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1.
Commun Biol ; 7(1): 609, 2024 May 20.
Article in English | MEDLINE | ID: mdl-38769408

ABSTRACT

Dairy fat has a unique lipid profile; it is rich in short- and medium-chain saturated fatty acids that induce ketone production and has a balanced ω6/ω3 ratio that promotes cognitive development in early life. Moreover, the high consumption of vegetable oils in pregnant and lactating women raises concerns regarding the quality of lipids provided to offspring. Here, we investigate maternal dairy fat intake during gestation and lactation in a highly valuable primate model for infant nutritional studies, the gray mouse lemur (Microcebus murinus). Two experimental diets are provided to gestant mouse lemurs: a dairy fat-based (DF) or vegetable fat-based diet (VF). The psychomotor performance of neonates is tested during their first 30 days. Across all tasks, we observe more successful neonates born to mothers fed a DF diet. A greater rate of falls is observed in 8-day-old VF neonates, which is associated with delayed psychomotor development. Our findings suggest the potential benefits of lipids originating from a lactovegetarian diet compared with those originating from a vegan diet for the psychomotor development of neonates.


Subject(s)
Cheirogaleidae , Cognition , Dietary Fats , Animals , Female , Cheirogaleidae/physiology , Pregnancy , Animals, Newborn , Psychomotor Performance , Dairy Products , Maternal Nutritional Physiological Phenomena , Lactation , Male , Plant Oils/administration & dosage
2.
Philos Trans R Soc Lond B Biol Sci ; 379(1905): 20230193, 2024 Jul 08.
Article in English | MEDLINE | ID: mdl-38768201

ABSTRACT

Vocalizations coordinate social interactions between conspecifics by conveying information concerning the individual or group identity of the sender. Social accommodation is a form of vocal learning where social affinity is signalled by converging or diverging vocalizations with those of conspecifics. To investigate whether social accommodation is linked to the social lifestyle of the sender, we investigated sex-specific differences in social accommodation in a dispersed living primate, the grey mouse lemur (Microcebus murinus), where females form stable sleeping groups whereas males live solitarily. We used 482 trill calls of 36 individuals from our captive breeding colony to compare acoustic dissimilarity between individuals with genetic relatedness, social contact time and body weight. Our results showed that female trills become more similar the more time females spend with each other, independent of genetic relationship, suggesting vocal convergence. In contrast, male trills were affected more by genetic than social factors. However, focusing only on socialized males, increasing time as cage partners caused greater divergence in males' trills. Thus, grey mouse lemurs show the capacity for social accommodation, with females converging their trills to signal social closeness to sleeping group partners, whereas males do not adapt or diverge their trills to signal individual distinctiveness. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.


Subject(s)
Cheirogaleidae , Social Behavior , Vocalization, Animal , Animals , Cheirogaleidae/physiology , Male , Female , Sex Characteristics , Sex Factors
3.
J Therm Biol ; 121: 103829, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38569326

ABSTRACT

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 Regulation
4.
J Comp Physiol B ; 194(2): 213-219, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38466418

ABSTRACT

Hibernation is a widespread metabolic strategy among mammals for surviving periods of food scarcity. During hibernation, animals naturally alternate between metabolically depressed torpor bouts and energetically expensive arousals without ill effects. As a result, hibernators are promising models for investigating mechanisms that buffer against cellular stress, including telomere protection and restoration. In non-hibernators, telomeres, the protective structural ends of chromosomes, shorten with age and metabolic stress. In temperate hibernators, however, telomere shortening and elongation can occur in response to changing environmental conditions and associated metabolic state. We investigate telomere dynamics in a tropical hibernating primate, the fat-tailed dwarf lemur (Cheirogaleus medius). In captivity, these lemurs can hibernate when maintained under cold temperatures (11-15 °C) with limited food provisioning. We study telomere dynamics in eight fat-tailed dwarf lemurs at the Duke Lemur Center, USA, from samples collected before, during, and after the hibernation season and assayed via qPCR. Contrary to our predictions, we found that telomeres were maintained or even lengthened during hibernation, but shortened immediately thereafter. During hibernation, telomere lengthening was negatively correlated with time in euthermia. Although preliminary in scope, our findings suggest that there may be a preemptive, compensatory mechanism to maintain telomere integrity in dwarf lemurs during hibernation. Nevertheless, telomere shortening immediately afterward may broadly result in similar outcomes across seasons. Future studies could profitably investigate the mechanisms that offset telomere shortening within and outside of the hibernation season and whether those mechanisms are modulated by energy surplus or crises.


