草食性小型哺乳动物的食粪行为

食粪行为广泛存在于草食性中小型哺乳动物中,是特指动物取食由盲肠内容物所形成的粪便的行为。这些动物具有特殊的结肠分离机制,能够产生两种不同的粪便。食粪行为延长了食物在消化道中的平均滞留时间;提高了对高纤维食物的消化率;弥补了食物中氨基酸和维生素的缺乏,满足了动物对这些营养物质的需求;是动物消化过程中的一个特殊组成部分。食粪行为的节律性是动物对取食和食粪的风险权衡的结果。食粪行为的发展是与动物草食性的特点紧密相关的,是动物对身体较小、食物质量低和天敌威胁等不利因素适应的结果。本对这些方面的研究进展进行了综述。     

Nutritional responses to different diet quality in the subterranean rodent Ctenomys talarum (tuco-tucos)

Nutritional response to different diet quality was examined in the subterranean rodent Ctenomys talarum (tuco-tuco). Animals maintained in captive conditions were fed with three plant species that differed in their fibre content. Tuco-tucos showed the ability to perform adjusts in short time lapse in response to diet quality; food ingestion, egestion and feces ingestion changed in animals under different plant species diets. Time budget, mainly time devoted to feeding and activity accompanied such changes. Coprophagy was practiced along the day and night following the arrhythmic activity pattern found for this species. Feces reingestion was not associated to resting. Furthermore, it was observed during fresh food ingestion, being pellets chewed. Soft and hard feces differed in morphological and nutritional characteristics.     

Coprophagy in female mice during pregnancy and lactation

Coprophagy in female mice was observed predominantly in the reproductive stage. Female mice exhibited coprophagy more frequently during pregnancy and ingested larger amounts of feces during pregnancy and lactation than when they were not pregnant. Feces were found to be rich in vitamin B12 and folic acid. However, there were no marked fluctuations in the levels of either vitamin in the feces during pregnancy or lactation as compared with levels when animals were not pregnant. Acceleration of coprophagy during pregnancy and lactation seemed to correlate with the increased nutritional requirements of females during the reproductive stage.     

A biogeographical perspective on the variation in mouse lemur density throughout Madagascar

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Seasonal Effects on Sleeping Site Ecology in a Nocturnal Pair-Living Lemur (Avahi occidentalis)

Seasonal changes may have a strong effect on the safety of sleeping sites in arboreal primates. For example, changes in vegetation thickness may impact predation risk and energy expenditure related to thermoregulation. We investigated how seasonality influenced sleeping site characteristics and usage pattern in an arboreal primate living in a highly seasonal environment. The western woolly lemur (Avahi occidentalis) lives in the dry deciduous forest of northwestern Madagascar, where leaf coverage greatly varies across the year. We examined the hypothesis that these lemurs change their sleeping site behavior dependent on season. We collected data on sleeping site height and location, and characterized usage patterns in six radiotagged pairs between May and December 2008. During the late dry season, pairs preferentially slept in the middle part of a tree. In contrast, there was no height preference during the early rainy season. The lemurs used more sleeping sites during the early rainy than during the late dry season and stayed more days at the same sleeping tree in the late dry season. Our findings support the hypothesis that season affects sleeping site selection in an arboreal primate species living in a highly seasonal environment. During the late dry season, western woolly lemurs are particularly conspicuous to hunters and we therefore suggest a better monitoring of the forest in this season to guarantee their future survival.     

The Effects of Climate Seasonality on Behavior and Sleeping Site Choice in Sahamalaza Sportive Lemurs, <Emphasis Type="Italic">Lepilemur sahamalaza</Emphasis>

Temperature, rainfall, and resource availability may vary greatly within a single year in primate habitats. Many primate species show behavioral and physiological adaptations to this environmental seasonality, including changes to their diets and activity. Sahamalaza sportive lemurs (Lepilemur sahamalaza) inhabit the northwest of Madagascar and have been studied only during the dry, colder period of the year. We investigated potential effects of climate seasonality on this species by collecting behavioral data between October 2015 and August 2016, encompassing both the warmer wet and the colder dry seasons. We collected 773.15 hours of behavioral data on 14 individual sportive lemurs to investigate year-round activity budgets, ranging behavior, and sleeping site locations. Additionally we recorded temperature and rainfall data at our study site to describe the environmental conditions during the study period. The study individuals significantly decreased their time spent traveling and increased their time spent resting in the dry season compared to the wet season. Although home range size and path lengths did not differ over the study period, sleeping locations were significantly different between seasons as the lemurs focused on more confined areas in colder periods. Overall, the results indicate that Sahamalaza sportive lemur behavior varies with season, in line with reports for other primates.     

