Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: II. Intraspecific patterns

Based on a year-long field study in northeastern Madagascar, I summarize annual patterns of niche use (food patch size, diet, forest height, and forest site) in two sympatric lemurs, Varecia variegata rubra and Eulemur fulvus albifrons. Furthermore, I examine intraspecific patterns of niche use according to sex, season, and reproductive stage in these two lemurs that differ in terms of energetic investment in reproduction. Lemurs as a group provide a special opportunity to test hypotheses concerning sex differences in niche use. Due to their body size monomorphism and seasonal, synchronous pattern of breeding, it is possible to directly evaluate whether sex differences in diet reflect high energetic investment in reproduction by females. Results confirm the hypothesis that intraspecific variation in niche use (e.g., sex differences, seasonal differences) would be more pronounced in V. v. rubra than in E. f. albifrons, due in large measure to the former's relatively high energetic investment in reproduction: 1a) Dietary sex differences in V. v. rubra are most pronounced during costly reproductive stages and involve acquisition of low-fiber, high-protein plant foods. Females of both species consume more seasonally available low-fiber protein (young leaves, flowers) relative to conspecific males during the hot dry season, but only in V. v. rubra females is this pattern also evident during gestation and lactation. 1b) The diets of female V. v. rubra and female E. f. albifrons are more similar to each other than are the diets of conspecific males and females in the case of V. v. rubra. This is not uniformly the case for female E. f. albifrons. This finding confirms a hypothesis put forward in Vasey ([2000] Am J Phys Anthropol 112:411-431) that energetic requirements of reproductive females drive niche separation more than do the energetic requirements of males. 1c) Both species synchronize most or all of lactation with seasonal food abundance and diversity. E. f. albifrons shows a more protracted period of synchrony, and this may contribute to its wide biogeographic distribution in Madagascar. 2) Sex differences and seasonal differences in microhabitat use reflect intraspecific patterns of thermoregulation, predator avoidance, and in the case of V. v. rubra, reproduction. One important factor selecting for body size monomorphism in lemurs appears to be the tight synchrony between lactation and periods of food abundance afforded by annual, seasonal breeding.     

Niche separation in Varecia variegata rubra and Eulemur fulvus albifrons: I. Interspecific patterns

Niche separation was documented in a year-long study of Varecia variegata rubra and Eulemur fulvus albifrons on the Masoala Peninsula, Madagascar. Feeding trees were measured, and diet, forest height, and forest site were recorded at 5-min time points on focal animals. For time point data, multivariate and bivariate analysis of frequencies was employed to examine how niche dimensions vary between species according to sex, season, and reproductive stage. V. v. rubra feeds in larger trees than E. f. albifrons. V. v. rubra has a diet consisting mainly of fruit, whereas E. f. lbifrons has a more varied diet. V. v. ubra ranges mainly above 15 m in tree crowns, whereas E. f. albifrons ranges mainly below 15 m in a wide array of forest sites. Both species are largely frugivorous, but they harvest fruit in different-sized trees, in different quantities, and in different forest strata. Niche partitioning varies in tandem with seasonal shifts in climate and food availability and with reproductive stages. Seasonal shifts in forest site and forest height use are largely attributed to species-specific tactics for behavioral thermoregulation and predator avoidance. The diet of E. f. albifrons is diverse whether examined by season or reproductive stage. However, females of both species diversify their diets with more low-fiber protein than males during gestation, lactation, and the hot seasons. This pattern is most pronounced for V. v. rubra females and may be directly attributed to high energetic investment in reproduction. These results suggest that niche partitioning may be driven more by the energetic requirements of reproductive females than males.     

Activity budgets and activity rhythms in red ruffed lemurs (Varecia rubra) on the Masoala Peninsula, Madagascar: seasonality and reproductive energetics

