M. Teague O'Mara

Growth and the development of sexual size dimorphism in lorises and galagos

Three fundamental ontogenetic pathways lead to the development of size differences between males and females. Males and females may grow at the same rate for different durations (bimaturism), grow for the same duration at different rates, or grow at a mix of rate and duration differences. While patterns of growth and the development of adult body size are well established for many haplorhines, the extent to which rate and duration differences affect strepsirrhine growth trajectories remains unclear. Here, we present iterative piecewise regression models that describe the ontogeny of adult body mass for males and females of five lorisoid species (i.e., lorises and galagos) from the Duke Lemur Center. We test the hypotheses that, like most haplorhines, sexual size dimorphism (SSD) is a result of bimaturism, and males and females of monomorphic species grow at the same rate for a similar duration. We confirm that the galagos in this sample (Galago moholi and Otolemur garnettii) show significant SSD that is achieved through bimaturism. Unlike monomorphic lemurids, the lorises in this sample show a diversity of ontogenetic patterns. Loris tardigradus does follow a lemur-like trajectory to monomorphism but Nycticebuscoucang and Nycticebus pygmaeus achieve larger adult female body sizes through a mixture of rate and duration differences. We show that contrary to previous assumptions, there are patterns of both similarity and difference in growth trajectories of comparably sized lorises and galagos. Furthermore, when ontogenetic profiles of lorisoid and lemurid growth are compared, it is evident that lorisoids grow faster for a shorter period of time.

Social influences on the development of ringtailed lemur feeding ecology

As they grow, young individuals can use both social and individual learning strategies to develop speciestypical feeding ecology, and the utility of these strategies may vary phylogenetically and with environmental stability. Focused learning from mothers and other group members is critical in monkeys, with behaviours such as co-feeding playing strong roles in determining postweaning survival. While adult lemurs are capable of social learning, it is unknown how social information is incorporated during the development of feeding or what social learning strategies are used in this process. Here we evaluate the use of social learning behaviours and the potential for social learning in young ringtailed lemurs, Lemur catta, at the Beza Mahafaly Special Reserve, Madagascar. We show that infant and juvenile ringtailed lemurs use basic and generalized stimulus enhancement that occurs through behavioural synchrony with older nearest neighbours. More focused co-feeding occurred at low levels, and many of the social learning behaviours observed in the other social primate taxa were absent. High levels of individual exploration also contributed to learning, evidenced through high dietary diversity in juveniles relative to other group members. Our observations are consistent with the idea that simple social learning rules are responsible for the development of ecological complexity in many generalist vertebrate species, and that more complicated learning behaviours may not be necessary to learn complex and varied diets.

No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat

Bat immune systems may allow them to respond to zoonotic agents more efficiently than other mammals. As the first line of defence, the taxonomically conserved acute phase immune reaction of leucocytosis and fever is crucial for coping with infections, but it is unknown if this response is a key constituent to bat immunological success. We investigated the acute phase reaction to a standard lipopolysaccharide (LPS) challenge in Pallass mastiff bats (Molossus molossus). Challenged bats lost mass, but in contrast to other mammals showed no leucocytosis or fever. There also was no influence on body temperature reduction during torpor. When compared to recent genome-wide assays for constituent immune genes, this lack of a conserved fever response to LPS contributes to a clearer understanding of the innate immune system in bat species and of the coevolution of bats with a wide diversity of pathogens.

Tracking Post-Hibernation Behavior and Early Migration Does Not Reveal the Expected Sex-Differences in a ''Female-Migrating'' Bat

Long-distance migration is a rare phenomenon in European bats. Genetic analyses and banding studies show that females can cover distances of up to 1,600 km, whereas males are sedentary or migrate only short distances. The onset of this sex-biased migration is supposed to occur shortly after rousing from hibernation and when the females are already pregnant. We therefore predicted that the sexes are exposed to different energetic pressures in early spring, and this should be reflected in their behavior and physiology. We investigated this in one of the three Central European long-distance migrants, the common noctule (Nyctalus noctula) in Southern Germany recording the first individual partial migration tracks of this species. In contrast to our predictions, we found no difference between male and female home range size, activity, habitat use or diet. Males and females emerged from hibernation in similar body condition and mass increase rate was the same in males and females. We followed the first migration steps, up to 475 km, of radio-tagged individuals from an airplane. All females, as well as some of the males, migrated away from the wintering area in the same northeasterly direction. Sex differences in long-distance migratory behavior were confirmed through stable isotope analysis of hair, which showed greater variation in females than in males. We hypothesize that both sexes faced similarly good conditions after hibernation and fattened at maximum rates, thus showing no differences in their local behavior. Interesting results that warrant further investigation are the better initial condition of the females and the highly consistent direction of the first migratory step in this population as summering habitats of the common noctule occur at a broad range in Northern Europe. Only research focused on individual strategies will allow us to fully understand the migratory behavior of European bats.

Ecological Risk Aversion and Juvenile Ring-Tailed Lemur Feeding and Foraging

The extended primate juvenile period has been linked to interactions between feeding ecology and sociality. However, accumulating field data on juvenile primates suggest variation in the linkages between foraging efficiency, group foraging and social behaviour. In many non-human primates, juvenile ability (strength, coordination and motor skills) does not limit foraging success. If predicted limitations in feeding are not found in juvenile monkeys, it is possible that the gregarious strepsirrhines may show foraging patterns similar to those implicated in the evolution of a life history where long juvenile periods are advantageous. To test these behavioural predictions, I present a mixed longitudinal sample of observations on feeding and foraging behaviour from ring-tailed lemurs (Lemur catta) at the Bezà Mahafaly Special Reserve, Madagascar. Like several platyrrhine species, close proximity during foraging, low feeding efficiency and low dietary diversity are not typical of ring-tailed lemurs. The lack of ecological trade-offs in these species may indicate stronger common roles of sociality and social complexity in structuring the elongation of the primate juvenile period.