Subject(s)
Cheirogaleidae , Hibernation , Telomere , Animals , Hibernation/physiology , Cheirogaleidae/physiology , Cheirogaleidae/genetics , Male , Female , Telomere Homeostasis/physiology , Telomere Shortening/physiology , Seasons
5.
Sci Rep ; 13(1): 7970, 2023 05 17.
Article in English | MEDLINE | ID: mdl-37198192

ABSTRACT

Non-human primates are a critical species for the identification of key biological mechanisms in normal and pathological aging. One of these primates, the mouse lemur, has been widely studied as a model of cerebral aging or Alzheimer's disease. The amplitude of low-frequency fluctuations of blood oxygenation level-dependent (BOLD) can be measured with functional MRI. Within specific frequency bands (e.g. the 0.01-0.1 Hz), these amplitudes were proposed to indirectly reflect neuronal activity as well as glucose metabolism. Here, we first created whole brain maps of the mean amplitude of low frequency fluctuations (mALFF) in young mouse lemurs (mean ± SD: 2.1 ± 0.8 years). Then, we extracted mALFF in old lemurs (mean ± SD: 8.8 ± 1.1 years) to identify age-related changes. A high level of mALFF was detected in the temporal cortex (Brodmann area 20), somatosensory areas (Brodmann area 5), insula (Brodmann areas 13-6) and the parietal cortex (Brodmann area 7) of healthy young mouse lemurs. Aging was associated with alterations of mALFF in somatosensory areas (Brodmann area 5) and the parietal cortex (Brodmann area 7).


Subject(s)
Alzheimer Disease , Cheirogaleidae , Lemur , Lemuridae , Sensorimotor Cortex , Strepsirhini , Animals , Cheirogaleidae/physiology , Magnetic Resonance Imaging , Brain/pathology , Aging , Alzheimer Disease/pathology
6.
Proc Natl Acad Sci U S A ; 120(14): e2214244120, 2023 04 04.
Article in English | MEDLINE | ID: mdl-36972440

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/physiology
7.
Chronobiol Int ; 39(3): 363-373, 2022 03.
Article in English | MEDLINE | ID: mdl-34802342

ABSTRACT

The biological clock generates circadian rhythms, with an endogenous period tau close to 24 h. The circadian resonance theory proposes that lifespan is reduced when endogenous period goes far from 24 h. It has been suggested that daily resetting of the circadian clock to the 24 h external photoperiod might induce marginal costs that would accumulate over time and forward accelerate aging and affect fitness. In this study, we aimed to evaluate the link between the endogenous period and biomarkers of aging in order to investigate the mechanisms of the circadian resonance theory. We studied 39 middle-aged and aged Microcebus murinus, a nocturnal non-human primate whose endogenous period is about 23.1 h, measuring the endogenous period of locomotor activity, as well as several physiological and behavioral parameters (rhythm fragmentation and amplitude, energetic expenditure, oxidative stress, insulin-like growth factor-1 (IGF-1) concentrations and cognitive performances) in both males and females. We found that aged males with tau far from 24 h displayed increased oxidative stress. We also demonstrated a positive correlation between tau and IGF-1 concentrations, as well as learning performances, in males and females. Together these results suggest that a great deviation of tau from 24 h leads to increased biomarkers of age-related impairments.