The activity budgets and daily activity rhythms of Varecia rubra were examined over an annual cycle according to season and reproductive stage. Given the relatively high reproductive costs and patchy food resources of this species, I predicted that V. rubra would 1) travel less and feed more during seasonal resource scarcity in an attempt to maintain energy balance, and 2) show sex differences in activity budgets due to differing reproductive investment. Contrary to the first prediction, V. rubra does not increase feeding time during seasonal food scarcity; rather, females feed for a consistent amount of time in every season, whereas males feed most during the resource-rich, hot dry season. The results are consistent with other predictions: V. rubra travels less in the resource-scarce cold rainy season, and there are some pronounced sex differences, with females feeding more and resting less than males in every season and in every reproductive stage except gestation. However, there are also some provocative similarities between the sexes when activity budgets are examined by reproductive stage. During gestation, female and male activity budgets do not differ and appear geared toward energy accumulation: both sexes feed and rest extensively and travel least during this stage. During lactation, activity budgets are geared toward high energy expenditure: both sexes travel most and in equal measure, and rest least, although it remains the case that females feed more and rest less than males. These similarities between female and male activity budgets appear related to cooperative infant care. The high energetic costs of reproduction in V. rubra females may require that they allot more time to feeding year round, and that their overall activity budget be more directly responsive to seasonal climate change, seasonal food distribution, and reproductive schedules.     

Daily activity and light exposure levels for five species of lemurs at the duke lemur center

Light is the primary synchronizer of all biological rhythms, yet little is known about the role of the 24‐hour luminous environment on nonhuman primate circadian patterns, making it difficult to understand the photic niche of the ancestral primate. Here we present the first data on proximate light–dark exposure and activity–rest patterns in free‐ranging nonhuman primates. Four individuals each of five species of lemurs at the Duke Lemur Center (Eulemur mongoz, Lemur catta, Propithecus coquereli, Varecia rubra, and Varecia variegata variegata) were fitted with a Daysimeter‐D pendant that contained light and accelerometer sensors. Our results reveal common as well as species‐specific light exposure and behavior patterns. As expected, all five species were more active between sunrise and sunset. All five species demonstrated an anticipatory increase in their pre‐sunrise activity that peaked at sunrise with all but V. rubra showing a reduction within an hour. All five species reduced activity during mid‐day. Four of the five stayed active after sunset, but P. coquereli began reducing their activity about 2 hours before sunset. Other subtle differences in the recorded light exposure and activity patterns suggest species‐specific photic niches and behaviors. The eventual application of the Daysimeter‐D in the wild may help to better understand the adaptive evolution of ancestral primates. Am J Phys Anthropol 153:68–77, 2014. © 2013 Wiley Periodicals, Inc.     

Sex ratio affects sex-specific innovation and learning in captive ruffed lemurs (Varecia variegata and Varecia rubra)

Recent years have witnessed extensive research into problem solving and innovation in primates, yet lemurs have not been subjected to the same level of attention as apes and monkeys, and the social context in which novel behavior appears has rarely been considered. We gave novel foraging puzzlebox devices to seven groups of ruffed lemurs (Varecia variegata and Varecia rubra) to examine the factors affecting rates of innovation and social learning. We found, across a range of group sex ratios, that animals of the less-represented sex were more likely to contact and solve the puzzlebox sooner than those of the more-represented sex. We established that while some individuals were able to solve the puzzleboxes there was no evidence of social learning. Our findings are consistent with previously reported male deference as a sexual strategy, but we conclude that the need for male deference diminishes when, within a group, males are rare.     

云南下关地区大绒鼠（Eothenomys miletus）体温调节和产热特征日节律的初步研究

为探讨横断山区小型哺乳动物体温调节和产热特征的日节律,对横断山区固有种大绒鼠（Eothenomys mile-tus）在24h中4个时间段（05：00—07：00、11：00—13：00、17：00—19：00、23：00—01：00）的体温、基础代谢率、非颤抖性产热进行了测定。结果显示大绒鼠的体温、基础代谢率、非颤抖性产热在24h内具有节律性波动,且变化趋势基本同步;各生理参数的最高值和最低值都分别出现在05：00—07：00和11：00—13：00时间段。结果表明,横断山区大绒鼠的基础代谢率、非颤抖性产热在其体温调节的日节律中起到了重要作用,同时,大绒鼠其夜间体温调节、产热特征显著高于白天,以适应横断山日温差大、食物资源丰富的特征。     

Interseasonal variation in the circadian rhythms of locomotor activity and temperature selection in sleepy lizards, <Emphasis Type="Italic">Tiliqua rugosa</Emphasis>

Few studies in non-mammalian vertebrates have examined how various effectors of the circadian system interact. To determine if the daily locomotor and behavioural thermoregulatory rhythms of Tiliqua rugosa are both controlled by the circadian system in different seasons, lizards were tested in laboratory thermal gradients in four seasons and in constant darkness. Circadian rhythmicity for both rhythms was present in each season, being most pronounced in spring and summer and least evident in autumn. Most lizards displayed a unimodal locomotor activity pattern across all seasons. However, some individuals presented a bimodal locomotor activity pattern in spring and summer. Seasonal variations in the phase relationships of both rhythms to the light:dark (LD) cycle were demonstrated. No seasonal differences in the free-running period lengths of either rhythm were detected, raising the possibility that a single circadian pacemaker drives both rhythms in this species. Our present results demonstrate that both rhythms are similarly controlled by the circadian system in each season. Although seasonal variations in the thermal preferences of reptiles both in the field and laboratory have previously been well documented, this study is the first to demonstrate circadian rhythms of temperature selection in a reptile species in each season.     

