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Anne D. Yoder - One of the best experts on this subject based on the ideXlab platform.
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Bamboo Specialists from Two Mammalian Orders (Primates, Carnivora) Share a High Number of Low-Abundance Gut Microbes
Microbial Ecology, 2018Co-Authors: Erin A. Mckenney, Michael Maslanka, Allen Rodrigo, Anne D. YoderAbstract:Bamboo specialization is one of the most extreme examples of convergent herbivory, yet it is unclear how this specific high-fiber diet might selectively shape the composition of the gut microbiome compared to host phylogeny. To address these questions, we used deep sequencing to investigate the nature and comparative impact of phylogenetic and dietary selection for specific gut microbial membership in three bamboo specialists—the bamboo lemur ( Hapalemur griseus , Primates: Lemuridae), giant panda ( Ailuropoda melanoleuca , Carnivora: Ursidae), and red panda ( Ailurus fulgens , Carnivora: Musteloideadae), as well as two phylogenetic controls—the ringtail lemur ( Lemur catta ) and the Asian black bear ( Ursus thibetanus ). We detected significantly higher Shannon diversity in the bamboo lemur (10.029) compared to both the giant panda (8.256; p = 0.0001936) and the red panda (6.484; p = 0.0000029). We also detected significantly enriched bacterial taxa that distinguished each species. Our results complement previous work in finding that phylogeny predominantly governs high-level microbiome community structure. However, we also find that 48 low-abundance OTUs are shared among bamboo specialists, compared to only 8 OTUs shared by the bamboo lemur and its sister species, the ringtail lemur ( Lemur catta , a generalist). Our results suggest that deep sequencing is necessary to detect low-abundance bacterial OTUs, which may be specifically adapted to a high-fiber diet. These findings provide a more comprehensive framework for understanding the evolution and ecology of the microbiome as well as the host.
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development and application of a phylogenomic toolkit resolving the evolutionary history of madagascar s lemurs
Genome Research, 2008Co-Authors: Julie E Horvath, Peter M Kappeler, David W Weisrock, Stephanie L Embry, Isabella Fiorentino, James P Balhoff, Gregory A Wray, Huntington F Willard, Anne D. YoderAbstract:Lemurs and the other strepsirrhine primates are of great interest to the primate genomics community due to their phylogenetic placement as the sister lineage to all other primates. Previous attempts to resolve the phylogeny of lemurs employed limited mitochondrial or small nuclear data sets, with many relationships poorly supported or entirely unresolved. We used genomic resources to develop 11 novel markers from nine chromosomes, representing ∼9 kb of nuclear sequence data. In combination with previously published nuclear and mitochondrial loci, this yields a data set of more than 16 kb and adds ∼275 kb of DNA sequence to current databases. Our phylogenetic analyses confirm hypotheses of lemuriform monophyly and provide robust resolution of the phylogenetic relationships among the five lemuriform families. We verify that the genus Daubentonia is the sister lineage to all other lemurs. The Cheirogaleidae and LepiLemuridae are sister taxa and together form the sister lineage to the Indriidae; this clade is the sister lineage to the Lemuridae. Divergence time estimates indicate that lemurs are an ancient group, with their initial diversification occurring around the Cretaceous-Tertiary boundary. Given the power of this data set to resolve branches in a notoriously problematic area of primate phylogeny, we anticipate that our phylogenomic toolkit will be of value to other studies of primate phylogeny and diversification. Moreover, the methods applied will be broadly applicable to other taxonomic groups where phylogenetic relationships have been notoriously difficult to resolve. [Supplemental material is available online at www.genome.org. The sequence data from this study have been submitted to GenBank under accession nos. EU057196–EU057514 and EU342218–EU342345.]
