ABSTRACT
Seasonal tropical environments are among those regions that are the most affected by shifts in temperature and rainfall regimes under climate change, with potentially severe consequences for wildlife population persistence. This persistence is ultimately determined by complex demographic responses to multiple climatic drivers, yet these complexities have been little explored in tropical mammals. We use long-term, individual-based demographic data (1994 to 2020) from a short-lived primate in western Madagascar, the gray mouse lemur (Microcebus murinus), to investigate the demographic drivers of population persistence under observed shifts in seasonal temperature and rainfall. While rainfall during the wet season has been declining over the years, dry season temperatures have been increasing, with these trends projected to continue. These environmental changes resulted in lower survival and higher recruitment rates over time for gray mouse lemurs. Although the contrasting changes have prevented the study population from collapsing, the resulting increase in life-history speed has destabilized an otherwise stable population. Population projections under more recent rainfall and temperature levels predict an increase in population fluctuations and a corresponding increase in the extinction risk over the next five decades. Our analyses show that a relatively short-lived mammal with high reproductive output, representing a life history that is expected to closely track changes in its environment, can nonetheless be threatened by climate change.
Subject(s)
Cheirogaleidae , Climate Change , Animals , Humans , Population Dynamics , Animals, Wild , Temperature , Mammals , Seasons , Cheirogaleidae/physiologyABSTRACT
Emotions are omnipresent in many animals' lives. It is a complex concept that encompasses physiological, subjective, behavioural and cognitive aspects. While the complex relationship between emotion and cognition has been well studied in humans and in some nonhuman primates, it remains rather unexplored for other nonhuman primate species, such as lemurs. In our study, we evaluated the performance of N = 48 grey mouse lemurs (Microcebus murinus) in a discrimination learning task using visual emotional stimuli. We tested whether the type of visual stimulus (positive, negative or neutral) influenced the cognitive performance of mouse lemurs. Individuals had to learn to discriminate between two platforms according to the associated visual stimuli and to jump to the target platform (leading to a reward). Our main finding was that emotional stimuli, whether positive or negative in valence, impaired cognitive performance when used as a target. Specifically, the lowest success rate occurred when the target was associated with the emotional stimuli, and the highest success rate occurred when it was associated with neutral stimuli. Our results show a similar pattern to that found in other primate species and support the adaptive role of emotion. Our results also support that individual differences could be a factor impacting the relation between emotion and cognition. This study is the first to explore how emotions interfere with the cognitive abilities of a lemur species and highlights the importance of acknowledging emotion in mouse lemurs as well as studying the emotion-cognition interaction in a wider range of primate species.
Subject(s)
Cheirogaleidae , Cognition , Discrimination Learning , Emotions , Animals , Cheirogaleidae/physiology , Cheirogaleidae/psychology , Male , Female , Photic StimulationABSTRACT
The physiological mechanisms of responses to stressors are at the core of ecophysiological studies that examine the limits of an organism's flexibility. Interindividual variability in these physiological responses can be particularly important and lead to differences in the stress response among population groups, which can affect population dynamics. Some observations of intersexual differences in heterothermy raise the question of whether there is a difference in energy management between the sexes. In this study, we assessed male and female differences in mouse lemurs (Microcebus murinus), a highly seasonal malagasy primate, by measuring their physiological flexibility in response to caloric restriction and examining the subsequent impact on reproductive success. Using complementary methods aiming to describe large-scale and daily variations in body temperature throughout a 6-month winter-like short-day (SD) period, we monitored 12 males and 12 females, applying chronic 40% caloric restriction (CR) to 6 individuals in each group. We found variations in Tb modulation throughout the SD period and in response to caloric treatment that depended on sex, as females, regardless of food restriction, and CR males, only, entered deep torpor. The use of deeper torpor, however, did not translate into a lower loss of body mass in females and did not affect reproductive success. Captive conditions may have buffered the depth of torpor and minimised the positive effects of torpor on energy savings. However, the significant sex differences in heterothermy we observed may point to physiological benefits other than preservation of energy reserves.
