A gestation period of 5.5 months and an inter-birth interval of 7 months were recorded. Adult females had a reproductive potential of 4 infants per year. The findings presented in this paper constitute the first information on the life history parameters of wild slender lorises.     

Diet and Feeding Behavior of Mysore Slender Lorises

We studied the feeding ecology of the Mysore slender loris (Loris lydekkerianus lydekkerianus) for 10.5 mo in a dry scrub forest at Ayyalur Interface Forestry Division, Tamil Nadu, South India. We recorded and analyzed 1240 feeding incidents, which indicate that the lorises were almost exclusively faunivorous, with 96% of all feeding events representing animal prey. Of prey items that could be identified (n = 605), 62.9% were ants and termites. Lorises fed on 9 orders and 17 families of insects, plus spiders, molluscs, and small vertebrates. Lorises infrequently fed on gums and a legume pod. They usually grabbed prey with one hand, while other appendages firmly held the substrate. Many of the identifiable prey items belong to insect taxa likely to contain toxic chemicals. Consumption of insects inferred to be toxic was accompanied by an elaborate behavioral repertoire of sneezing, slobbering and urine-washing. A high proportion of insects eaten by slender lorises (71%) occurred in patches or aggregations. The utilization of aggregated social insects may have implications for understanding the unusually high degree of gregarious behavior exhibited by the lorises.     

Social lives of adult Mysore slender lorises (Loris lydekkerianus lydekkerianus)

Despite the persistent use of the word "solitary" to describe nocturnal primate social behavior, increasing numbers of studies are revealing sophisticated levels of social interactions among nocturnal primates. This study explores the relationships among 11 adult Mysore slender lorises (Loris lydekkerianus lydekkerianus) studied over 10(1/2) months in Tamil Nadu, India. When all observations regarding dependent offspring are excluded, the animals spent on average 38% of their activity in various forms of neutral, affiliative, and agonistic behaviors. Affiliative behaviors were the most common type of social interaction, and males in general were more social than females. Low values for Cole's index (CI) of association emphasize that females rarely interacted with same-sex conspecifics, but commonly interacted with males. In turn, males also formed strong affiliative relationships with other adult males. This index also indicates that levels of affiliation are strongest among animals that share sleeping sites. The Hinde index (HI) suggests that males control proximity to females more than the reverse. A female's tolerance of multiple males in her home range and at a sleeping site may be related to high spatial variability of food resources. Such resources may constrain females with costly reproductive strategies (up to two sets of twins per annum) to a small home range. With their larger home ranges, males may be able to monopolize females by initiating social interactions, and also provide a benefit to females by contributing to parental care.     

Activity budget and positional behavior of the Mysore slender loris (Loris tardigradus lydekkerianus): implications for slow climbing locomotion.

Both predator defense and feeding ecology models have been proposed to explain the relatively slow climbing locomotion of the Lorisinae. During a study of the socioecology of the Mysore slender loris (Loris tardigradus lydekkerianus) in Tamil Nadu, India, six categories of behavior and eleven different postures were recorded to estimate a general activity budget for the slender loris, and are examined here particularly in relation to slow climbing locomotor strategies. Reactions to potential predators are also described. The main study population was composed of 15 animals. Activity budgets were compiled in three ways: all instantaneous point samples collected over 1,173 h pooled (n = 13,717), the means of individual lorises (n = 15) and behavior at the moment of first contact (n = 357). No significant difference was found between these three data sets. Approximately 45% of the activity budget was spent in inactive behaviors including sitting vigilant, resting and sleeping. Foraging and traveling comprised nearly half the activity budget, with the rest of the time spent grooming. The most common postures assumed by lorises were sitting and quadrupedal walking. Individual lorises were relatively gregarious and spent up to half their activity budget with other animals. Unlike pottos and angwantibos, lorises did not freeze, head butt or drop from branches in reaction to potential predators, but either ignored them, fled or made loud calls. Cryptic and slow climbing locomotion were used before traveling on open ground between discontinuous substrates, thereby supporting hypotheses relating to predator pressure, and also before capturing fast moving insect prey, supporting hypotheses relating to diet. It is proposed that a divergence in foraging strategies between bushbabies and lorisines may be the best adaptive explanation for their behavioral and morphological differences, including predator defense mechanisms.     