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Structure and Function of CC-Chemokine Receptor 5 Homologues Derived from Representative Primate Species and Subspecies of the Taxonomic Suborders Prosimii and Anthropoidea
Journal of virology, 2003Co-Authors: Kevin J. Kunstman, Bridget A. Puffer, Bette T. Korber, Carla Kuiken, Una R. Smith, Jennifer Kunstman, Jennifer Stanton, Michael B. Agy, Riri Shibata, Anne D. YoderAbstract:A chemokine receptor from the seven-transmembrane-domain G-protein-coupled receptor superfamily is an essential coreceptor for the cellular entry of human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency virus (SIV) strains. To investigate nonhuman primate CC-chemokine receptor 5 (CCR5) homologue structure and function, we amplified CCR5 DNA sequences from peripheral blood cells obtained from 24 representative species and subspecies of the primate suborders Prosimii (family Lemuridae) and Anthropoidea (families Cebidae, Callitrichidae, Cercopithecidae, Hylobatidae, and Pongidae) by PCR with primers flanking the coding region of the gene. Full-length CCR5 was inserted into pCDNA3.1, and multiple clones were sequenced to permit discrimination of both alleles. Compared to the human CCR5 sequence, the CCR5 sequences of the Lemuridae, Cebidae, and Cercopithecidae shared 87, 91 to 92, and 96 to 99% amino acid sequence homology, respectively. Amino acid substitutions tended to cluster in the amino and carboxy termini, the first transmembrane domain, and the second extracellular loop, with a pattern of species-specific changes that characterized CCR5 homologues from primates within a given family. At variance with humans, all primate species examined from the suborder Anthropoidea had amino acid substitutions at positions 13 (N to D) and 129 (V to I); the former change is critical for CD4-independent binding of SIV to CCR5. Within the Cebidae, Cercopithecidae, and Pongidae (including humans), CCR5 nucleotide similarities were 95.2 to 97.4, 98.0 to 99.5, and 98.3 to 99.3%, respectively. Despite this low genetic diversity, the phylogeny of the selected primate CCR5 homologue sequences agrees with present primate systematics, apart from some intermingling of species of the Cebidae and Cercopithecidae. Constructed HOS.CD4 cell lines expressing the entire CCR5 homologue protein from each of the Anthropoidea species and subspecies were tested for their ability to support HIV-1 and SIV entry and membrane fusion. Other than that of Cercopithecus pygerythrus, all CCR5 homologues tested were able to support both SIV and HIV-1 entry. Our results suggest that the shared structure and function of primate CCR5 homologue proteins would not impede the movement of primate immunodeficiency viruses between species.
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Phylogeny of the Lemuridae: Effects of Character and Taxon Sampling on Resolution of Species Relationships within Eulemur☆
Cladistics, 1999Co-Authors: Anne D. Yoder, Jodi A. IrwinAbstract:DNA sequences from three mitochondrial genes and one nuclear gene were analyzed to determine the phylogeny of the Malagasy primate family Lemuridae. Whether analyzed separately or in combination, the data consistently indicate that Eulemur species comprise a clade that is sister to a Lemur catta plus Hapalemur clade. The genus Varecia is basal to both. Resolution of cladogenic events within Eulemur was found to be extremely problematic with a total of six alternative arrangements offered by various data sets and weighting regimes. We attempt to determine the best arrangement of Eulemur taxa through a variety of character and taxon sampling strategies. Because our study includes all but one Eulemur species, increased taxon sampling is probably not an option for enhancing phylogenetic accuracy. We find, however, that the combined genetic data set is more robust to changes in taxon sample than are any of the individual data sets, suggesting that increased character sampling stabilizes phylogenetic resolution. Nonetheless, due to the difficult nature of the problem, we may have to accept certain aspects of Eulemur interrelationships as uncertain.