Subject(s)
Caloric Restriction , Cheirogaleidae , Energy Metabolism , Seasons , Animals , Female , Male , Cheirogaleidae/physiology , Torpor/physiology , Sex Characteristics , Body Temperature , Reproduction , Body Temperature RegulationABSTRACT
Madagascar is home to many threatened and endemic primate species, yet this island has seen dramatic declines in lemur habitat due to forest loss. This forest loss has resulted in an increasingly fragmented forest landscape, with fragments isolated from each other by grasslands (i.e., matrix). The grassland matrix is not entirely homogeneous containing matrix elements such as isolated trees and shrubs and linear features such as drainage lines. Because most lemurs are predominantly arboreal, they may preferentially use matrix elements to facilitate dispersal between fragments for access to mates or reduce feeding competition, allowing gene flow between fragments of habitat. Therefore, it is important to understand to what degree they use the matrix. We investigated matrix use in two mouse lemurs, the grey mouse lemur (Microcebus murinus) and the golden-brown mouse lemur (Microcebus ravelobensis) in a fragmented landscape in northwest Madagascar. We tested the predictions that: (1) lemurs use matrix less often than forest fragments, (2) if they use the matrix, then they will preferentially use matrix elements compared to grassland, and (3) M. murinus will disperse into the matrix further than M. ravelobensis. In 2011, we visually surveyed line transects in four areas containing matrix elements and four adjacent forest fragments during nocturnal walks. In 2017, we set up traplines in four areas of the matrix containing matrix elements, three areas that were grassland, and six traplines in adjacent fragments. We compared the relative abundance of mouse lemurs in matrix transects to fragmented forest transects, and the relative abundance of captured lemurs in matrix elements, grassland, and fragment traplines. We found that encounter rates of mouse lemurs did not significantly differ between the matrix and fragmented forest transects or traplines. Our sample size was too low to determine if the mean distance from the forest was greater for either Microcebus spp. Our study highlights that mouse lemurs do use matrix elements and there may be interspecific differences in use. Further research is needed to confirm species-specific matrix use, why mouse lemurs use matrix, and how much matrix elements facilitate movement for each species in fragmented landscapes.
Subject(s)
Cheirogaleidae/physiology , Ecosystem , Animals , Behavior, Animal , Forests , Grassland , MadagascarABSTRACT
The biological clock expresses circadian rhythms, whose endogenous period (tau) is close to 24 h. Daily resetting of the circadian clock to the 24 h natural photoperiod might induce marginal costs that would accumulate over time and forward affect fitness. It was proposed as the circadian resonance theory. For the first time, we aimed to evaluate these physiological and cognitive costs that would partially explain the mechanisms of the circadian resonance hypothesis. We evaluated the potential costs of imposing a 26 h photoperiodic regimen compared to the classical 24 h entrainment measuring several physiological and cognitive parameters (body temperature, energetic expenditure, oxidative stress, cognitive performances) in males of a non-human primate (Microcebus murinus), a nocturnal species whose endogenous period is about 23.5 h. We found significant higher resting body temperature and energy expenditure and lower cognitive performances when the photoperiodic cycle length was 26 h. Together these results suggest that a great deviation of external cycles from tau leads to daily greater energetic expenditure, and lower cognitive capacities. To our knowledge, this study is the first to highlight potential mechanisms of circadian resonance theory.
Subject(s)
Cheirogaleidae/physiology , Circadian Rhythm , Animals , Body Temperature , Circadian Clocks , Cognition , Male , Motor Activity , Photoperiod , VibrationABSTRACT
Solitary species often employ chemocommunication to facilitate mate localization. In the solitarily foraging, nocturnal mouse lemurs (Microcebus spp.), females advertise their short period of estrus acoustically and by increased scent marking, whereas males search widely for receptive females. Both sexes can be trained by operant conditioning to discriminate conspecific from heterospecific urine scent. However, it is not known, if males during and outside the reproductive season show different spontaneous interest in conspecific female urine, and if urine from estrous females elicits a higher investigation response than that from diestrous females. We established a spontaneous discrimination paradigm and quantified olfactory investigation responses of 21 captive male mouse lemurs of M. lehilahytsara and M. murinus when presenting 1 conspecific and 1 heterospecific female urine odor sample simultaneously. Overall, M. murinus investigated stimuli significantly longer than M. lehilahytsara. Moreover, males of M. murinus showed significantly longer olfactory investigation at conspecific urine samples during but not outside the reproductive season. This indicates that female urinary cues are spontaneously discriminated by male M. murinus and that this discrimination is more relevant during the reproductive season. However, males of both species did not show different responses toward urine samples from estrous versus diestrous females. Finally, male age did not correlate with the overall duration of olfactory investigation, and investigation levels were similar when testing with fresh or frozen urine samples. In conclusion, this new spontaneous discrimination paradigm provides a useful additional tool to study olfactory communication of nocturnal primates from the receiver's perspective.