Subject(s)
Cheirogaleidae , Animals , Cheirogaleidae/physiology , Circadian Rhythm/physiology , Cognition , Female , Insulin-Like Growth Factor I , Male , Photoperiod
8.
Sci Rep ; 11(1): 24463, 2021 12 27.
Article in English | MEDLINE | ID: mdl-34961788

ABSTRACT

Bioacoustic analyses of animal vocalizations are predominantly accomplished through manual scanning, a highly subjective and time-consuming process. Thus, validated automated analyses are needed that are usable for a variety of animal species and easy to handle by non-programing specialists. This study tested and validated whether DeepSqueak, a user-friendly software, developed for rodent ultrasonic vocalizations, can be generalized to automate the detection/segmentation, clustering and classification of high-frequency/ultrasonic vocalizations of a primate species. Our validation procedure showed that the trained detectors for vocalizations of the gray mouse lemur (Microcebus murinus) can deal with different call types, individual variation and different recording quality. Implementing additional filters drastically reduced noise signals (4225 events) and call fragments (637 events), resulting in 91% correct detections (Ntotal = 3040). Additionally, the detectors could be used to detect the vocalizations of an evolutionary closely related species, the Goodman's mouse lemur (M. lehilahytsara). An integrated supervised classifier classified 93% of the 2683 calls correctly to the respective call type, and the unsupervised clustering model grouped the calls into clusters matching the published human-made categories. This study shows that DeepSqueak can be successfully utilized to detect, cluster and classify high-frequency/ultrasonic vocalizations of other taxa than rodents, and suggests a validation procedure usable to evaluate further bioacoustics software.


Subject(s)
Cheirogaleidae/physiology , Vocalization, Animal , Animals , Machine Learning , Software , Ultrasonics
9.
Curr Opin Neurobiol ; 71: 92-99, 2021 12.
Article in English | MEDLINE | ID: mdl-34768148

ABSTRACT

The gray mouse lemur (Microcebus murinus), one of the world's smallest primates, is thought to share a similar ecological niche and many anatomical traits with early euprimates. As a result, it has been considered a suitable model system for early primate physiology and behavior. Moreover, recent studies have demonstrated that mouse lemurs have comparable cognitive abilities and cortical functional organization as haplorhines. Finally, the small brain size of mouse lemurs provides us with actual lower limits for miniaturization of functional brain circuits within the primate clade. Considering its phylogenetic position and early primate-like traits, the mouse lemurs are a perfect model species to study the early evolution of primate brains.


Subject(s)
Cheirogaleidae , Animals , Brain , Cheirogaleidae/physiology , Cognition , Phylogeny
10.
Commun Biol ; 4(1): 1084, 2021 09 15.
Article in English | MEDLINE | ID: mdl-34526636

ABSTRACT

Quaternary climatic changes have been invoked as important drivers of species diversification worldwide. However, the impact of such changes on vegetation and animal population dynamics in tropical regions remains debated. To overcome this uncertainty, we integrated high-resolution paleoenvironmental reconstructions from a sedimentary record covering the past 25,000 years with demographic inferences of a forest-dwelling primate species (Microcebus arnholdi), in northern Madagascar. Result comparisons suggest that climate changes through the African Humid Period (15.2 - 5.5 kyr) strongly affected the demographic dynamics of M. arnholdi. We further inferred a population decline in the last millennium which was likely shaped by the combination of climatic and anthropogenic impacts. Our findings demonstrate that population fluctuations in Malagasy wildlife were substantial prior to a significant human impact. This provides a critical knowledge of climatically driven, environmental and ecological changes in the past, which is essential to better understand the dynamics and resilience of current biodiversity.


Subject(s)
Cheirogaleidae/physiology , Ecosystem , Animals , Madagascar , Population Dynamics
11.
Sci Rep ; 11(1): 5740, 2021 03 11.
Article in English | MEDLINE | ID: mdl-33707506