Hematology and serum chemistry values of juvenile and adult ruffed lemurs (Varecia variegata)

Hematologic and serum chemistry values are presented for adult and juvenile red ruffed lemurs (Varecia variegata rubra) and black and white ruffed lemurs (Varecia variegata variegata) maintained in a zoological collection. Hematologic and serum chemical values are compared between age groups and subspecies and with other primate species. Elevated hematocrit, total protein, and serum albumin values were noted. Significant differences in cholesterol, total protein, and serum albumin values between the two age groups are discussed.     

Modulation of circadian clocks by nutrients and food factors

Daily activity rhythms that are dominated by internal clocks are called circadian rhythms. A central clock is located in the suprachiasmatic nucleus of the hypothalamus, and peripheral clocks are located in most mammalian peripheral cells. The central clock is entrained by light/dark cycles, whereas peripheral clocks are entrained by feeding cycles. The effects of nutrients on the central and peripheral clocks have been investigated during the past decade and much interaction between them has come to light. For example, a high-fat diet prolongs the period of circadian behavior, a ketogenic diet advances the onset of locomotor activity rhythms, and a high-salt diet advances the phase of peripheral molecular clocks. Moreover, some food factors such as caffeine, nobiletin, and resveratrol, alter molecular and/or behavioral circadian rhythms. Here, we review nutrients and food factors that modulate mammalian circadian clocks from the cellular to the behavioral level.     

Circadian and ultradian activity rhythms in manatee (Trichechus manatus manatus) in captivity

In this study, we show temporal organization of activity patterns in larger temporal series recording. The objective of this study was to determine the temporal pattern of the rest-activity rhythm in manatee (Trichechus manatus manatus) in captivity. Activity recordings were programmed from August 2010 to September 2011 with actimetry devices, and behavior recordings were conducted in dry and rainy seasons. We showed that the marine manatee presents a complex temporal organization, in which the rest-activity rhythm comprises several frequencies with a predominant circadian component and multiple ultradian components. Our results indicate that the animals were more active during the day with respect to the night. The temporal organization of this cycle entails multiple frequencies that include ultradian rhythms, which may be expressions generated by physiological needs, such as food availability and thermoregulatory requirements. These patterns should be taken into consideration for future studies of biological rhythms in manatee.     

Spatial and trophic niche differentiation in two sympatric lizards (Tropidurus torquatus and Cnemidophorus ocellifer) with different foraging tactics

Abstract In a ‘restinga’ habitat of southeastern Brazil, we studied the food habits and the microhabitat use of two lizards with distinct foraging modes: the tropidurid Tropidurus torquatus, a sit-and-wait predator, and the teiid Cnemidophorus ocellifer, a wide forager. The diet of the two species differed strongly, indicating a low level of similarity in their trophic niche. The sit-and-wait predator fed mainly on mobile prey, whereas the wide forager fed mainly on sedentary prey (larvae). The spatial niche breadth of T. torquatus was larger than that of C. ocellifer. Despite interspecific differences, the two species overlapped greatly in micro-habitat use. The data indicate that at Linhares the two lizard species differed more in food resources than in microhabitat, and that most of the food differences reflect the foraging patterns of the species.     

Disruption of Daily Rhythms by High-Fat Diet Is Reversible

In mammals a network of circadian clocks coordinates behavior and physiology with 24-h environmental cycles. Consumption of high-fat diet disrupts this temporal coordination by advancing the phase of the liver molecular clock and altering daily rhythms of eating behavior and locomotor activity. In this study we sought to determine whether these effects of high-fat diet on circadian rhythms were reversible. We chronically fed mice high-fat diet and then returned them to low-fat chow diet. We found that the phase of the liver PERIOD2::LUCIFERASE rhythm was advanced (by 4h) and the daily rhythms of eating behavior and locomotor activity were altered for the duration of chronic high-fat diet feeding. Upon diet reversal, the eating behavior rhythm was rapidly reversed (within 2 days) and the phase of the liver clock was restored by 7 days of diet reversal. In contrast, the daily pattern of locomotor activity was not restored even after 2 weeks of diet reversal. Thus, while the circadian system is sensitive to changes in the macronutrient composition of food, the eating behavior rhythm and liver circadian clock are specifically tuned to respond to changes in diet.     