Subject(s)
Cheirogaleidae/physiology , Smell/physiology , Animals , Conditioning, Operant , Estrus , Female , Male , Seasons , Sexual Behavior, Animal , Species SpecificityABSTRACT
The environment of juvenile primates is very challenging. They have to forage and move on the same substrates as adults do and escape the same predators, despite their immature state. In this study, we explore the developmental strategies that may provide effective locomotor abilities early in life. This could provide new insights into the selective pressures acting on juvenile primates and into evolution of primate locomotion. We conducted an ontogenetic study of 36 arboreal gray mouse lemurs from birth to adulthood (6 months of age). The investigated parameters were, for both limbs, (1) grasping behavior during locomotion (i.e., grip postures), (2) grasping performance (i.e., pull strength), and (3) motor coordination (i.e., rotarod test). Our results show that 8-day-old babies are able to climb substrates of various slopes and diameters outside of their nest. Although juveniles cannot successfully complete a motor coordination test before 30 days of age, young individuals display relative pull strengths that are very high or even on par with adults, guaranteeing stability on narrow substrates. These powerful grasps highlight the importance of the grasping function for these juveniles that are not carried and move independently on arboreal substrates shortly after their first week of life. Moreover, the pedal grasping provides a secure grasp on all substrates across ontogeny; however, manual secure grasps decrease during development, being highly used only shortly after birth on vertical and narrow substrates. These results first suggest different functional roles of the hands and feet, with the hind limbs ensuring body balance on the substrates, freeing the upper limbs for manipulation. They further show vertical and narrow branches to be especially challenging, requiring strong grasps, which suggests that they may drive the evolution of strong grasping abilities in primates.
Subject(s)
Cheirogaleidae/physiology , Hand Strength , Locomotion , Rotarod Performance Test/veterinary , Animals , Animals, Zoo/growth & development , Animals, Zoo/physiology , Cheirogaleidae/growth & development , Female , MiceSubject(s)
Cheirogaleidae/genetics , Genetics/trends , Models, Animal , Animal Identification Systems , Animals , Atlases as Topic , Cheirogaleidae/physiology , Cheirogaleidae/psychology , Congresses as Topic/organization & administration , Female , Humans , Madagascar , Male , Mice , Parks, Recreational , RainforestABSTRACT
The effects of calorie restriction have now been studied in two non-human primates, the macaque Macaca mulatta and the mouse lemur Microcebus murinus. The study on lemurs and one of the two studies on macaques have reported a lifespan increase. In this review, I argue that these results are better explained by a lifespan decrease in the control group because of a bad diet and/or overfeeding, rather than by a real lifespan increase in calorie-restricted animals. If these results can be readily translated to humans, it would mean that no beneficial effect of calorie restriction on lifespan can be expected in normal-weight or lean people, but that overweight and/or obese people could benefit to some extent from a decrease in excessive food intake.