Rethinking Primate Origins Again

In 1974, Cartmill introduced the theory that the earliest primate adaptations were related to their being visually oriented predators active on slender branches. Given more recent data on primate‐like marsupials, nocturnal prosimians, and early fossil primates, and the context in which these primates first appeared, this theory has been modified. We hypothesize that our earliest primate relatives were likely exploiting the products of co‐evolving angiosperms, along with insects attracted to fruits and flowers, in the slender supports of the terminal branch milieu. This has been referred to as the primate/angiosperm co‐evolution theory. Cartmill subsequently posited that: “If the first euprimates had grasping feet and blunt teeth adapted for eating fruit, but retained small divergent orbits…” then the angiosperm coevolution theory would have support. The recent discovery of Carpolestes simpsoni provides this support. In addition, new field data on small primate diets, and a new theory concerning the visual adaptations of primates, have provided further evidence supporting the angiosperm coevolution theory.Am. J. Primatol. 75:95‐106, 2013. © 2012 Wiley Periodicals, Inc.     

Primate origins: Lessons from a neotropical marsupial

The didelphid Caluromys shows evolutionary convergence towards prosimians in having a relatively large brain, large eyes, small litters, slow development, and agile locomotion. The selection pressures that favored the emergence of primate-like traits in Caluromys from a generalized didelphid ancestor may be analogous to the selection pressures favoring the initial divergence of primates from a primitive nonprimate ancestor, and thus Caluromys provides an independent test of the arboreal hypothesis (Smith: Annual Report of the Board of Regents of the Smithsonian Institution 1912:553–572, 1913), the visual predation hypothesis (Cartmill: The Functional and Evolutionary Biology of Primates, pp. 97–122, 1972), and the angiosperm exploitation hypothesis (Sussman: American Journal of Primatology, in press) of primate origins. Quantitative data on free-ranging C. derbianus in Costa Rica demonstrate that it is highly arboreal, uses visually directed predation to capture arthropod prey, and makes extensive use of terminal branch foraging, where it feeds on small angiosperm products. These observations are consistent with predictions from each model of primate origins, thus suggesting that the hypotheses are not mutually exclusive but are interdependent. The initial divergence of primates probably involved exploitation of the rich angiosperm products and associated insects found in fine terminal branches; visually directed predation may have evolved as an efficient method of insect capture in the terminal branch milieu.     

Distribution Patterns of Slender Loris Subspecies (<Emphasis Type="Italic">Loris lydekkerianus</Emphasis>) in Kerala,Southern India

Gray slender lorises (Loris lydekkerianus) are 1 of 2 nocturnal primate genera occurring in India. Although the distribution and abundance of the species is known for some parts of southern India, the relative distribution of the 2 subspecies, Loris lydekkerianus lydekkerianus and L. l. malabaricus, and their comparative densities and extent of overlap between their distributions remains largely unknown. We investigated the distribution pattern and relative density of slender lorises in the Western Ghats mountain range in the state of Kerala in southern India. We surveyed 36 forest ranges in 17 forest divisions of northern and central Kerala from February to November 2009 for the presence of lorises. We sighted slender lorises in 22 forest ranges in a variety of vegetation types, and the relative abundance of the species ranged from 0.02 to 1.44 lorises/km. Our results confirm that both loris subspecies are present in Kerala: Mysore slender lorises have a narrow patchy distribution on the eastern edges of the Western Ghats mountain range, and Malabar slender lorises have a fairly contiguous distribution on the western slopes of the Western Ghats. We recommend more detailed surveys in southern Kerala to identify the distribution patterns of the subspecies in these areas.     

Spacing system of the Mysore slender loris (Loris lydekkerianus lydekkerianus)

Loris lydekkerianus lydekkerianus has been shown to have a promiscuous copulatory pattern, to maintain social networks via frequent loud calls, to interact socially throughout the night with all age classes, and to sleep socially. Though these behaviors point towards a multimale social system, no study of their spacing system has yet been provided to support this view. From October 1997-August 1998, I conducted a study of the Mysore slender loris in Ayyalur, India. During 1,400 field hours, data were collected on range use of 3 adult females, 3 adult males, 1 subadult female, and 1 subadult male. Lorises slept in groups averaging 4 individuals, composed of an adult female, her offspring, and 1-2 adult and subadult males. Sleeping sites for three groups were located within 1.9 ha in the center of the study area. The minimum convex polygon in hectares encompassing each animal's range was determined, as well as overlap among home ranges of individual lorises. Average home range sizes were: adult males, 3.6 ha +/- 0.09; subadult/smaller males, 1.17 ha +/- 0.26; and adult and subadult females, 1.59 ha +/- 0.24. Male ranges overlapped with at least 2-3 other adult males (0.72 ha +/- 0.23). Female ranges overlapped slightly with at least 2 other female ranges (0.22 ha +/- 0.25). Male ranges overlapped those of at least 3 females (0.82 ha +/- 0.51). Patterns of home range and sleeping site support previous suggestions of a multimale social system, similar to aye ayes and some galagos.     