ABSTRACT

In nature, photoperiod signals environmental seasonality and is a strong selective "zeitgeber" that synchronizes biological rhythms. For animals facing seasonal environmental challenges and energetic bottlenecks, daily torpor and hibernation are two metabolic strategies that can save energy. In the wild, the dwarf lemurs of Madagascar are obligate hibernators, hibernating between 3 and 7 months a year. In captivity, however, dwarf lemurs generally express torpor for periods far shorter than the hibernation season in Madagascar. We investigated whether fat-tailed dwarf lemurs (Cheirogaleus medius) housed at the Duke Lemur Center (DLC) could hibernate, by subjecting 8 individuals to husbandry conditions more in accord with those in Madagascar, including alternating photoperiods, low ambient temperatures, and food restriction. All dwarf lemurs displayed daily and multiday torpor bouts, including bouts lasting ~ 11 days. Ambient temperature was the greatest predictor of torpor bout duration, and food ingestion and night length also played a role. Unlike their wild counterparts, who rarely leave their hibernacula and do not feed during hibernation, DLC dwarf lemurs sporadically moved and ate. While demonstrating that captive dwarf lemurs are physiologically capable of hibernation, we argue that facilitating their hibernation serves both husbandry and research goals: first, it enables lemurs to express the biphasic phenotypes (fattening and fat depletion) that are characteristic of their wild conspecifics; second, by "renaturalizing" dwarf lemurs in captivity, they will emerge a better model for understanding both metabolic extremes in primates generally and metabolic disorders in humans specifically.


Subject(s)
Cheirogaleidae/physiology , Hibernation/physiology , Animals , Feeding Behavior , Female , Linear Models , Male , North Carolina , Photoperiod , Temperature , Time Factors , Torpor/physiology , Weight Loss
12.
Sci Rep ; 11(1): 1252, 2021 01 13.
Article in English | MEDLINE | ID: mdl-33442034

ABSTRACT

The ability to associate memorized objects with their location in space gradually declines during normal aging and can drastically be affected by neurodegenerative diseases. This study investigates object-location paired-associates learning (PAL) in the grey mouse lemur (Microcebus murinus), a nonhuman primate model of brain aging. Touchscreen-based testing of 6 young adults (1-5 years) and 6 old adults (> 7 years) in the procedural rodent dPAL-task revealed significant age-related performance decline, evident in group differences in the percentage of correct decision during learning and the number of sessions needed to reach a predefined criterion. Response pattern analyses suggest decreased susceptibility to relative stimulus-position biases in young animals, facilitating PAL. Additional data from a subset of "overtrained" individuals (n = 7) and challenge sessions using a modified protocol (sPAL) further suggest that learning criteria routinely used in animal studies on PAL can underestimate the endpoint at which a stable performance is reached and that more conservative criteria are needed to improve construct validity of the task. To conclude, this is the first report of an age effect on dPAL and corroborates the role of mouse lemurs as valuable natural nonhuman primate models in aging research.


Subject(s)
Aging/physiology , Brain/physiology , Cheirogaleidae/physiology , Paired-Associate Learning/physiology , Animals , Female , Male
13.
Folia Primatol (Basel) ; 92(1): 1-11, 2021.
Article in English | MEDLINE | ID: mdl-33291109

ABSTRACT

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 , Madagascar
14.
Curr Biol ; 31(4): 733-741.e7, 2021 02 22.
Article in English | MEDLINE | ID: mdl-33275889

ABSTRACT

Orientation preference maps (OPMs) are a prominent feature of primary visual cortex (V1) organization in many primates and carnivores. In rodents, neurons are not organized in OPMs but are instead interspersed in a "salt and pepper" fashion, although clusters of orientation-selective neurons have been reported. Does this fundamental difference reflect the existence of a lower size limit for orientation columns (OCs) below which they cannot be scaled down with decreasing V1 size? To address this question, we examined V1 of one of the smallest living primates, the 60-g prosimian mouse lemur (Microcebus murinus). Using chronic intrinsic signal imaging, we found that mouse lemur V1 contains robust OCs, which are arranged in a pinwheel-like fashion. OC size in mouse lemurs was found to be only marginally smaller compared to the macaque, suggesting that these circuit elements are nearly incompressible. The spatial arrangement of pinwheels is well described by a common mathematical design of primate V1 circuit organization. In order to accommodate OPMs, we found that the mouse lemur V1 covers one-fifth of the cortical surface, which is one of the largest V1-to-cortex ratios found in primates. These results indicate that the primate-type visual cortical circuit organization is constrained by a size limitation and raises the possibility that its emergence might have evolved by disruptive innovation rather than gradual change.


