Joanna Fietz

Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat?

Abstract The fat-tailed dwarf lemur (Cheirogaleus medius; Cheirogaleidae) lives in the tropical forests of Madagascar. It is exceptional among primates, because this small nocturnal lemur hibernates during the dry season from the end of April until October. This field study was carried out to assess seasonal changes in body mass and behavioral traits (locomotor activity, feeding ecology) of C. medius that enable this species to accumulate large quantities of fat within weeks. Feeding observations of 36 radio-collared individuals were combined with a mark-recapture study in western Madagascar during the rainy seasons from 1995 to 1998. Pulp of fruit species not consumed, as well as fruit species eaten by C. medius was analyzed for lipid and sugar contents. Body mass changes of recaptured individuals revealed that C. medius may double its body mass within a few weeks. Most of the increase in body mass took place between March and April after infants had been weaned and directly before the onset of hibernation. Locomotor activity was significantly reduced during the period of body mass gain. During the entire study, fruits, nectar, and flowers of 34 different plant species comprised about 80% of the diet, supplemented by a seasonally varying intake of animal prey. Lipid contents of consumed fruits were comparatively low throughout the study period. No difference in lipid content was detectable between fruit species consumed and not consumed by C. medius. During prehibernation fattening, C. medius consumed mostly fruit species with a high sugar content, significantly higher than that of fruit species that were not consumed. The results suggest that a reduction in locomotor activity as well as a preference for fruit species with a high sugar content enable C. medius to deposit large quantities of fat in a few weeks.

MHC-associated mating strategies and the importance of overall genetic diversity in an obligate pair-living primate

Mate choice is one of the most important evolutionary mechanisms. Females can improve their fitness by selectively mating with certain males. We studied possible genetic benefits in the obligate pair-living fat-tailed dwarf lemur (Cheirogaleus medius) which maintains life-long pair bonds but has an extremely high rate of extra-pair paternity. Possible mechanisms of female mate choice were investigated by analyzing overall genetic variability (neutral microsatellite marker) as well as a marker of adaptive significance (major histocompatibility complex, MHC-DRB exon 2). As in human medical studies, MHC-alleles were grouped to MHC-supertypes based on similarities in their functional important antigen binding sites. The study indicated that females preferred males both as social and as genetic fathers for their offspring having a higher number of MHC-alleles and MHC-supertypes, a lower overlap with female’s MHC-supertypes as well as a higher genome wide heterozygosity than randomly assigned males. Mutual relatedness had no influence on mate choice. Females engaged in extra-pair mating shared a significant higher number of MHC-supertypes with their social partner than faithful females. As no genetic differences between extra-pair young (EPY) and intra-pair young (IPY) were found, females might engage in extra-pair mating to ‘correct’ for genetic incompatibility. Thus, we found evidence that mate choice is predicted in the first place by the ‘good-genes-as-heterozygosity hypothesis’ whereas the occurrence of extra-pair matings supports the ‘dissassortative mating hypothesis’. To the best of our knowledge this study represents the first investigation of the potential roles of MHC-genes and overall genetic diversity in mate choice and extra-pair partner selection in a natural, free-living population of non-human primates.

Influences of the feeding ecology on body mass and possible implications for reproduction in the edible dormouse (Glis glis)

The edible dormouse (Glis glis) is a small rodent and an obligate hibernator. Dormice undergo strong fluctuations of reproductive output during years that seem to be timed to coincide with future food supply. This behaviour enables them to avoid producing young that will starve with a high probability due to food shortage, and to increase their lifetime reproductive success. Aims of this study were to elucidate the extent to which feeding ecology in the edible dormouse has an impact on body mass and the fatty acid (FA) pattern of the white adipose tissue (WAT) before and after hibernation, which in turn might influence reproductive status in spring. Dormice show strong seasonal fluctuations of the body mass, which is reduced by one third during hibernation. Body mass and its changes depend on autumnal food availability as well as on the dietary FA pattern. During the pre-hibernation fattening period, dormice eat lipid rich food with a high content of linoleic acid. During hibernation, linoleic acid content is slightly but significantly reduced and body mass loss during winter is negatively correlated with the pre-hibernation linoleic acid content in the WAT. No relation between reproductive status and body mass, body condition or the FAs pattern of the WAT could be detected. However, in a year of high reproduction, dormice commence the shift to seed eating earlier than in a year of low reproduction. These seeds could be either a predictor for future food supply in autumn, or represent a high-energy food compensating high energetic costs of sexual activity in male edible dormice.