Distribution, Habitat Correlates, and Conservation of Loris lydekkerianus in Karnataka, India

We surveyed slender lorises (Loris lydekkerianus) in Karnataka, south India intermittently during November 2001–July 2004 and estimated their relative abundance via direct sightings. Two subspecies, Loris lydekkerianus lydekkerianus and L. l. malabaricus, with different morphological traits, occur in the eastern drier region and the western wet region of the state, respectively. The distribution of Loris lydekkerianus lydekkerianus is patchy in a small region in the southeast, which contradicts earlier reports of its abundance throughout the state. Loris lydekkerianus malabaricus occurs throughout the Western Ghats as a contiguous population. The encounter rates of Loris lydekkerianus lydekkerianus and L. l. malabaricus are 0.41 individuals/km and 0.21 individuals/km, respectively. Whereas several forest tracts in the distributional range of Loris lydekkerianus malabaricus are protected areas, no such area exists in the distributional range of L. l. lydekkerianus. Loris lydekkerianus faces serious challenges of conservation because it largely occurs in commercial plantations, which can be relatively unstable habitats as harvesting can take place at any time.

Polycystic nephropathy in slender lorises (Loris lydekkerianus)

In a colony of slender lorises, 20 deaths that occurred over a period of 11 years were investigated postmortem. Juvenile/adult polycystic nephropathy was observed in one newborn and 13 adult slender lorises. Although polycystic kidney disease (PKD) in humans and other animals is known to be inherited, it is not clear whether kidney alterations in slender lorises are genetically transmitted, stress related, or induced by microbiological influences.     

Observations of mating, birthing and parental behaviour in three subspecies of slender loris (Loris tardigradus and Loris lydekkerianus ) in India and Sri Lanka

Studies of the life history parameters of slender lorises in captivity have led to conflicting results regarding gestation length, birth seasonality, interspecies variation in litter size and the degree of parental care given to offspring. During the course of field studies of Loris lydekkerianus lydekkerianus, L. l. nordicus and L. tardigradus tardigradus, data were collected on these life history variables, as well as on behaviours relating to mating. All 3 taxa displayed courtship behaviour involving the pursuit of a female by multiple males. Mating corresponded closely with captive observations, with a period of prolonged single intromissions lasting 3-11 min. One gestation period of 163 days was calculated for L. l. lydekkerianus. Births for all 3 taxa were distributed throughout the year, and males were seen mating throughout the year. All 3 taxa gave birth to singletons and twins; no subspecific pattern in litter size was evident. Females carried infants for the first 4 weeks of life and were regularly attended by males, which groomed both the mother and her offspring. After infants had been parked, female L. l. lydekkerianus and L. l. nordicus rarely returned before dawn, though males visited and played with infants. Female L. t. tardigradus maintained proximity with their infants, whilst males were not observed in proximity to infants during the night. All 3 taxa slept in social groups. High-energy milk, in combination with male care, may aid in the potentially high reproductive output of 4 infants per year.     

Primate origins and the evolution of angiosperms

Traditionally, the morphological traits of primates were assumed to be adaptations to an arboreal way of life. However, Cartmill [1972] pointed out that a number of morphological traits characteristic of primates are not found in many other arboreal mammals. He contends that orbital convergence and grasping extremities indicate that the initial divergence of primates involved visual predation on insects in the lower canopy and undergrowth of the tropical forest. However, recent research on nocturnal primates does not support the visually-oriented predation theory. Although insects were most likely important components of the diets of the earliest euprimates, it is argued here that visual predation was not the major impetus for the evolution of the adaptive traits of primates. Recent paleobotanical research has yielded evidence that a major evolutionary event occurred during the Eocene, involving the angiosperms and their dispersal agents. As a result of long-term diffuse coevolutionary interactions with flowering plants, modern primates, bats, and plant-feeding birds all first arose around the Paleocene-Eocene boundary and became the major seed dispersers of modern tropical flora during the Eocene. Thus, it is suggested here that the multitude of resources available on the terminal branches of the newly evolved angiosperm, rain forest trees led to the morphological adaptations of primates of modern aspect.     