Subject(s)
Cheirogaleidae , Primary Visual Cortex/anatomy & histology , Primary Visual Cortex/physiology , Animals , Cheirogaleidae/anatomy & histology , Cheirogaleidae/physiology , Female , Male , Models, Neurological , Neurons/physiology , Orientation , Primary Visual Cortex/cytology
15.
Behav Brain Res ; 399: 113053, 2021 02 05.
Article in English | MEDLINE | ID: mdl-33279643

ABSTRACT

The grey mouse lemur (Microcebus murinus) is a promising nonhuman primate model for brain ageing and neurodegenerative diseases. Age-related cognitive decline in this model is well described, however, data on possible relations between attention and age, as they are known from humans, are missing. We tested 10 mouse lemurs in a touchscreen-based version of the 5-choice-serial-reaction-time-task (5CSRTT) on visuo-spatial attention: subjects had to interact with a briefly presented stimulus occurring unpredictably in one out of five locations on the touchscreen. Animals were trained to an 80 % performance at a four seconds stimulus presentation duration (SPD) and subsequently challenged by a SPD of two seconds. Additionally, ventricular expansion was assessed using structural magnetic resonance imaging. Trials to the 80 % criterion at four seconds SPD correlated significantly with age and with ventricular expansion, especially around the occipital lobe. Once criterion performance was reached, two seconds challenge performance was independent of age. In four subjects that were additionally challenged with 1.5, 1.0, 0.8, or 0.6 s SPDs or variable delays preceding stimulus presentation, performance linearly declined with decreasing SPD, i.e. increasing attentional demand. In conclusion, this is the first report of 5CSRTT data in mouse lemurs and demonstrates the general applicability of this task of visuo-spatial attention to this nonhuman primate model. Results further demonstrate age-related deficits in learning during acquisition of the 5CSRTT and suggest that both may be linked through age-related atrophy of occipital structures and a resulting deficit in central visual processes.


Subject(s)
Attention/physiology , Cheirogaleidae/physiology , Cognitive Aging/physiology , Conditioning, Operant/physiology , Psychomotor Performance/physiology , Serial Learning/physiology , Age Factors , Animals , Behavior, Animal/physiology , Female , Magnetic Resonance Imaging , Male , Motor Activity/physiology , Reaction Time/physiology , Space Perception/physiology , Visual Perception/physiology
16.
Sci Rep ; 10(1): 18002, 2020 10 22.
Article in English | MEDLINE | ID: mdl-33093578

ABSTRACT

Circadian rhythms are ubiquitous attributes across living organisms and allow the coordination of internal biological functions with optimal phases of the environment, suggesting a significant adaptive advantage. The endogenous period called tau lies close to 24 h and is thought to be implicated in individuals' fitness: according to the circadian resonance theory, fitness is reduced when tau gets far from 24 h. In this study, we measured the endogenous period of 142 mouse lemurs (Microcebus murinus), and analyzed how it is related to their survival. We found different effects according to sex and season. No impact of tau on mortality was found in females. However, in males, the deviation of tau from 24 h substantially correlates with an increase in mortality, particularly during the inactive season (winter). These results, comparable to other observations in mice or drosophila, show that captive gray mouse lemurs enjoy better fitness when their circadian period closely matches the environmental periodicity. In addition to their deep implications in health and aging research, these results raise further ecological and evolutionary issues regarding the relationships between fitness and circadian clock.


Subject(s)
Aging/physiology , Biological Evolution , Cheirogaleidae/physiology , Circadian Rhythm , Mortality/trends , Photoperiod , Seasons , Animals , Circadian Clocks , Female , Male
17.
Am J Primatol ; 82(10): e23184, 2020 10.
Article in English | MEDLINE | ID: mdl-32770568

ABSTRACT

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 , Urine
18.
Am J Primatol ; 82(9): e23180, 2020 09.
Article in English | MEDLINE | ID: mdl-32716088

ABSTRACT

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 Specificity
19.
Chem Senses ; 45(7): 581-592, 2020 10 09.
Article in English | MEDLINE | ID: mdl-32710747

ABSTRACT

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 Specificity
20.
Folia Primatol (Basel) ; 91(6): 697-710, 2020.
Article in English | MEDLINE | ID: mdl-32731251

ABSTRACT

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 , Male
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