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Phylogeny of the Lemuridae: Effects of character and taxon sampling on resolution of species relationships within Eulemur. Cladistics 15: 351361
1999Co-Authors: Anne D. Yoder, Jodi A. IrwinAbstract:DNA sequences from three mitochondrial genes and one nuclear gene were analyzed to determine the phylogeny of the Malagasy primate family Lemuridae. Whether ana-lyzed separately or in combination, the data consistently indicate that Eulemur species comprise a clade that is sister to a Lemur catta plus Hapalemur clade. The genus Varecia is basal to both. Resolution of cladogenic events within Eulemur was found to be extremely problematic with a total of six alternative arrangements offered by various data sets and weighting regimes. We attempt to determine the best arrangement of Eulemur taxa through a variety of character and taxon sampling strategies. Because our study includes all but one Eulemur species, increased taxon sampling is probably not an option for enhancing phylogenetic accuracy. We find, however, that the combined genetic data set is more robust to changes in taxon sample than are any of the individual data sets, suggesting that increased character sampling stabilizes phylogenetic resolution. Nonetheless, due to the difficult nature of the problem, we may have to accept 1To whom correspondence should be addressed at Department o
Timothy M Eppley - One of the best experts on this subject based on the ideXlab platform.
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do functional traits offset the effects of fragmentation the case of large bodied diurnal lemur species
American Journal of Primatology, 2020Co-Authors: Timothy M Eppley, Luca Santini, Jen Tinsman, Giuseppe DonatiAbstract:Primates worldwide are faced with increasing threats making them more vulnerable to extinction. Anthropogenic disturbances, such as habitat degradation and fragmentation, are among the main concerns, and in Madagascar, these issues have become widespread. As this situation continues to worsen, we sought to understand how fragmentation affects primate distribution throughout the island. Further, because species may exhibit different sensitivity to fragmentation, we also aimed to estimate the role of functional traits in mitigating their response. We collated data from 32 large-bodied lemur species ranges, consisting of species from the families Lemuridae (five genera) and Indriidae (two genera). We fitted Generalized Linear Models to determine the role of habitat fragmentation characteristics, for example, forest cover, patch size, edge density, and landscape configuration, as well as the protected area (PA) network, on the species relative probability of presence. We then assessed how the influence of functional traits (dietary guild, home range size) mitigate the response of species to these habitat metrics. Habitat area had a strong positive effect for many species, and there were significantly negative effects of fragmentation on the distribution of many lemur species. In addition, there was a positive influence of PAs on many lemur species' distribution. Functional trait classifications showed that lemurs of all dietary guilds are negatively affected by fragmentation; however, folivore-frugivores show greater flexibility/variability in terms of habitat area and landscape complexity compared to nearly exclusive folivores and frugivores. Furthermore, species of all home range sizes showed a negative response to fragmentation, while habitat area had an increasingly positive effect as home range increased in size. Overall, the general trends for the majority of lemur species are dire and point to the need for immediate actions on a multitude of fronts, most importantly landscape-level reforestation efforts.
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predator avoidance and dietary fibre predict diurnality in the cathemeral folivore hapalemur meridionalis
Behavioral Ecology and Sociobiology, 2017Co-Authors: Timothy M Eppley, Joerg U Ganzhorn, Julia Watzek, Giuseppe DonatiAbstract:Though numerous mammalian taxa exhibit cathemerality (i.e. activity distributed across the 24-h cycle), this includes very few primates, exceptions being species from Aotinae and Lemuridae. Four non-mutually exclusive hypotheses have been proposed to explain the ultimate determinants for cathemeral activity in lemurs: thermoregulatory benefits, anti-predator strategy, competition avoidance and metabolic dietary-related needs. However, these have only been explored in the frugivorous genus Eulemur, with some species increasing nocturnality as a possible response to avoid diurnal raptors and to increase their ability to digest fibre during resource-scarce periods. Since Eulemur lack specializations for digesting bulk food, this strategy would allow for processing fibres over the full 24-h. The folivorous lemurids, i.e. genus Hapalemur, provide a divergent model to explore these hypotheses due to gastrointestinal adaptations for digesting dietary fibre and small body size compared to Eulemur. We linked continuous activity data collected from archival tags with observational behaviour and feeding data from three groups of adult Hapalemur meridionalis from January to December 2013. We tested the effects of thermoregulation, predator avoidance and the weighted proportion of digestible dietary fibre on the daily diurnal/nocturnal activity ratio using a Linear Mixed-Model. Our best-fit model revealed that increased canopy exposure and dietary fibre predicted greater diurnality. Our findings partly contrast with previous predictions for frugivorous lemurids. We propose a divergent adaptive explanation for folivorous lemurids. We suggest that the need to avoid terrestrial predators, as well as longer digestive bouts during bulk food periods, may override cathemerality in favour of diurnality in these bamboo lemurs. Southern bamboo lemurs are active throughout the 24-h day, with high proportions of dietary fibre increasing diurnality, in contrast to other cathemeral primates. They also increase diurnality on days when using areas with greater canopy exposure, potentially avoiding nocturnal predators in risky foraging areas. We suggest that folivorous lemurids may require long periods of inactivity to conserve energy and digest dietary fibre, thus limiting activity to periods of optimal foraging efficiency over the 24-h cycle.