The Narrow Niche hypothesis: gray squirrels shed new light on primate origins

Current hypotheses for primate origins propose that nails and primate-like grasping hands and feet were important early adaptations for feeding in fine branches. Comparative research in this area has focused on instances of convergence in extant animals, showing that species with primate-like morphology feed predominantly from terminal branches. Little has been done to test whether animals without primate-like morphology engage in similar behavior. We tested the fine-branch niche hypothesis for primate origins by observing branch use in Eastern gray squirrels, Sciurus carolinensis, a species lacking primate grasping adaptations that has been understudied in the context of primate origins. We hypothesized that because gray squirrels lack primate-like grasping adaptations, they would avoid feeding and foraging in terminal branches. Instantaneous focal animal sampling was used to examine the locomotor and postural behaviors used while feeding and foraging. Our results demonstrate habitual and effective usage of terminal branches by gray squirrels while feeding and foraging, primarily on tree seeds (e.g., oak, maple, and elm). Discriminant function analysis indicates that gray squirrels feed and forage like primates, unlike some other tree squirrel species. Given the absence of primate-like features in gray squirrels, we suggest that although selection for fine-branch foraging may be a necessary condition for primate origins, it is not sufficient. We propose an alternative model of primate origins. The Narrow Niche hypothesis suggests that the primate morphological suite evolved not only from selection pressure for fine branch use, but also from a lack of engagement in other activities.     

Signal convergence in fruits: a result of selection by frugivores?

The Dispersal Syndrome hypothesis remains contentious, stating that apparently nonrandom associations of fruit characteristics result from selection by seed dispersers. We examine a key assumption under this hypothesis, i.e. that fruit traits can be used as reliable signals by frugivores. We first test this assumption by looking at whether fruit colour allows birds and primates to distinguish between fruits commonly dispersed by birds or primates. Second, we test whether the colours of fruits dispersed by primates are more contrasting to primates than the colours of bird‐dispersed fruits, expected if fruit colour is an adaptation to facilitate the detection by seed dispersers. Third, we test whether fruit colour has converged in unrelated plant species dispersed by similar frugivores. We use vision models based on peak sensitivities of birds’ and primates’ cone cells. We base our analyses on the visual systems of two types of birds (violet and ultraviolet based) and three types of primates (trichromatic primates from the Old and the New Worlds, and a dichromatic New World monkey). Using a Discriminant Function Analysis, we find that all frugivore groups can reliably discriminate between bird‐ and primate‐dispersed fruits. Fruit colour can be a reliable signal to different seed dispersers. However, the colours of primate‐dispersed fruits are less contrasting to primates than those of bird‐dispersed fruits. Fruit colour convergence in unrelated plants is independent of phylogeny and can be better explained by disperser type, which supports the hypothesis that frugivores are important in fruit evolution. We discuss adaptive and nonadaptive hypotheses that can potentially explain the pattern we found.     

Social behaviour of the slender Loris (Loris tardigradus lydekkerianus)

The social behaviour of the nocturnal prosimian Loris tardigradus lydekkerianus in its natural habitat was studied for 21 months in a scrub jungle in Dindigul, southern India. A total of 22834 scans were collected during 2656 hours of observation on identified and unidentified lorises. Social interactions were observed between individuals of all age-sex classes, both during the night and at dawn, when the animals met to sleep together. The majority of aggressive encounters between individuals occurred in territorial and mating contexts. Individuals also communicated with each other through chemical and vocal signals. Adults and sub-adults of both sexes were observed to immigrate into the study area, leading to social interactions with resident individuals.     

Slow Lorises (<Emphasis Type="Italic">Nycticebus</Emphasis> spp.) Really Are Slow: a Study of Food Passage Rates

