Melanie Dammhahn

Comparative Feeding Ecology of Sympatric Microcebus berthae and M. murinus

Most Malagasy primate communities harbor a diverse assemblage of omnivorous species. The mechanisms allowing the coexistence of closely related species are poorly understood, partly because only preliminary data on the feeding ecology of most species are available. We provide an exemplary feeding ecology data set to illuminate coexistence mechanisms between sympatric gray and Madame Berthe’s mouse lemurs (Microcebus murinus, M. berthae). We studied their feeding ecology in Kirindy Forest/CFPF, a highly seasonal dry deciduous forest in western Madagascar. Between August 2002 and December 2007, we regularly (re-)captured, marked, and radiotracked females of both species. A combination of direct behavioral observations and fecal analyses revealed that both Microcebus species used fruit, arthropods, gum, insect secretions, and small vertebrates as food sources. However, Microcebus berthae and M. murinus differed in both composition and seasonal variation of their diets. Whereas the diet of Microcebus murinus varied seasonally and was generally more diverse, M. berthae relied mainly on insect secretions supplemented by animal matter. The differences were also reflected in a very narrow feeding niche of Microcebus berthae and a comparatively broad feeding niche of M. murinus. Resource use patterns of Madame Berthe’s and more so of opportunistic gray mouse lemurs broadly followed resource availability within the strongly seasonal dry forest. Feeding niche overlap between the 2 sympatric species was high, indicating that food resource usage patterns did not reflect niche partitioning, but can instead be explained by constraints due to food availability.

Are personality differences in a small iteroparous mammal maintained by a life-history trade-off?

Despite increasing interest, animal personality is still a puzzling phenomenon. Several theoretical models have been proposed to explain intraindividual consistency and interindividual variation in behaviour, which have been primarily supported by qualitative data and simulations. Using an empirical approach, I tested predictions of one main life-history hypothesis, which posits that consistent individual differences in behaviour are favoured by a trade-off between current and future reproduction. Data on life-history were collected for individuals of a natural population of grey mouse lemurs (Microcebus murinus). Using open-field and novel-object tests, I quantified variation in activity, exploration and boldness for 117 individuals over 3 years. I found systematic variation in boldness between individuals of different residual reproductive value. Young males with low current but high expected future fitness were less bold than older males with high current fecundity, and males might increase in boldness with age. Females have low variation in assets and in boldness with age. Body condition was not related to boldness and only explained marginal variation in exploration. Overall, these data indicate that a trade-off between current and future reproduction might maintain personality variation in mouse lemurs, and thus provide empirical support of this life-history trade-off hypothesis.

Is risk taking during foraging a personality trait? A field test for cross-context consistency in boldness

During foraging, animals have to balance the risk of predation with the energy gain. The amount of risk animals take for a given resource depends on their energy budget but is expected also to vary between individuals of different personality types. We tested whether individuals of free-ranging grey mouse lemurs, Microcebus murinus, forage risk-sensitively and are consistent in their risk-taking behaviour. Furthermore, we tested whether boldness towards a novel object predicts risk taking in a foraging task. In a field experiment, we simulated low and high predation risk at artificial feeding sites. During focal platform observations, we quantified behaviours related to exploration and feeding for 36 individuals. Furthermore, we used a novel object test to quantify variation in boldness for 22 of these individuals. As predicted, grey mouse lemurs foraged risk-sensitively indicated by longer latencies to enter a feeding platform and to start feeding as well as by relatively longer feeding time compared to nonfeeding in high-risk situations. Individual differences in risk taking were repeatable and repeatability increased with increasing risk. Individual plasticity was higher for low-risk individuals providing field evidence for coping styles. There was no relationship between individual body condition and risk-taking behaviour. Finally, boldness measured in a novel object test was correlated with risk taking in a foraging task, providing a rare ecological validation for this personality trait. These results suggest that intrinsic individual differences in boldness need to be considered as an important source of variation when testing predictions of risk-sensitive foraging using optimality approaches.