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cathemerality in a small folivorous primate proximate control of diel activity in hapalemur meridionalis
Behavioral Ecology and Sociobiology, 2015Co-Authors: Timothy M Eppley, Joerg U Ganzhorn, Giuseppe DonatiAbstract:A non-adherence to a strict diurnal or nocturnal activity cycle is prevalent among mammals, including taxa of Lemuridae, but rare among other primates. While non-mutually exclusive ecological hypotheses attempted to explain the evolution of this activity, termed cathemerality, as either an old or a recent phenomenon, the scarcity of systematic data collected over 24 h limits our potential to explore its proximate and ultimate determinants. Among strepsirrhines, systematic studies involving only two lemurid genera (Eulemur and Lemur) have recorded this activity pattern, while fewer quantitative observations are available for other taxa. If cathemerality could be shown in most members of Lemuridae despite their different ecological adaptations, this would support the hypothesis that this trait is basal and appeared early during lemurid evolution. Here, we investigated whether the folivorous southern bamboo lemur (Hapalemur meridionalis) exhibits cathemeral activity, and determined which environmental factors influence its pattern. We deployed ten archival tags across four social groups to continuously record activity data over a 15-month period. This allowed us to generate a diurnal/nocturnal (DN) ratio for each 24-h period and assess their diel activity. Our data suggest that southern bamboo lemurs are cathemeral within Mandena; while climatic factors showed no influence, nocturnal activity increased with greater nocturnal luminance. Despite contrasting dietary niches, visual morphologies, and body sizes between Hapalemur, Eulemur, and Lemur, all three exhibit cathemerality and lunarphilia. The close phylogenetic proximity of these lemurids supports this flexible activity pattern as an ancestral trait that likely dates to the origin of the Lemuridae radiation.
Nayuta Yamashita - One of the best experts on this subject based on the ideXlab platform.
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cathemerality in wild ring tailed lemurs lemur catta in the spiny forest of tsimanampetsotsa national park camera trap data and preliminary behavioral observations
Primates, 2014Co-Authors: Marni Lafleur, Nayuta Yamashita, Michelle L Sauther, Frank P Cuozzo, Ibrahim Antho Jacky Youssouf, Richard L BenderAbstract:Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered “strictly diurnal”. We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010–April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25 % of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5 % of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53 % nighttime, 43 % daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.
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molar morphology and variation in two malagasy lemur families Lemuridae and indriidae
Journal of Human Evolution, 1998Co-Authors: Nayuta YamashitaAbstract:Abstract The lemurs of Madagascar represent a radiation of primates exhibiting considerable ecological and morphological diversity. Dentally, all lemurs possess the characteristic strepsirhine anterior tooth comb, but exhibit variation in their postcanine teeth that may be related to dietary differences. In this study, I examine two factors that could complicate a strictly functional interpretation of tooth form variation in two families of Malagasy primates, the Lemuridae and Indriidae. (1) Allometry may be responsible for observed variation. Body size, not specific tooth features, may be the object of selection; tooth features may vary among taxa as a consequence of differences in body size. (2) Taxonomic affiliation may “explain” variation without recourse to functional explanations. Tooth morphology among closely-related taxa may be constrained developmentally or as a result of stabilizing selection. Morphological variation between families, therefore, may not be the result of current functional differences related to physical dietary properties, but may result from past events that are lineage-specific. Morphological features from the upper and lower second molars of seven lemurid and four indriid taxa are compared. The results of this study indicate that the majority of second molar features scale isometrically. Initial separation by families is warranted by the homogeneous slopes but different elevations in analyses of covariance between families. Intrafamilial variation is considerable for lemurids, but more discrete among indriids. Functional explanations for tooth form variability should take into consideration the degree of variation within taxa. For this particular dataset, the two families should be analyzed separately, and, because of the considerable overlap of subspecies with full species among lemurids, the lowest taxonomic unit recognized should be used.