Energetic constraints on sexual activity in the male edible dormouse (Glis glis)

The aim of this study was to examine to what extent reproductive activity in male edible dormice (Glis glis) might be energetically constrained. Demographic data, morphometric data, and oral body temperature (Tor) measurements were collected in two study areas between 1993 and 2002 in southwest Germany and combined with subcutaneous body temperature (Tsc) registrations of captive dormice. Tsc measurements were collected directly after emergence from hibernation (June) until the end of the mating season (July). Wild edible dormice showed strong fluctuations in their reproductive output between years. Not all males were sexually active each year and the number of litters born was positively correlated with the number of sexually active males, which suggests that sexual activity in males is constrained and in turn limits reproductive success. A comparison of the Tor of sexually quiescent and active males revealed that sexually quiescent males had significantly lower Tor (median: 28.8°C; 25/75% quartiles: 16.4/31.0; n=31) than sexually active males (median: 34.2°C; 25/75% quartiles: 32.0/35.6; n=156). Body condition of sexually active and quiescent males was not different after emergence from hibernation. However, sexually active males showed a significant reduction in their body condition between June and July, the time of mating, while body condition of sexually quiescent males remained constant. Continuous Tsc registrations in captive sexually active male dormice showed strong circadian Tsc fluctuations. Even though daily torpor bouts with Tsc below 20°C occurred in these males, most of the time Tsc fluctuated above 30°C, which is known as the critical body temperature threshold above which testes maturation can take place in this species. These results demonstrate that male dormice incur high costs due to sexual activity and that thermoregulation is determined by a trade-off between energetic savings and reproductive activity.

Costs and Potential Benefits of Parental Care in the Nocturnal Fat-Tailed Dwarf Lemur (Cheirogaleus medius)

Parental care should evolve only if fitness benefits exceed fitness costs. In Cheirogaleus medius, a small nocturnal lemur of western Madagascar, we found the peculiar situation of considerable parental care by both sexes, combined with an extremely high rate of extra-pair young (EPY). In this paper, we try to elucidate the costs and benefits of parental care in C. medius, and we discuss hypotheses as to why males might actively participate in raising young, especially with regard to the high rate of EPY. The study was carried out in the dry deciduous forest of western Madagascar between 1996 and 2001. The most important components of parental care in C. medius are babysitting and guarding of the young. Observational data suggest that thermoregulatory demands during the first days after birth and defence from predators may be the driving factors selecting for this infant care behaviour. The reproducing individuals of both sexes incur considerable energetic costs by this behaviour, resulting in reduced fat stores and body condition in comparison to non-reproducing individuals. The reason why males also care for EPY remains elusive. We propose that males might not be able to detect individual relatedness and that they would jeopardise the survival of their own young if they gave no parental care. Alternatively, they might gain advantages other than direct fitness from raising EPY, for example if caring behaviour increases their chances in further reproduction, or if EPY are fathered by close kin.

White adipose tissue composition in the free-ranging fat-tailed dwarf lemur (Cheirogaleus medius; Primates), a tropical hibernator

Abstract. In temperate species, hibernation is enhanced by high levels of essential fatty acids in white adipose tissue. Essential fatty acids cannot be synthesized by mammals, thus nutritional ecology should play a key role in physiological adaptations to hibernation. Tropical hibernators are exposed to different physiological demands than hibernators in temperate regions and are expected to be subject to different constraints. The aims of this study were to assess whether or not the tropical hibernator Cheirogaleus medius shows biochemical changes in its white adipose tissue before and during hibernation. A capture–recapture study was combined with feeding observations in western Madagascar. Before and after hibernation, 77 samples of white adipose tissue from 57 individuals of C. medius, as well as dietary items eaten during pre-hibernation fattening, were sampled and analyzed for their fatty acid composition. In contrast to temperate hibernators, C. medius exhibits extremely low essential fatty acid concentrations in its white adipose tissue (2.5%) prior to hibernation. The fatty acid pattern of the white adipose tissue did not change during pre-hibernation fattening and did not reflect dietary fatty acid composition. During hibernation, fat stores showed only minor but significant compositional changes. Because of its prevalence, the main fuel during hibernation was the monounsaturated oleic acid, which seemed to be preferentially synthesized from dietary carbohydrates. Results suggest that essential fatty acids do not represent an ecological limitation for hibernation in the tropics, at least not in the fat-tailed dwarf lemur.