Subject(s)
Caloric Restriction , Cheirogaleidae/physiology , Longevity/physiology , Macaca mulatta/physiology , Animals , Case-Control Studies , Humans , Overweight/diet therapyABSTRACT
Predator odors such as urine and feces are known to elicit antipredator behaviors in prey including avoidance, fear, and curiosity. We measured how wild brown mouse lemurs (Microcebus rufus) responded to odors of mammalian, avian, and snake predators as well as nonpredator controls. The first experiment took place under controlled conditions in a laboratory where we recorded the occurrence of four behavioral categories (ignore, curiosity, alert, and fear) in response to a single odor. Subjects exhibited behavioral change significantly more often in response to the predator than to control stimuli, but did not distinguish between familiar and unfamiliar predators. Mammalian predator urine and feces were most likely to elicit behavioral change. The owl was the only predator to never elicit behavioral change, possibly because owls do not provide relevant odor cues. A second experiment employing live traps in the forest found that neither predator nor control odors affected the likelihood of capture. Due to their longevity, odors do not provide accurate information of spatial and temporal risk, and while mouse lemurs may have initially hesitated to enter a trap, in the absence of additional information about risk, they may have eventually ignored the stimuli. This study found that brown mouse lemurs are able to distinguish between predator and nonpredator odors, and that risk assessment may be affected by the experience, as well as predator and sensory stimulus quality.
Subject(s)
Behavior, Animal/physiology , Cheirogaleidae/physiology , Odorants , Predatory Behavior , Animals , Boidae , Feces , Female , Madagascar , Male , Mammals , Strigiformes , UrineABSTRACT
Studies on the impact of habitat loss on species occurrence consistently find that the amount of habitat (measured as patch area) is a major determinant of species occurrence at a patch-level. However, patch-level research may fail to detect important patterns and processes only observable at a landscape-level. A landscape-level approach that incorporates species-specific scale responses is needed to better understand what drives species occurrence. Our aim was to determine the landscape-level scale of effect of habitat amount on the occurrence of three species of nocturnal lemurs (Cheirogaleus medius, Microcebus murinus, and M. ravelobensis). We surveyed line transects to determine the occurrence of three lemur species within a fragmented landscape of deciduous dry forest and anthropogenic grassland in northwestern Madagascar. To determine the scale of effect of habitat loss on lemur occurrence, we compared logistic regression models of occurrence against habitat amount among eight different landscape scales using Akaike's Information Criterion values. We found differing scale responses among the lemurs in our study. Occurrence of C. medius responded to habitat amount at scales between 0.5-4 ha, M. murinus at scales between 1 and 4 ha and M. ravelobensis at scales between 0.125 and 4 ha. We suggest that the scale of effect for C. medius is mediated by their ability to hibernate. A relatively lower scale-response for Microcebus spp. likely reflect their omnivorous diet, small habitat requirements, and limited dispersal ability. Differences in scale responses between M. murinus and M. ravelobensis are likely a result of differing dispersal ability and responses to edge effects between these species. Our study is among the first on lemurs to show the value of a landscape-level approach when assessing the effects of habitat loss on species occurrence.
Subject(s)
Cheirogaleidae/physiology , Ecosystem , Animal Distribution , Animals , Diet , Forests , Grassland , Hibernation , Logistic Models , MadagascarABSTRACT
Delimitation of cryptic species is increasingly based on genetic analyses but the integration of distributional, morphological, behavioral, and ecological data offers unique complementary insights into species diversification. We surveyed communities of nocturnal mouse lemurs (Microcebus spp.) in five different sites of northeastern Madagascar, measuring a variety of morphological parameters and assessing reproductive states for 123 individuals belonging to five different lineages. We documented two different non-sister lineages occurring in sympatry in two areas. In both cases, sympatric species pairs consisted of a locally restricted (M. macarthurii or M. sp. #3) and a more widespread lineage (M. mittermeieri or M. lehilahytsara). Estimated Extents of Occurrence (EOO) of these lineages differed remarkably with 560 and 1,500 km2 versus 9,250 and 50,700 km2 , respectively. Morphometric analyses distinguished unambiguously between sympatric species and detected more subtle but significant differences among sister lineages. Tail length and body size were most informative in this regard. Reproductive schedules were highly variable among lineages, most likely impacted by phylogenetic relatedness and environmental variables. While sympatric species pairs differed in their reproductive timing (M. sp. #3/M. lehilahytsara and M. macarthurii/M. mittermeieri), warmer lowland rainforests were associated with a less seasonal reproductive schedule for M. mittermeieri and M. lehilahytsara compared with populations occurring in montane forests. Distributional, morphological, and ecological data gathered in this study support the results of genomic species delimitation analyses conducted in a companion study, which identified one lineage, M. sp. #3, as meriting formal description as a new species. Consequently, a formal species description is included. Worryingly, our data also show that geographically restricted populations of M. sp. #3 and its sister species (M. macarthurii) are at high risk of local and perhaps permanent extinction from both deforestation and habitat fragmentation.