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Seasonally and site specificity of mechanical dietary patterns in two malagasy lemur families (Lemuridae and Indriidae)
International Journal of Primatology, 1996Co-Authors: Nayuta YamashitaAbstract:Relationships between tooth morphology and physical food properties are well established. Because food breakdown is initiated by the dentition, one may posit that variations in tooth form are related functionally to the physical demands placed on them by the diet. Yet classification of diets as leaves, fruits , and insects does not adequately describe foods in mechanically significant ways. Furthermore, physical dietary properties have not been well quantified. I describe patterns of two physical food properties — hardness and shear strength — in the diets of five lemur taxa in Madagascar— Propithecus diadema edwardsi, Lemur fulvus rufus, and Lemur rubriventer— in the rain forest site of Ranomafana National Park and Propithecus v. verreauxi and Lemur catta at the dry forest site of Beza Mahafaly special reserve. I compared mean plant values for each lemur taxon, the most stressful foods eaten and the amount of time spent feeding on each dietary item. Variation in food hardness is a site phenomenon with fluctuations within sites. Shear strength is strongly seasonal. Lemur diets, as traditionally classified, are not mechanically uniform since frugivores and folivores could be separated on the basis of the physical properties of their foods. Finally, I assign taxa to dietary categories that are mechanically descriptive and derive several predictions regarding expected tooth morphologies from them .
Kathleen M Muldoon - One of the best experts on this subject based on the ideXlab platform.
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evolutionary and phylogenetic insights from a nuclear genome sequence of the extinct giant subfossil koala lemur megaladapis edwardsi
Proceedings of the National Academy of Sciences of the United States of America, 2021Co-Authors: Stephanie Marciniak, Laurie R. Godfrey, Mehreen R Mughal, Richard J Bankoff, Heritiana D D Randrianatoandro, Brooke E Crowley, Christina M Bergey, Kathleen M MuldoonAbstract:No endemic Madagascar animal with body mass >10 kg survived a relatively recent wave of extinction on the island. From morphological and isotopic analyses of skeletal “subfossil” remains we can reconstruct some of the biology and behavioral ecology of giant lemurs (primates; up to ∼160 kg) and other extraordinary Malagasy megafauna that survived into the past millennium. Yet, much about the evolutionary biology of these now-extinct species remains unknown, along with persistent phylogenetic uncertainty in some cases. Thankfully, despite the challenges of DNA preservation in tropical and subtropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here, we present a nuclear genome sequence (∼2× coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (∼85 kg). To support the testing of key phylogenetic and evolutionary hypotheses, we also generated high-coverage nuclear genomes for two extant lemurs, Eulemur rufifrons and Lepilemur mustelinus, and we aligned these sequences with previously published genomes for three other extant lemurs and 47 nonlemur vertebrates. Our phylogenetic results confirm that Megaladapis is most closely related to the extant Lemuridae (typified in our analysis by E. rufifrons) to the exclusion of L. mustelinus, which contradicts morphology-based phylogenies. Our evolutionary analyses identified significant convergent evolution between M. edwardsi and an extant folivore (a colobine monkey) and an herbivore (horse) in genes encoding proteins that function in plant toxin biodegradation and nutrient absorption. These results suggest that koala lemurs were highly adapted to a leaf-based diet, which may also explain their convergent craniodental morphology with the small-bodied folivore Lepilemur.