Small-scale coexistence of two mouse lemur species (Microcebus berthae and M. murinus) within a homogeneous competitive environment

Understanding the co-occurrence of ecologically similar species remains a puzzling issue in community ecology. The species-rich mouse lemurs (Microcebus spec.) are distributed over nearly all remaining forest areas of Madagascar with a high variability in species distribution patterns. Locally, many congeneric species pairs seem to co-occur, but only little detailed information on spatial patterns is available. Here, we present the results of an intensive capture–mark–recapture study of sympatric Microcebus berthae and M. murinus populations that revealed small-scale mutual spatial exclusion. Nearest neighbour analysis indicated a spatial aggregation in Microcebus murinus but not in M. berthae. Although the diet of both species differed in proportions of food categories, they used the same food sources and had high feeding niche overlap. Also, forest structure related to the spatial distribution of main food sources did not explain spatial segregation because parts used by each species exclusively did not differ in density of trees, dead wood and lianas. We propose that life history trade-offs that result in species aggregation and a relative increase in the strength of intra-specific over inter-specific competition best explain the observed pattern of co-occurrence of ecologically similar congeneric Microcebus species.

Social System of Microcebus berthae, the World’s Smallest Primate

Our goal was to provide a first characterization of the social system of pygmy mouse lemurs (Microcebus berthae), the world’s smallest primate species. During a 4-mo field study of 12 females and 27 males, we combined capture-recapture and morphometric data with detailed behavioral observations of individually marked subjects and genetic paternity analyses of a population in Kirindy Forest, western Madagascar. We describe the social organization of Microcebus berthae as a solitary forager living in an individualized neighborhood system characterized by extensive intra- and intersexual home range overlap of adult individuals within a male-biased population. Male and female pygmy mouse lemurs inhabited home ranges (males: 4.9 ha; females: 2.5 ha) that are more than twice as large as those of sympatric Microcebus murinus. On average, pygmy mouse lemurs of both sexes spent about half of the days sleeping alone. Preliminary analysis of genetic population structure suggests female philopatry and male dispersal. Sleeping associations of variable composition that consisted not preferentially of close relatives and proximity during part of the nightly activity contributed together with regular social interactions to the maintenance of a social network. The spatial distribution pattern of adult males and females, the absence of sexual size dimorphism, relatively large male testicular volume and moderate female estrous synchrony suggest a promiscuous mating system with a high potential for scramble competition. In general, there are many similarities between the social system of Microcebus berthae and those of other Microcebus spp. However, striking differences with sympatric gray mouse lemurs (Microcebus murinus) in female home range size, dispersion and sleeping behavior indicate the existence of species-specific socioecological adaptations in closely related species occupying very similar ecological niches.

Scramble or Contest Competition Over Food in Solitarily Foraging Mouse Lemurs (Microcebus spp.): New Insights From Stable Isotopes

The relationships between resource distribution, type of competition, and consequences for social organization have been formalized in the socioecological model (SEM) which predicts that ecological factors are the main determinants of female distribution. We tested this basic prediction in two solitary primates (Microcebus berthae and M. murinus) which differ in female association patterns. Using stable nitrogen and carbon isotope data of hair samples and food sources we quantified inter-specific differences in diet. delta(13)C in M. berthae reflected a diet composed mainly of insect secretions. Higher within-species as well as seasonal variation in delta(13)C of M. murinus indicated a wider trophic niche including plant and animal source food. Constantly elevated delta(15)N in M. murinus most likely reflected extended torpor during the lean season. This energy-saving strategy together with a wider, more opportunistic feeding niche might reduce female competition in this species, facilitating smaller female ranges, and a higher association potential. In contrast, delta(15)N fluctuated seasonally in M. berthae, most likely indicating varying amounts of arthropod food in the diet. Intense scramble competition over small and seasonally limited resources might lead to female spatial avoidance and a reduced association potential in M. berthae. Thus, differences in female association patterns between these two solitary foragers are due to different types of competition and overall intensities of intra-specific competition.

Senescence or selective disappearance? Age trajectories of body mass in wild and captive populations of a small-bodied primate

Classic theories of ageing consider extrinsic mortality (EM) a major factor in shaping longevity and ageing, yet most studies of functional ageing focus on species with low EM. This bias may cause overestimation of the influence of senescent declines in performance over condition-dependent mortality on demographic processes across taxa. To simultaneously investigate the roles of functional senescence (FS) and intrinsic, extrinsic and condition-dependent mortality in a species with a high predation risk in nature, we compared age trajectories of body mass (BM) in wild and captive grey mouse lemurs (Microcebus murinus) using longitudinal data (853 individuals followed through adulthood). We found evidence of non-random mortality in both settings. In captivity, the oldest animals showed senescence in their ability to regain lost BM, whereas no evidence of FS was found in the wild. Overall, captive animals lived longer, but a reversed sex bias in lifespan was observed between wild and captive populations. We suggest that even moderately condition-dependent EM may lead to negligible FS in the wild. While high EM may act to reduce the average lifespan, this evolutionary process may be counteracted by the increased fitness of the long-lived, high-quality individuals.