Annual and circadian activity patterns of badgers (Meles meles) in Białowieża Primeval Forest (eastern Poland) compared with other Palaearctic populations

Aim The annual and circadian rhythms and duration of activity of Eurasian badger Meles meles (Linnaeus 1758) were studied in a low‐density population inhabiting the primeval woodland in the European temperate zone. Results were compared with available data from the literature on seasonal changes in body mass and winter inactivity of badgers from across the Palaearctic region. Location Field work was carried out in Bia?owie?a Primeval Forest, eastern Poland. Biogeographical variation was reviewed based on twenty‐three localities in the Palaearctic region (from Western Europe to Central Siberia). Methods Thirteen badgers were radio‐collared in 1997–2001. Their circadian activity was sampled by 24‐h sessions of continuous radio‐tracking with location taken at 15‐min intervals. Annual activity was studied by radio‐tracking and inspections of setts. Earthworm (badgers’ main food) biomass was estimated in four types of habitats throughout the year. Results Badgers were nocturnal with one long bout of activity. Their rhythms of diel activity differed between spring and autumn, and between adult and subadult individuals. On average, badgers emerged from setts at 19:00 hours and returned to them at 03:42 hours. The highest level of activity was recorded between 20:00 and 03:00 hours. Duration of daily activity was, on average, 8.2 h day^?1, but varied significantly between seasons. The seasonal changes were inversely related to the abundance of earthworms. Duration of activity also depended on daily temperature, especially in the cold season. In winter, badgers stayed inactive for an average of 96 days per year. In autumn, they built fat reserves and their body mass nearly doubled compared with the spring values. The literature review on annual cycle of activity and body mass changes in Eurasian badgers showed that fat storage and duration of winter sleep strongly depended on climate (best approximated by January mean temperature). In regions with warm climates, badgers were active year round and their body mass changed only slightly, while in regions with severe winters badgers increased their body mass twofold from spring to autumn, and stayed inactive for as long as 6 months per year. Main conclusion We propose that, in the temperate and boreal zones of the Palaearctic region, the ultimate determinant of biogeographical variation in badgers’ annual activity is the winter shortage of earthworms, which are the main component of badger diet.     

Seasonal Variations and Diurnal Rhythms of Gonadotropin (GtH2) Levels in Immature and Mature Female Carp (Cyprinus carpio L)

Daily changes of gonadotropin (GtH2) blood levels of immature and mature carp females were investigated in four seasons during the year: spring, summer (spawning period) and in autumn and winter (“resting” period). GtH2 levels were measured using ELISA method. The maturity stage of oocytes was determined histologically and on the base of germinal vesicle position in the oocyte. It appeared shown that GtH2 levels changed daily during the year in the range of 3.56 to 6.61 ng/ml, regardless of the state of ovarian maturity. Cosinor analysis and ellipse of errors revealed the presence of a circadian rhythm in GtH2 levels only in mature females during the reproduction period (L:D=16:8, water temp. 20 to 22°C).     

邦亮东黑冠长臂猿日食性与活动节律的季节性变化

日食性变化和活动节律是动物行为的重要方面,通过对日食性变化与活动节律的研究,可以了解食物、温度和光照时间等环境因素的变化对动物行为的影响,以及动物在行为上的应对策略。2009 年1 -12 月,在广西靖西县邦亮东部黑冠长臂猿自治区级自然保护区内,采用瞬时扫描取样法对2 群东黑冠长臂猿觅食行为和活动节律进行了研究。结果显示,东黑冠长臂猿的活动和食性在旱季和雨季都具有明显的节律。鸣叫只发生在12:00之前,但旱季的鸣叫时间偏晚。在日节律上,东黑冠长臂猿在离开过夜树后和进入过夜树前各有一个取食高峰,07:00 喜欢取食果实和无花果,16:00 也选择更多的果实,但无花果较少,13:00 - 15:00 取食更多的叶和芽。在10:00 - 12:00,其用于休息和社会活动的时间增加。在雨季,东黑冠长臂猿以果实和无花果为主要食物,并且花大量时间觅食无脊椎动物;但在旱季,其食物以叶和芽为主。与之相适应,东黑冠长臂猿在旱季通过减少移动增加休息来节约能量开支和应对低温,同时它们增加取食的时间以获得等价的能量和营养。雨季时社会行为的比例明显高于旱季,而且其高峰出现在08:00 - 10:00,但旱季社会行为主要出现在11:00 - 14:00。在雨季东黑冠长臂猿没有出现休息高峰,相反在旱季10:00 左右出现一个明显的休息高峰。上述行为节律体现了东黑冠长臂猿对环境季节性变化的良好适应,使其能够在寒冷并且退化的喀斯特森林中生存繁衍。     