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evolutionary and phylogenetic insights from a nuclear genome sequence of the extinct giant subfossil koala lemur megaladapis edwardsi
bioRxiv, 2020Co-Authors: Stephanie Marciniak, Laurie R. Godfrey, Mehreen R Mughal, Richard J Bankoff, Heritiana D D Randrianatoandro, Brooke E Crowley, Christina M Bergey, Kathleen M MuldoonAbstract:Abstract No endemic Madagascar animal with body mass >10 kg survived a relatively recent wave of extinction on the island. From morphological and isotopic analyses of skeletal ‘subfossil’ remains we can reconstruct some of the biology and behavioral ecology of giant lemurs (primates; up to ~160 kg), elephant birds (up to ~860 kg), and other extraordinary Malagasy megafauna that survived well into the past millennium. Yet much about the evolutionary biology of these now extinct species remains unknown, along with persistent phylogenetic uncertainty in some cases. Thankfully, despite the challenges of DNA preservation in tropical and sub-tropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here we present a nuclear genome sequence (~2X coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (~85kg). To support the testing of key phylogenetic and evolutionary hypotheses we also generated new high-coverage complete nuclear genomes for two extant lemur species, Eulemur rufifrons and Lepilemur mustelinus, and we aligned these sequences with previously published genomes for three other extant lemur species and 47 non-lemur vertebrates. Our phylogenetic results confirm that Megaladapis is most closely related to the extant Lemuridae (typified in our analysis by E. rufifrons) to the exclusion of L. mustelinus, which contradicts morphology-based phylogenies. Our evolutionary analyses identified significant convergent evolution between M. edwardsi and extant folivorous primates (colobine monkeys) and ungulate herbivores (horses) in genes encoding protein products that function in the biodegradation of plant toxins and nutrient absorption. These results suggest that koala lemurs were highly adapted to a leaf-based diet, which may also explain their convergent craniodental morphology with the small-bodied folivore Lepilemur.
Giuseppe Donati - One of the best experts on this subject based on the ideXlab platform.
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do functional traits offset the effects of fragmentation the case of large bodied diurnal lemur species
American Journal of Primatology, 2020Co-Authors: Timothy M Eppley, Luca Santini, Jen Tinsman, Giuseppe DonatiAbstract:Primates worldwide are faced with increasing threats making them more vulnerable to extinction. Anthropogenic disturbances, such as habitat degradation and fragmentation, are among the main concerns, and in Madagascar, these issues have become widespread. As this situation continues to worsen, we sought to understand how fragmentation affects primate distribution throughout the island. Further, because species may exhibit different sensitivity to fragmentation, we also aimed to estimate the role of functional traits in mitigating their response. We collated data from 32 large-bodied lemur species ranges, consisting of species from the families Lemuridae (five genera) and Indriidae (two genera). We fitted Generalized Linear Models to determine the role of habitat fragmentation characteristics, for example, forest cover, patch size, edge density, and landscape configuration, as well as the protected area (PA) network, on the species relative probability of presence. We then assessed how the influence of functional traits (dietary guild, home range size) mitigate the response of species to these habitat metrics. Habitat area had a strong positive effect for many species, and there were significantly negative effects of fragmentation on the distribution of many lemur species. In addition, there was a positive influence of PAs on many lemur species' distribution. Functional trait classifications showed that lemurs of all dietary guilds are negatively affected by fragmentation; however, folivore-frugivores show greater flexibility/variability in terms of habitat area and landscape complexity compared to nearly exclusive folivores and frugivores. Furthermore, species of all home range sizes showed a negative response to fragmentation, while habitat area had an increasingly positive effect as home range increased in size. Overall, the general trends for the majority of lemur species are dire and point to the need for immediate actions on a multitude of fronts, most importantly landscape-level reforestation efforts.