Conservation biology of Malagasy strepsirhines: a phylogenetic approach

The phylogenetic diversity of extant lemurs represents one of the most important but least studied aspects of the conservation biology of primates. The phylogenetic diversity of a species is inversely proportional to the relative number and closeness of its phylogenetic relatives. Phylogenetic diversity can then be used to determine conservation priorities for specific biogeographic regions. Although Malagasy strepsirhines represent the highest phylogenetic diversity among primates at the global level, there are few phylogenetic data on species-specific and regional conservation plans for lemurs in Madagascar. Therefore, in this paper the following questions are addressed for extant lemurs: 1) how does the measure of taxonomic uniqueness used by Mittermeier et al. (1992 Lemurs of Madagascar; Gland, Switzerland: IUCN) equate with an index of phylogenetic diversity, 2) what are the regional conservation priorities based on analyses of phylogenetic diversity in extant lemurs, and 3) what conservation recommendations can be made based on analyses of phylogenetic diversity in lemurs? Taxonomic endemicity standardized weight (TESW) indices of phylogenetic diversity were used to determine the evolutionary component of biodiversity and to prioritize regions for conserving lemur taxa. TESW refers to the standardization of phylogenetic diversity indices for widespread taxa and endemicity of species. The phylogenetic data came from recent genetic studies of Malagasy strepsirhines at the species level. Lemur species were assigned as being either present or absent in six biogeographic regions. TESW indices were combined with data on lemur complementarity and protected areas to assign conservation priorities at the regional level. Although there were no overall differences between taxonomic ranks and phylogenetic rankings, there were significant differences for the top-ranked taxa. The phylogenetic component of lemur diversity is greatest for Daubentonia madagascariensis, Allocebus trichotis, Lepilemur septentrionalis, Indri indri, and Mirza coquereli. Regional conservation priorities are highest for lemurs that range into northeast humid forests and western dry forests. Expansion of existing protected areas in these regions may provide the most rapid method for preserving lemurs. In the long term, new protected areas must be created because there are lemur species that: 1) are not found in existing protected areas, 2) exist only in one or two protected areas, and 3) are still being discovered outside the current network of protected areas. Data on the population dynamics and feeding ecology of phylogenetically important species are needed to ensure that protected areas adequately conserve lemur populations in Madagascar.     

Reingestion of feces in rodents and its daily rhythmicity

Summary The ingestion of feces is widespread among rodent species and is an extensively employed component of the repertoire of feeding behaviors in some species. Coprophagy is thus a significant consideration in the nutrition and dietary ecology of many rodents. As certain fecal pellets pass from the anus, they are taken up directly into the mouth, chewed, and swallowed. The nocturnally active herbivorous kangaroo rat Dipodomys microps ingests about 1/4 of the feces it produces daily and the daily pattern of reingestion shows a consistent rhythm. For about 8 h of the daytime, during the non-foraging, resting phase of the day, D. microps reingests all fecal pellets produced; during the remainder of the day it leaves all feces produced. The reingested feces contain more nitrogen and water, and less inorganic ions than the non-reingested feces. The extent of reingestion varies among rodent species in relation to diet, and coprophagy is more important in the more herbivorous species. The granivorous kangaroo rat D. merriami ingests feces rarely. The herbivorous vole Microtus californicus ingests about 1/4 of its feces, as does D. microps. However, in contrast to D. microps, M. californicus shows a series of rhythmic, short-term (one to several hour duration) alternations between reingestion and non-reingestion during the course of the day and night. This pattern correlates with the pattern of foraging in M. californicus, which extends over both night and day.     

Use of Vocal Fingerprinting for Specific Discrimination of Gray (Microcebus murinus) and Rufous Mouse Lemurs (Microcebus rufus)

Advertisement calls are often important noninvasive tools for discriminating cryptic species and for assessing specific diversity and speciation patterns in nature. We investigated the contribution of these calls to uncover specific diversity in nocturnal Malagasy lemurs. We compared sexual advertisement and predator advertisement calls of two mouse lemur species, western gray and eastern rufous mouse lemurs (Microcebus murinus and M. rufus, respectively) living in two contrasting habitats (dry deciduous vs. rain forest), and analyzed them statistically. Both species emitted several highly variable whistle calls in the context of predator-avoidance. Intrapopulation variation was high and overlapped interspecific variation. Sexual advertisement calls, given in the mating context, displayed a totally distinct, species-specific acoustic structure. Whereas gray mouse lemurs produced rapidly multifrequency modulated, long trill calls, rufous mouse lemurs gave slowly frequency-modulated short chirp calls. Our results suggest specific status for gray and rufous mouse lemurs and indicate the importance of predation and social needs in shaping vocal communication.     