The characteristics of food ingested by a primate affect its assimilation of energy by modulating food passage rate. In general, digestive time increases in folivorous primates and decreases in frugivorous primates when they are fed higher fiber diets but this relationship is understudied in exudativorous primates. We compared the food passage rate of five slow loris species. We studied 34 wild-caught slow lorises (15 Nycticebus coucang, 15 N. javanicus, and 4 N. menegensis) in an Indonesian rescue center and four captive-born slow lorises (2 N. bengalensis and 2 N. pygmaeus) in a UK institution. We fed the Indonesian subjects two different diets: a captive-type diet comprising fruits, vegetables, and insects and a wild-type diet formulated to be similar in nutrients to that consumed by slow lorises in the wild, consisting of gum, insects, vegetables, and nectar. We fed the UK subjects a diet of gum, vegetables, insects, and hard-boiled eggs. We formulated this diet to mimic the wild diet, with notably higher fiber fractions and lower soluble sugars than the previous diet. We measured two variables: the transit time (TT) and the mean retention time (MRT). We mixed 1 tsp. of glitter in bananas or gum as our markers and fed them to the slow lorises immediately before their main diet. We noted the date and time of feeding and of appearances of the marker in feces. We weighed food given and left over for each individual to calculate ingested foods and nutrients. We found that TTs were not affected by diet treatment but MRTs were significantly longer for all species fed the wild-type diet. Our results show that Nycticebus spp. have long MRTs for their body weight, and N. pygmdaeus may have the slowest MRT of all primates in relation to body mass. The digestive flexibility of exudativorous primates should allow them to maximize fermentation opportunities when they ingest more (appropriate) fiber by increasing the amount of time the fiber substrate stays in the large intestine. Exudativorous primates appear to have plastic digestive strategies that may be an adaptation to cope with relatively nutrient-poor staple food sources such as gum. The provision of gum in a captive setting may therefore provide benefits for gut health in slow lorises.     

Use of forest canopy by European red squirrelsSciurus vulgaris in Northern Greece: claws and the small branch niche

Moving and standing in trees impose multiple problems to arboreal mammals. Among them, the major ones are the negotiation of slender terminal branches and of large vertical supports. Both microhabitats are important as they have been linked alternatively to the evolutionary loss of claws in early primates. Therefore, rates of use of these different supports by claw-bearing arboreal mammals may offer insights to their actual significance in the adaptive evolution of early primates. In this context, canopy, tree crown, branch size, inclination, and texture use were recorded on four adult free ranging European red squirrelsSciurus vulgaris Linnaeus, 1758 in a mixed coniferous forest in northern Greece.S. vulgaris was mainly arboreal, exploiting the terminal branch zone, using frequently oblique and intermediately textured supports<5 cm and moderately large vertical branches. Furthermore, comparative data from other sciurid species and clawed primates showed positive correlations of small and horizontal support use, and negative ones of vertical support use to body mass. These findings show that keeled functional claws do not impede habitual use of slender branches and may not facilitate efficient climbing on large vertical trunks. These observations partly question the association between habitual use of the small branch niche and primate adaptations and lend support to alternative hypotheses, underscoring the importance of inquiring for more complex mechanisms that lead to the evolution of the unique set of primate morphological adaptations.     

The impact of plant secondary compounds on primate feeding behavior

The recent literature on plant secondary compounds and their influence on primate feeding behavior is reviewed. Many studies of nonhuman primates document the extreme selectivity that primates, particularly herbivorous species, demonstrate in their food choice. Until quite recently investigators interpreted this to mean that herbivorous primates were not food limited. This view has been challenged in the past 10 years by researchers concentrating on the primate–plant interaction. Chemical analyses have demonstrated that plant parts are of varying quality due to differences in nutrient and secondary compound content. The assumption that all leaves (or fruits, flowers, and insects) are potential foods of equal value to the primates eating them is refuted. The observed selectivity and preferences of primates for specific plant or insect species and parts are now viewed as strategies for dealing with the nutrient and secondary compound content variation in these foods.     

Reproduction in the slender loris (Loris tardigradus malabaricus)

A breeding colony of slender lorises (Loris tardigradus malabaricus) was studied to obtain data for comparison with other prosimian species, to contribute reproductive information for improving management of captive lorises, and to resolve some uncertainties in the literature regarding reproduction in the slender loris. At the Duke University Primate Center, a female slender loris reached sexual maturity at approximately ten months of age and conceived at one year of age. The length of the estrous cycle was 29–40 days, with copulation occurring over two consecutive days during estrus. Gestation length was 166–169 days. Litter size for each six births was one. Conception did not occur during an immediate post-partum estrus, but four months after birth, resulting in a 9 1/2-month interbirth interval. There was no evidence of reproductive seasonality. Lactation lasted between five and seven months. Reproductive rates of slender lorises are among the lowest of primates less than 500 g. Differences in reproductive parameters may exist between different subspecies of slender lorises.     

Extreme primates: Ecology and evolution of Asian lorises

Asia's slow and slender lorises (Nycticebus and Loris) are among nature's most extreme primates. Until recently, it was not understood why lorises have such huge forward‐facing eyes, strange steady climbing locomotion, tiny dependent babies, and a bite that potentially can kill a human! Indeed, early studies described them as slow, solitary, and boring. Twenty years of field research now indicate that lorises are among the most intriguing mammal species.