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predator avoidance and dietary fibre predict diurnality in the cathemeral folivore hapalemur meridionalis
Behavioral Ecology and Sociobiology, 2017Co-Authors: Timothy M Eppley, Joerg U Ganzhorn, Julia Watzek, Giuseppe DonatiAbstract:Though numerous mammalian taxa exhibit cathemerality (i.e. activity distributed across the 24-h cycle), this includes very few primates, exceptions being species from Aotinae and Lemuridae. Four non-mutually exclusive hypotheses have been proposed to explain the ultimate determinants for cathemeral activity in lemurs: thermoregulatory benefits, anti-predator strategy, competition avoidance and metabolic dietary-related needs. However, these have only been explored in the frugivorous genus Eulemur, with some species increasing nocturnality as a possible response to avoid diurnal raptors and to increase their ability to digest fibre during resource-scarce periods. Since Eulemur lack specializations for digesting bulk food, this strategy would allow for processing fibres over the full 24-h. The folivorous lemurids, i.e. genus Hapalemur, provide a divergent model to explore these hypotheses due to gastrointestinal adaptations for digesting dietary fibre and small body size compared to Eulemur. We linked continuous activity data collected from archival tags with observational behaviour and feeding data from three groups of adult Hapalemur meridionalis from January to December 2013. We tested the effects of thermoregulation, predator avoidance and the weighted proportion of digestible dietary fibre on the daily diurnal/nocturnal activity ratio using a Linear Mixed-Model. Our best-fit model revealed that increased canopy exposure and dietary fibre predicted greater diurnality. Our findings partly contrast with previous predictions for frugivorous lemurids. We propose a divergent adaptive explanation for folivorous lemurids. We suggest that the need to avoid terrestrial predators, as well as longer digestive bouts during bulk food periods, may override cathemerality in favour of diurnality in these bamboo lemurs. Southern bamboo lemurs are active throughout the 24-h day, with high proportions of dietary fibre increasing diurnality, in contrast to other cathemeral primates. They also increase diurnality on days when using areas with greater canopy exposure, potentially avoiding nocturnal predators in risky foraging areas. We suggest that folivorous lemurids may require long periods of inactivity to conserve energy and digest dietary fibre, thus limiting activity to periods of optimal foraging efficiency over the 24-h cycle.
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cathemerality in a small folivorous primate proximate control of diel activity in hapalemur meridionalis
Behavioral Ecology and Sociobiology, 2015Co-Authors: Timothy M Eppley, Joerg U Ganzhorn, Giuseppe DonatiAbstract:A non-adherence to a strict diurnal or nocturnal activity cycle is prevalent among mammals, including taxa of Lemuridae, but rare among other primates. While non-mutually exclusive ecological hypotheses attempted to explain the evolution of this activity, termed cathemerality, as either an old or a recent phenomenon, the scarcity of systematic data collected over 24 h limits our potential to explore its proximate and ultimate determinants. Among strepsirrhines, systematic studies involving only two lemurid genera (Eulemur and Lemur) have recorded this activity pattern, while fewer quantitative observations are available for other taxa. If cathemerality could be shown in most members of Lemuridae despite their different ecological adaptations, this would support the hypothesis that this trait is basal and appeared early during lemurid evolution. Here, we investigated whether the folivorous southern bamboo lemur (Hapalemur meridionalis) exhibits cathemeral activity, and determined which environmental factors influence its pattern. We deployed ten archival tags across four social groups to continuously record activity data over a 15-month period. This allowed us to generate a diurnal/nocturnal (DN) ratio for each 24-h period and assess their diel activity. Our data suggest that southern bamboo lemurs are cathemeral within Mandena; while climatic factors showed no influence, nocturnal activity increased with greater nocturnal luminance. Despite contrasting dietary niches, visual morphologies, and body sizes between Hapalemur, Eulemur, and Lemur, all three exhibit cathemerality and lunarphilia. The close phylogenetic proximity of these lemurids supports this flexible activity pattern as an ancestral trait that likely dates to the origin of the Lemuridae radiation.