Subject(s)
Cheirogaleidae/anatomy & histology , Cheirogaleidae/classification , Cheirogaleidae/physiology , Animal Distribution , Animals , Ecosystem , Female , Madagascar , Male , Phylogeny , Reproduction/physiology , Seasons , Species SpecificityABSTRACT
Primate loud calls often encode information relating to species identity. A previous study of loud calls of fork-marked lemurs (genus Phaner) indicated differences among the calls of four populations that have been accorded species status on the grounds of morphology and biogeography: Phaner electromontis, P. parienti, P. furciferand P. pallescens. I made field recordings of two typical calls (kiu and kea) emitted by all four populations and conducted playback experiments in Kirindy Forest to investigate whether free-ranging P. pallescensindividuals could discriminate the loud calls of their own species from those of others. Individual response behaviour, social context and call type used in playback were analysed using a goodness-of-fit G test. The effect of specific call identity was significant, while the effects of context and call type were not. Individuals responded to P. pallescens calls by approaching the speaker, but not to the calls of other populations. P. pallescens individuals appear to be capable of distinguishing the loud calls of their conspecifics, but the fact that the habitat structure of the sites of recording and playback of P. pallescenscalls was similar sounds a note of caution. Future studies should repeat the experiments with the other populations of fork-marked lemurs.
Subject(s)
Cheirogaleidae/physiology , Vocalization, Animal , Animals , Female , Madagascar , MaleABSTRACT
The nocturnal mouse and dwarf lemurs from Madagascar are known to express heterothermy. Whereas dwarf lemurs (Cheirogaleus) are obligate hibernators, mouse lemurs (Microcebus) can express a great range of heterothermic responses, including daily torpor, prolonged torpor or hibernation, depending on the species, population or individual. Although there is indirect evidence of heterothermy in a handful of mouse lemur species, direct physiological confirmation is currently limited to four: Microcebus berthae(dry forest), M. ravelobensis(dry forest), M. griseorufus(spiny forest), M. murinus(dry forest/littoral forest). We studied Goodman's mouse lemurs (M. lehilahytsara) at the high-altitude rain forest of Tsinjoarivo, central-eastern Madagascar. We captured a total of 45 mouse lemurs during pre- and post-torpor seasons. We recorded body mass and measured tail base circumference, which was used as proxy for fattening. Moreover, using telemetry, we obtained sporadic skin temperature data from a mouse lemur female between March and June. From June 9 to 16, we performed more intensive data sampling and thereby confirmed the expression of prolonged torpor in this female, when skin temperatures consistently displayed values below 25°C for more than 24 h. We documented 3 torpor bouts, 2 of which were interrupted by naturally occurring arousals. Torpor bout duration ranged from approximately 47 to maximally about 69 h. We found similarities between the Goodman's mouse lemur torpor profile and those known from other species, including the fact that only a portion of any mouse lemur population deposits fat stores and undergoes torpor in a given year. The variable expression of heterothermy in Goodman's mouse lemurs contrasts with obligatory hibernation displayed by two sympatric species of dwarf lemurs, suggesting cheirogaleids use a range of metabolic strategies to cope with seasonality and cold environments.