Functional associations of similar MHC alleles and shared parasite species in two sympatric lemurs

Several recent studies of animals in their natural surroundings found evidence for effects of certain major histocompatibility complex (MHC) immune gene alleles on the parasite load. However, in multi-infected individuals the particular selection pressure exerted by specific parasites has rarely been explored. In this study we took advantage of the parasitological and genetic data of two previously investigated Malagasy lemur species (Cheirogaleus medius and Microcebus murinus). We investigated whether the two sympatric and ecologically similar primates are infected by similar parasite species and explored if certain parasites are associated with particular MHC alleles. Our study revealed that most of the parasite egg morphotypes were found in both hosts. In each lemur species we identified one MHC allele which was positively associated with Ascaris-infection. Interestingly, these MHC alleles were very similar to each other but differed from all other investigated MHC alleles in an amino acid substitution in a putative functional important antigen binding site. Thus, our study gives first intriguing evidence for a direct connection between certain antigen binding sites of MHC molecules with a particular parasite in two wild primate populations. This may indicate that indeed certain parasites exert direct selective pressure on the MHC of wild living hosts.

Genetic consequences of forest fragmentation for a highly specialized arboreal mammal--the edible dormouse.

Habitat loss and fragmentation represent the most serious extinction threats for many species and have been demonstrated to be especially detrimental for mammals. Particularly, highly specialized species with low dispersal abilities will encounter a high risk of extinction in fragmented landscapes. Here we studied the edible dormouse (Glis glis), a small arboreal mammal that is distributed throughout Central Europe, where forests are mostly fragmented at different spatial scales. The aim of this study was to investigate the effect of habitat fragmentation on genetic population structures using the example of edible dormouse populations inhabiting forest fragments in south western Germany. We genotyped 380 adult individuals captured between 2001 and 2009 in four different forest fragments and one large continuous forest using 14 species-specific microsatellites. We hypothesised, that populations in small forest patches have a lower genetic diversity and are more isolated compared to populations living in continuous forests. In accordance with our expectations we found that dormice inhabiting forest fragments were isolated from each other. Furthermore, their genetic population structure was more unstable over the study period than in the large continuous forest. Even though we could not detect lower genetic variability within individuals inhabiting forest fragments, strong genetic isolation and an overall high risk to mate with close relatives might be precursors to a reduced genetic variability and the onset of inbreeding depression. Results of this study highlight that connectivity among habitat fragments can already be strongly hampered before genetic erosion within small and isolated populations becomes evident.

Ways to measure body temperature in the field.

Body temperature (Tb) represents one of the key parameters in ecophysiological studies with focus on energy saving strategies. In this study we therefore comparatively evaluated the usefulness of two types of temperature-sensitive passive transponders (LifeChips and IPTT-300) and one data logger (iButton, DS1922L) mounted onto a collar to measure Tb in the field. First we tested the accuracy of all three devices in a water bath with water temperature ranging from 0 to 40°C. Second, we evaluated the usefulness of the LifeChips and the modified iButtons for measuring Tb of small heterothermic mammals under field conditions. For this work we subcutaneously implanted 14 male edible dormice (Glis glis) with transponders, and equipped another 14 males with data loggers to simultaneously record Tb and oxygen consumption with a portable oxygen analyzer (Oxbox). In one individual we recorded Tb with both devices and analyzed recorded Tb patterns. LifeChips are able to measure temperature within the smallest range from 25 to 40°C with an accuracy of 0.07±0.12°C. IPTT-300 transponders measured temperature between 10 and 40°C, but accuracy decreased considerably at values below 30°C, with maximal deviations of nearly 7°C. An individual calibration of each transponder is therefore needed, before using it at low Tbs. The accuracy of the data logger was comparatively good (0.12±0.25°C) and stable over the whole temperature range tested (0-40°C). In all three devices, the repeatability of measurements was high. LifeChip transponders as well as modified iButtons measured Tb reliably under field conditions. Simultaneous Tb-recordings in one edible dormouse with an implanted LifeChip and a collar-mounted iButton revealed that values of both measurements were closely correlated. Taken together, we conclude that implanted temperature-sensitive transponders represent an appropriate and largely non-invasive method to measure Tb also under field conditions.

Selection of food and ranging behaviour in a sexually monomorphic folivorous lemur: Lepilemur ruficaudatus

Monomorphic lemurs of Madagascar allow us to investigate whether there are behavioural mechanisms that compensate for sex-specific differences in the costs of maintenance and reproduction in arboreal primates. Food selection of the pair-living Lepilemur ruficaudatus was studied in relation to food chemistry, and travel distances were measured as possible indications of differential investment in ranging activities (possibly related to the defence of territories and/or mating opportunities). Fourteen females and 14 males were radio-tracked for a total of 365 half-nights (from dusk to midnight or from midnight to dawn) at different times of the year (birth, lactation and weaning, pre-mating, post-mating). When based on monthly means, the two sexes did not differ in nightly travel distances. Food selection of females and males did not differ in relation to the chemical composition of leaves, but fruits consumed by females had lower fibre contents than fruits consumed by males. Even though other behavioural data are fragmentary, little evidence exists for behavioural mechanisms in L. ruficaudatus to compensate for the different energetic costs of females and males.