On the possible adaptive value of coprophagy in free-ranging chimpanzees

Coprophagy occurred during major periods of feeding on fruits of Dialium spp. (Caesalpiniaceae) in a group of orphaned chimpanzees released in Conkouati Douli National Park, Republic of Congo. Since stress, boredom or food scarcity could not explain coprophagy according to our daily behavioral and veterinary control observations, we suggest that Dialium seeds were the item of interest in the feces. Two types of Dialium seeds were commonly found in the feces after chimpanzees swallowed the mesocarp and whole seeds together. These seeds were either whole and hard or whole/broken and soft imbibed. A mechanical and/or chemical effect of the gut passage may enable the chimpanzees to chew and ingest the seeds, thus providing nutritional intake.     

Comparison of serum iron, total iron binding capacity, ferritin, and percent transferrin saturation in nine species of apparently healthy captive lemurs

Lemurs kept in captivity have been reported to be highly prone to accumulate excessive amounts of iron in tissues (hemosiderosis). Diagnosis of the condition is most commonly made during a postmortem examination because an antemortem diagnosis requires a liver biopsy, a procedure that may not be well tolerated by all animals. The lack of a noninvasive method to evaluate iron status in captive lemurs limits investigators' ability to effectively screen animals for the presence of hemosiderosis, and to detect the condition early when treatment protocols are most effective. This study was conducted in an effort to provide data regarding iron analyte values in healthy captive lemurs of multiple species. The relationship of various iron-related metabolites was evaluated in 177 clinically normal lemurs of nine different species. Serum iron (sI), total iron binding capacity (TIBC), and ferritin concentration were measured directly and the percent transferrin saturation (TS) was calculated. Significant differences in various iron metabolites were observed among several species, suggesting that normal reference values for iron metabolites in lemurs may need to be developed on a species by species basis.     

Olfactory predator recognition in the brown mouse lemur (Microcebus rufus) in Ranomafana National Park,Madagascar

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.     

The influence of growth patterns on sexual size monomorphism in lemurs

The lack of sexual size dimorphism among lemurs is puzzling given the high degree of polygyny in this clade. It has been proposed that the unique ecological conditions of Madagascar favour rapid completion of growth, limiting the opportunities for bimaturism and sexual size dimorphism in lemurs. Using recently compiled large data sets on many species across the lemur clade, I examined the prevalence of sexual size monomorphism of body mass among lemurs and tested the hypothesis that limited growth durations constrain sexual size dimorphism. I used segmented regression analyses to accurately model growth in each species. The majority of species analysed exhibited a period of rapid growth followed by a distinct period of slow growth prior to attainment of adult body mass. Whereas the first period of growth was constrained by the need to attain the majority of adult body mass prior to the onset of the infant's first dry season, the subsequent period of slow growth was unconstrained and sufficiently long to promote sexual bimaturism. Sex differences in the duration and rate of growth during this second growth phase appeared to account for the sexual size dimorphism exhibited by three lemur species. Therefore, constraints on growth processes do not limit sexual size dimorphism in lemurs, and other explanations for the prevalence of sexual size monomorphism in this clade should be examined. The importance of considering ontogeny in future investigations of sexual size monomorphism in lemurs is highlighted.     

Use of Mangroves by Lemurs

Despite an increasing recognition of the ecosystem services provided by mangroves, we know little about their role in maintaining terrestrial biodiversity, including primates. Madagascar’s lemurs are a top global conservation priority, with 94 % of species threatened with extinction, but records of their occurrence in mangroves are scarce. I used a mixed-methods approach to collect published and unpublished observations of lemurs in mangroves: I carried out a systematic literature search and supplemented this with a targeted information request to 1243 researchers, conservation and tourism professionals, and others who may have visited mangroves in Madagascar. I found references to, or observations of, at least 23 species in 5 families using mangroves, representing >20% of lemur species and >50% of species whose distributions include mangrove areas. Lemurs used mangroves for foraging, sleeping, and traveling between terrestrial forest patches, and some were observed as much as 3 km from the nearest permanently dry land. However, most records were anecdotal and thus tell us little about lemur ecology in this habitat. Mangroves are more widely used by lemurs than has previously been recognized and merit greater attention from primate researchers and conservationists in Madagascar.     

Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar

Hybrid zones in ecotones can be useful model systems for the study of evolutionary processes that shape the distribution and discreteness of species. Such studies could be important for an improved understanding of the complex biogeography of Madagascar, which is renowned for its outstanding degree of small-scale endemism. Certain forest remnants in central Madagascar indicate that transitional corridors across the island could have connected microendemics in different forest types in the past. Evolutionary processes in such corridors are difficult to study because most of these corridors have disappeared due to deforestation in central Madagascar. We studied a hybrid zone in one of the few remaining ecotonal corridors between dry and humid forests in Madagascar, which connects two species of mouse lemurs, Microcebus griseorufus in dry spiny forest and Microcebus murinus in humid littoral forest. We sampled 162 mouse lemurs at nine sites across this boundary. Morphometric analyses revealed intermediate morphotypes of many individuals in transitional habitat. Bayesian clustering of microsatellite genotypes and assignment tests yielded evidence for a mixed ancestry of mouse lemurs in the ecotone, where we also observed significant linkage disequilibria and heterozygote deficiency. In contrast to these observations, mitochondrial haplotypes displayed a sharply delimited boundary at the eastern edge of spiny forest, which was noncoincident with the signals from microsatellite data. Among several alternative scenarios, we propose asymmetric nuclear introgression due to male-biased dispersal, divergent environmental selection, and an expansion of dry spiny forest in the course of aridification as a probable explanation of our observations.     

Tamarind tree seed dispersal by ring-tailed lemurs

In Madagascar, the gallery forests of the south are among the most endangered. Tamarind trees (Tamarindus indica) dominate these riverine forests and are a keystone food resource for ring-tailed lemurs (Lemur catta). At Berenty Reserve, the presence of tamarind trees is declining, and there is little recruitment of young trees. Because mature tamarinds inhibit growth under their crowns, seeds must be dispersed away from adult trees if tree recruitment is to occur. Ring-tailed lemurs are likely seed dispersers; however, because they spend much of their feeding, siesta, and sleeping time in tamarinds, they may defecate a majority of the tamarind seeds under tamarind trees. To determine whether they disperse tamarind seeds away from overhanging tamarind tree crowns, we observed two troops for 10 days each, noted the locations of feeding and defecation, and collected seeds from feces and fruit for germination. We also collected additional data on tamarind seedling recruitment under natural conditions, in which seedling germination was abundant after extensive rain, including under the canopy. However, seedling survival to 1 year was lower when growing under mature tamarind tree crowns than when growing away from an overhanging crown. Despite low fruit abundance averaging two fruits/m³ in tamarind crowns, lemurs fed on tamarind fruit for 32% of their feeding samples. Daily path lengths averaged 1,266 m, and lemurs deposited seeds throughout their ranges. Fifty-eight percent of the 417 recorded lemur defecations were on the ground away from overhanging tamarind tree crowns. Tamarind seeds collected from both fruit and feces germinated. Because lemurs deposited viable seeds on the ground away from overhanging mature tamarind tree crowns, we conclude that ring-tailed lemurs provide tamarind tree seed dispersal services.     

Extinction and ecological retreat in a community of primates

The lemurs of Madagascar represent a prodigious adaptive radiation. At least 17 species ranging from 11 to 160 kg have become extinct during the past 2000 years. The effect of this loss on contemporary lemurs is unknown. The concept of competitive release favours the expansion of living species into vacant niches. Alternatively, factors that triggered the extinction of some species could have also reduced community-wide niche breadth. Here, we use radiocarbon and stable isotope data to examine temporal shifts in the niches of extant lemur species following the extinction of eight large-bodied species. We focus on southwestern Madagascar and report profound isotopic shifts, both from the time when now-extinct lemurs abounded and from the time immediately following their decline to the present. Unexpectedly, the past environments exploited by lemurs were drier than the protected (albeit often degraded) riparian habitats assumed to be ideal for lemurs today. Neither competitive release nor niche contraction can explain these observed trends. We develop an alternative hypothesis: ecological retreat, which suggests that factors surrounding extinction may force surviving species into marginal or previously unfilled niches.     

Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a malagasy primate community

Understanding the mechanisms maintaining local species richness is a major topic in tropical ecology. In ecological communities of Madagascar, primates represent a major part of mammalian diversity and, thus, are a suitable taxon to study these mechanisms. Previous research suggested that ecological niche differentiation facilitates the coexistence of lemurs. However, detailed data on all species making up diverse local primate assemblages is rarely available, hampering community‐wide tests of niche differentiation among Malagasy mammals. Here, we took an indirect approach and used stable isotopes as long‐term indicators of individuals' diets to answer the question of whether trophic patterns and food‐related mechanisms stabilize coexistence in a species‐rich lemur community. We analyzed stable carbon and nitrogen isotopes in hair collected from eight syntopic lemurs in Kirindy Forest. We found that lemur species were well separated into trophic niches and ranged over two trophic levels. Furthermore, species were densely packed in isotopic space suggesting that past competitive interactions between species are a major structuring force of this dry forest lemur community. Results of other comparative studies on primates and our findings underline that—in contrast to communities worldwide—the structure and composition of lemur communities follow predictions of ecological niche theory. Patterns of competitive interactions might be more clearly revealed in Malagasy primate communities than elsewhere because lemurs represent a large fraction of ecologically interacting species in these communities. The pronounced trophic niche differentiation among lemurs is most likely due to intense competition in the past as is characteristic for adaptive radiations. Am J Phys Anthropol 153:249–259, 2014. © 2013 Wiley Periodicals, Inc.     

Seeing red: behavioral evidence of trichromatic color vision in strepsirrhine primates

Among primates, catarrhines (Old World monkeys and apes) andcertain platyrrhines (New World monkeys) possess trichromaticcolor vision, which might confer important evolutionary advantages,particularly during foraging. Recently, a polymorphism has beenshown to shift the spectral sensitivity of the X-linked opsinprotein in certain strepsirrhines (e.g., Malagasy lemurs); however,its behavioral significance remains unknown. We assign genotypesat the X-linked variant to 45 lemurs, representing 4 species,and test if the genetic capacity for trichromacy impacts foragingperformance, particularly under green camouflage conditionsin which red detection can be advantageous. We confirm polymorphismat the critical site in sifakas and ruffed lemurs and fail tofind this polymorphism in collared lemurs and ring-tailed lemurs.We show that this polymorphism may be linked to "behavioraltrichromacy" in heterozygous ruffed lemurs but find no comparableevidence in a single heterozygous sifaka. Despite their putativedichromatic vision, female collared lemurs were surprisinglyefficient at retrieving both red and green food items undercamouflage conditions. Thus, species-specific feeding ecologiesmay be as important as trichromacy in influencing foraging behavior.Although the lemur opsin polymorphism produced measurable behavioraleffects in at least one species, the ruffed lemur, these effectswere modest, consistent with the modest shift in spectral sensitivity.Additionally, the magnitude of these effects varied across individualsof the same genotype, emphasizing the need for combined geneticand behavioral studies of trichromatic vision. We conclude thattrichromacy may be only one of several routes toward increasedforaging efficiency in visually complex environments.     

Ecology and conservation of the crowned lemur, Lemur coronatus, at Ankarana, n. Madagascar. With notes on Sanford's lemur, other sympatrics and subfossil lemurs

Forests of Ankarana limestone massif in northern Madagascar support one of the largest and least disturbed populations of Crowned Lemurs, Lemur coronatus. This paper reports a preliminary study of the ecology of this species in the Ankarana Special Reserve conducted at the end of the dry season in 1986, with additional information collected a year later. Crowned Lemurs occur in very high densities in the semi-deciduous canopy forest and this probably represents a dry season refuge for the species. They also use more open habitats, including sparsely vegetated limestone and degraded forest. Sanford's Lemur, Lemur fulvus sanfordi, also inhabits the Ankarana forests but is most abundant in degraded habitats. Crowned and Sanford's Lemurs had similar patterns of activity, which included nocturnal travelling and feeding bouts. Crowned Lemurs proved to be unusual among Lemur species in displaying low spatial troop cohesion and a lack of obvious troop hierarchy. Stronglyoides-like enteric helminths infested about one third of Crowned Lemurs but were apparently not causing disease. Crowned Lemurs fall prey to the Fosa, Cryptoprocta ferox, and the young possibly also to the largest raptors. A total of seven living lemur species (including the very rare Propithecus diadema perrieri and Daubentonia madagascariensis) were confirmed at Ankarana by the authors, and three further species have been reported by other observers. In addition to these ten extant lemurs, four subfossil species have been discovered: three of them (Hapalemur simus, Palaeopropithecus and Mesopropithecus) by the authors. The possibility that all 14 lemurs were once sympatric is discussed. For the present, the lemurs of Ankarana are protected from hunting by local taboo. Nevertheless they are under severe threat from habitat destruction, despite Ankarana's Special Reserve status. Given the very restricted distributions of Crowned and Sanford's Lemurs, both must be considered as threatened with extinction.