Subject(s)
Cheirogaleidae/physiology , Torpor/physiology , Adipose Tissue/physiology , Altitude , Animals , Body Weight , Female , Madagascar , MaleABSTRACT
In the early 1990s, Microcebus murinus, a small primate endemic to Madagascar, emerged as a potential animal model for the study of aging and Alzheimer's disease. This paper traces the use of the lesser mouse lemur in research on aging and associated neurodegenerative diseases, focusing on a basic material precondition that made this possible, namely, the conversion of a wild animal into an experimental organism that lives, breeds, and survives in the laboratory. It argues that the "old" mouse lemur model can be considered as an eco-zootechnical acquisition. This is shown by examining how, since the early 1970s, French mouse lemur researchers have articulated colony productivity and viability with the influence of environmental factors on the demographics and physiology of the species. The appearance and maintenance of a growing number of old mouse lemurs in French research facilities are related to three developments: the application of the ecological notion of "social stress" to the understanding and management of the behavior of the captive population; the experimental demonstration that a variety of seasonal physiological changes in the species were influenced by the photoperiod; and the related attempt to accelerate aging in mouse lemurs through the manipulation of annual light conditions.
Subject(s)
Aging , Cheirogaleidae/physiology , Models, Animal , Animals , Disease Models, Animal , Neurodegenerative Diseases/pathology , Neurodegenerative Diseases/physiopathologyABSTRACT
It has been proposed that primates use advertisement calls exclusively to negotiate spacing, but the function of female calls has rarely been studied. Here, we investigated the function of male and female advertisement calls in the northern giant mouse lemur (Mirza zaza),a non-gregarious nocturnal primate from north-western Madagascar. We recorded advertisement calls and associated behaviours of 35 M. zaza individuals at the Duke University Lemur Center. We found that females of M. zazaexclusively use their advertisement calls to advertise oestrus. In contrast, male advertisement calls appeared to be used in a spacing context. These findings show that primates can use their advertisement calls for both spacing and mate attraction, and that the sexes may differ in how they use these calls. The novel find of females of M. zazaattracting mates with loud advertisement calls contrasts with many non-primate taxa, where acoustic mate attraction is usually a function of male advertisement calls, and with other primates, where females use visual and olfactory cues to attract males. The loud female advertisement calls of M. zaza likely ensure mating success during the short receptive phase in this non-gregariously foraging, nocturnal primate.
Subject(s)
Cheirogaleidae/physiology , Sexual Behavior, Animal , Territoriality , Vocalization, Animal , Animals , Female , Madagascar , MaleABSTRACT
Hibernation is an adaptive strategy some mammals use to survive highly seasonal or unpredictable environments. We present the first investigation on the transcriptomics of hibernation in a natural population of primate hibernators: Crossley's dwarf lemurs (Cheirogaleus crossleyi). Using capture-mark-recapture techniques to track the same animals over a period of 7 months in Madagascar, we used RNA-seq to compare gene expression profiles in white adipose tissue (WAT) during three distinct physiological states. We focus on pathway analysis to assess the biological significance of transcriptional changes in dwarf lemur WAT and, by comparing and contrasting what is known in other model hibernating species, contribute to a broader understanding of genomic contributions of hibernation across Mammalia. The hibernation signature is characterized by a suppression of lipid biosynthesis, pyruvate metabolism and mitochondrial-associated functions, and an accumulation of transcripts encoding ribosomal components and iron-storage proteins. The data support a key role of pyruvate dehydrogenase kinase isoenzyme 4 (PDK4) in regulating the shift in fuel economy during periods of severe food deprivation. This pattern of PDK4 holds true across representative hibernating species from disparate mammalian groups, suggesting that the genetic underpinnings of hibernation may be ancestral to mammals.
Subject(s)
Animals, Wild/genetics , Animals, Wild/physiology , Cheirogaleidae/genetics , Cheirogaleidae/physiology , Hibernation/genetics , Transcriptome/genetics , Animals , Body Temperature , Carbohydrate Metabolism/genetics , Gene Expression Profiling , Iron/metabolism , Lipid Metabolism/genetics , Mitochondria/metabolism , Protein Biosynthesis/genetics , RNA, Messenger/genetics , RNA, Messenger/metabolismABSTRACT
The gaits of the adult grey mouse lemur Microcebus murinus were studied during treadmill locomotion over a large range of velocities. The locomotion sequences were analysed to determine the gait and the various spatiotemporal gait parameters of the limbs. We found that velocity adjustments are accounted for differently by stride frequency and stride length depending on whether the animal showed a symmetrical or an asymmetrical gait. When using symmetrical gaits the increase in velocity is associated with a constant contribution of the stride length and stride frequency; the increase of the stride frequency being always lower. When using asymmetrical gaits, the increase in velocity is mainly assured by an increase in the stride length which tends to decrease with increasing velocity. A reduction in both stance time and swing time contributed to the increase in stride frequency for both gaits, though with a major contribution from the decrease in stance time. The pattern of locomotion obtained in a normal young adult mouse lemurs can be used as a template for studying locomotor control deficits during aging or in different environments such as arboreal ones which likely modify the kinematics of locomotion.