Cyclic bouts of extreme bradycardia counteract the high metabolism of frugivorous bats

Active flight requires the ability to efficiently fuel bursts of costly locomotion while maximizing energy conservation during non-flying times. We took a multi-faceted approach to estimate how fruit-eating bats (Uroderma bilobatum) manage a high-energy lifestyle fueled primarily by fig juice. Miniaturized heart rate telemetry shows that they use a novel, cyclic, bradycardic state that reduces daily energetic expenditure by 10% and counteracts heart rates as high as 900 bpm during flight. Uroderma bilobatum support flight with some of the fastest metabolic incorporation rates and dynamic circulating cortisol in vertebrates. These bats will exchange fat reserves within 24 hr, meaning that they must survive on the food of the day and are at daily risk of starvation. Energetic flexibly in U. bilobatum highlights the fundamental role of ecological pressures on integrative energetic networks and the still poorly understood energetic strategies of animals in the tropics.

Perceptual bias does not explain preference for prey call adornment in the frog-eating bat

Eavesdropping predators sometimes show preferences for certain prey signal variants, yet the ultimate and proximate reasons for such preferences are often unclear. The fringe-lipped bat, Trachops cirrhosus, eavesdrops on the advertisement calls of male túngara frogs, Physalaemus pustulosus, and shows a marked preference for complex (adorned) calls over simple (non-adorned) calls. We hypothesized that this preference stems from perceptual biases in the sensory and/or cognitive systems of T. cirrhosus. To test this hypothesis, we conducted a series of preference experiments in which we presented bats with various modified simple calls, each altered to possess one of the acoustic properties that distinguish complex calls from simple calls. We reasoned that if perceptual bias accounts for the bat’s preference for complex calls, then a novel stimulus with similar acoustic properties to the complex call should be attractive as well (i.e., the preference should be permissive). Except for weak evidence suggesting that the longer duration of complex calls could contribute to their greater attractiveness to T. cirrhosus, we did not find any indication that perceptual biases account for this eavesdropper preference. Instead, we suggest that T. cirrhosus developed their preference for call complexity because eavesdropping on complex calls provides greater fitness benefits than eavesdropping on simple calls, for example, because eavesdropping on complex calls may increase probability of prey capture and/or lead to more profitable food patches.

The development of sex differences in ring-tailed lemur feeding ecology

Sex differences in feeding ecology may develop in response to fluctuations in physiological costs to females over their reproductive cycles, or to sexual size dimorphism, or function to minimize feeding competition within a group via resource partitioning. For most mammal species, it is unknown how these factors contribute to sex differences in feeding, or how the development of males and females reflects these intraspecific feeding differences. We show changes in dietary composition, diversity, overlap, and foraging behavior throughout development in ring-tailed lemurs (Lemur catta) and test how the development of sex differences in feeding is related to female costs of reproduction and year-round resource partitioning. Sex differences in dietary composition were only present when females were lactating, but sex differences in other aspects of feeding, including dietary diversity, and relative time spent feeding and foraging, developed at or near the time of weaning. Sex difference in juveniles and subadults, when present, were similar to the differences found in adults. The low year-round dietary overlap and early differences in dietary diversity indicate that some resource partitioning may begin with young individuals and fluctuate throughout development. The major differences between males and females in dietary composition suggest that these larger changes in diet are closely tied to female reproductive state when females must shift their diet to meet energetic and nutritional requirements.

Determinants of spring migration departure decision in a bat

Migratory decisions in birds are closely tied to environmental cues and fat stores, but it remains unknown if the same variables trigger bat migration. To learn more about the rare phenomenon of bat migration, we studied departure decisions of female common noctules (Nyctalus noctula) in southern Germany. We did not find the fattening period that modulates departure decisions in birds. Female noctules departed after a regular evening foraging session, uniformly heading northeast. As the day of year increased, migratory decisions were based on the interactions among wind speed, wind direction and air pressure. As the migration season progressed, bats were likely to migrate on nights with higher air pressure and faster tail winds in the direction of travel, and also show high probability of migration on low-pressure nights with slow head winds. Common noctules thus monitor complex environmental conditions to find the optimal migration night.

Foraging and Roosting Behaviour of the Fringe-Lipped Bat, Trachops cirrhosus, on Barro Colorado Island, Panamá

The Neotropical fringe-lipped bat, Trachops cirrhosus, is a generalist predator that hunts frogs and insects by homing in on their mating calls. Although research has examined cognition and prey preferences of bats in captivity, little is known of the foraging or roosting behaviour of this species in the wild. We radio tracked six T. cirrhosus individuals on Barro Colorado Island, Panamá. Bat day roosts were all in hollow cashew trees, Anacardium excelsum, in mixed sex groups of three to five T. cirrhosus individuals, with frequent roost switching. Radio tracked individuals flew an average of 218 ± 227 m from their day roosts to 12.0 ± 10.17 ha foraging areas (50% utilization distribution [UD] kernels = areas where bats spent 50% of their time as estimated from a probability distribution). These 50% UD kernels were less than 10% of their average total range use, but larger than previously reported for T. cirrhosus. Radio tracked individuals overlapped in 50% UD kernel foraging areas by only 2.1 ± 5.9 % on average. Foraging behaviour consisted predominantly of short sally flights of less than one minute, indicating bats were likely perch hunting. Bats were more frequently in flight, and had longer flight durations, at the beginning of the night and just before dawn than throughout the rest of the night. These data provide insight into the foraging behaviour of T. cirrhosus in the wild, that is a species fast becoming a model system of cognition in captivity.