Females go where the food is: does the socio-ecological model explain variation in social organisation of solitary foragers?

The socio-ecological model (SEM) links ecological factors with characteristics of social systems and allows predictions about the relationships between resource distribution, type of competition and social organisation. It has been mainly applied to group-living species but ought to explain variation in social organisation of solitary species as well. The aim of this study was to test basic predictions of the SEM in two solitary primates, which differ in two characteristics of female association patterns: (1) spatial ranging and (2) sleeping associations. Beginning in August 2002, we regularly (re-)captured and marked individuals of sympatric populations of Madame Berthes and grey mouse lemurs (Microcebus berthae, Microcebus murinus) in Kirindy Forest (Madagascar). We recorded data on spatial patterns, feeding and social behaviour by means of direct observation of radio-collared females. The major food sources of M. berthae occurred in small dispersed patches leading to strong within-group scramble competition and over-dispersed females with a low potential for female associations. In contrast, M. murinus additionally used patchily distributed, high-quality (large) resources facilitating within-group contest competition. The combined influence of less strong within-group scramble and contest as well as between-group contest over non-food resources allowed females of this species to cluster in space. Additionally, we experimentally manipulated the spatial distribution of food sources and found that females adjusted their spatial patterns to food resource distribution. Thus, our results support basic predictions of the SEM and demonstrated that it can also explain variation in social organisation of solitary foragers.

Individual flexibility in energy saving: body size and condition constrain torpor use

Summary Phenotypic flexibility is a major mechanism in compensating climate-driven changes in resource availability. Heterotherms can use daily torpor to overcome resource shortages and adverse environmental conditions. The expression of this adaptive energy-saving strategy varies among individuals, but the factors constraining individual flexibility remain largely unknown. As energy availability depends on individual stores and/or on the ability to acquire food, the propensity and flexibility in torpor use are expected to be constrained by body condition and/or size, respectively. The aim of this study was to test whether the dependency of torpor depth on air temperature was constrained by body condition and/or body size in a small heterothermic primate, the grey mouse lemur (Microcebus murinus). During the onset of the dry season, we monitored air temperature as well as skin temperatures of 14 free-ranging individuals (12 females, two males) of known body mass and size. Unexpectedly, torpor depth depended as much on air temperature as on body condition and size. Fatter, or larger, mouse lemurs underwent deeper torpor than smaller, or leaner, ones. Individual reaction norms of torpor depth to air temperature also revealed that the propensity to undergo deep torpor and the flexibility in torpor depth were enhanced by large body size and high body condition, whereas small, lean individuals remained normothermic. Our study illustrates that alternative physiological strategies to overcome temperature constraints co-occur in a population, with body size and condition being key determinants of the energy conservation strategy that an individual can launch.

Spatial memory in the grey mouse lemur (Microcebus murinus)

Wild animals face the challenge of locating feeding sites distributed across broad spatial and temporal scales. Spatial memory allows animals to find a goal, such as a productive feeding patch, even when there are no goal-specific sensory cues available. Because there is little experimental information on learning and memory capabilities in free-ranging primates, the aim of this study was to test whether grey mouse lemurs (Microcebus murinus), as short-term dietary specialists, rely on spatial memory in relocating productive feeding sites. In addition, we asked what kind of spatial representation might underlie their orientation in their natural environment. Using an experimental approach, we set eight radio-collared grey mouse lemurs a memory task by confronting them with two different spatial patterns of baited and non-baited artificial feeding stations under exclusion of sensory cues. Positional data were recorded by focal animal observations within a grid system of small foot trails. A change in the baiting pattern revealed that grey mouse lemurs primarily used spatial cues to relocate baited feeding stations and that they were able to rapidly learn a new spatial arrangement. Spatially concentrated, non-random movements revealed preliminary evidence for a route-based restriction in mouse lemur space; during a subsequent release experiment, however, we found high travel efficiency in directed movements. We therefore propose that mouse lemur spatial memory is based on some kind of mental representation that is more detailed than a route-based network map.