Subject(s)
Cheirogaleidae , Gait , Animals , Biomechanical Phenomena , Cheirogaleidae/physiology , Functional Laterality , Gait/physiology , Male , Spatio-Temporal AnalysisABSTRACT
The critically endangered Claire's mouse lemur, only found in the evergreen rain forest of the National Park Lokobe (LNP) and a few lowland evergreen rain forest fragments of northern Madagascar, was described recently. The present study provides the first quantified information on vocal acoustics of calls, sound associated behavioral context, acoustic niche, and vocal activity of this species. We recorded vocal and social behavior of six male-female and six male-male dyads in a standardized social-encounter paradigm in June and July 2016 at the LNP, Nosy Bé island. Over six successive nights per dyad, we audio recorded and observed behaviors for 3 hr at the beginning of the activity period. Based on the visual inspection of spectrograms and standardized multiparametric sound analysis, we identified seven different call types. Call types can be discriminated based on a combination of harmonicity, fundamental frequency variation, call duration, and degree of tonality. Acoustic features of tonal call types showed that for communication, mouse lemurs use the cryptic, high frequency/ultrasonic frequency niche. Two call types, the Tsak and the Grunt call, were emitted most frequently. Significant differences in vocal activity of the Tsak call were found between male-female and male-male dyads, linked primarily to agonistic conflicts. Dominant mouse lemurs vocalized more than subdominant ones, suggesting that signaling may present an honest indicator of fitness. A comparison of our findings of the Claire's mouse lemur with published findings of five bioacoustically studied mouse lemur species points to the notion that a complex interplay between ecology, predation pressure, and phylogenetic relatedness may shape the evolution of acoustic divergence between species in this smallest-bodied primate radiation. Thus, comparative bioacoustic studies, using standardized procedures, are promising to unravel the role of vocalization for primate species diversity and evolution and for identifying candidates for vocalization-based non-invasive monitoring for conservation purposes.
Subject(s)
Cheirogaleidae/physiology , Vocalization, Animal/physiology , Animals , Endangered Species , Female , Madagascar , Male , Social Dominance , Sound Spectrography , Ultrasonic WavesABSTRACT
Reproduction is a fundamental trait in the life history of any species and contributes to species diversity and evolution. Here, we aim to review the barely known variation in reproductive patterns of the smallest-bodied primate radiation, the Malagasy mouse lemurs, focusing on twelve species of four phylogenetic clades. We present a new reproductive field dataset collected between May and November 1996-2016 for nine species (Microcebus murinus, M. myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi, M. sambiranensis, M. margothmarshae, M. mamiratra, and M. lehilahytsara) and add published field information on three additional species. In the majority of species, the estrus of females was recorded in the period of long days (day length longer than 12 hr), whereas male testes size increased about one to three months prior to this. Reproductive schedules varied considerably between the four clades. Sympatric species-pairs of different clades differed in the timing of female and male reproduction, suggesting strong phylogenetic constraints. Populations of the same species in a different ecological setting varied in the onset of reproduction, suggesting substantial environmental plasticity. Warm temperatures and rainfall throughout the year may allow for less expressed reproductive seasonality. Our results suggest that an interplay between phylogenetic relatedness, ambient temperature (as a proxy for thermo regulatory constraints), and rainfall (as a proxy for food availability), may best explain this variation. Findings further point to a more complex control of mouse lemur reproduction than previously described and illuminate phylogenetic constraints and adaptive potentials in behavioral reaction norms of a species-rich primate radiation.