同域分布鼬獾和食蟹獴活动节律的比较

为探明同域分布的鼬獾（Melogale moschata）和食蟹獴（Herpestes urva）的日活动节律、时间生态位及其两者共存机制,于2016年12月至2017年12月,在广西弄岗国家级自然保护区开展红外相机监测获取数据,后采用核密度估计（Kernel density estimation）和重叠指数（Coefficient of overlap）对该地区的鼬獾和食蟹獴进行了研究。结果表明：鼬獾属于典型的夜行性动物,其日活动模式为双峰型,活动峰值出现在01：00—05：00和21：00—24：00;与雨季相比,旱季的活动峰值均提前1 h,活动高峰期延长3 h。食蟹獴为典型昼行性动物,其日活动模式为单峰型,活动峰值出现在11：00—18：00,与雨季相比,旱季活动高峰期提前并延长1 h。两者间的日活动模式重叠指数较低（Δ=0.17）,但旱季（Δ=0.22）高于雨季（Δ=0.12）。两者主要通过改变时间生态位来避免对食物资源和领域的竞争,从而实现共存。     

Circadian Rhythm Variation in Attempted Suicide by Deliberate Self-Poisoning, and in Completed Suicide, in Central Nepal

Daily rhythms are described in almost every variable that can be measured, including suicide rate. The present study aims to find if circadian rhythm exist in suicidal poisoning and completed suicide due to poisoning in central Nepal. The study included all the attempted suicide cases admitted in Patan Hospital and all the completed suicide cases by poisoning reported to Kathmandu District Police during March 2002 to April 2003. The time was grouped into 24 increments of 1 hour. The data were analysed by Kolmogorov-Smirnov test and cosinor analysis. The circadian rhythm of attempted suicide by deliberate self poisoning exhibits a peak at 18:00 h, whereas no circadian rhythm is seen in completed suicides by poisoning although it is bimodal in distribution (6:00-12:00 and 15:00-20:00) with peaks at 7:00 and 18:00 h.     

大绒鼠及高山姬鼠体温调节和蒸发失水的日节律

为比较横断山区同域分布物种大绒鼠(Eothenomys miletus)和高山姬鼠(Apodemus chevrieri)的日节律特征,对两种鼠在24 h中4个时间段(04:00～06:00时、10:00～12:00时、16:00～18:00时和22:00～24:00时)的体温和蒸发失水进行了测定.结果显示,大绒鼠、高...     

Seasonal Variations and Diurnal Rhythms of Gonadotropin (GtH2) Levels in Immature and Mature Female Carp (Cyprinus carpio L)

Daily changes of gonadotropin (GtH2) blood levels of immature and mature carp females were investigated in four seasons during the year: spring, summer (spawning period) and in autumn and winter (“resting” period). GtH2 levels were measured using ELISA method. The maturity stage of oocytes was determined histologically and on the base of germinal vesicle position in the oocyte. It appeared shown that GtH2 levels changed daily during the year in the range of 3.56 to 6.61 ng/ml, regardless of the state of ovarian maturity. Cosinor analysis and ellipse of errors revealed the presence of a circadian rhythm in GtH2 levels only in mature females during the reproduction period (L:D=16:8, water temp. 20 to 22°C).     

Chronobiological background to cathemerality: circadian rhythms in Eulemur fulvus albifrons (Prosimii) and Aotus azarai boliviensis (Anthropoidea)

Cathemeral activity, in which the animals' motor activity is almost evenly distributed throughout the dark and the light portion of the day, has been described in various lemur genera (Eulemur, Hapalemur) and in the owl monkey Aotus azarai of the Argentinean Chaco. Proximate and ultimate factors responsible for this behaviour are still being debated. However, the chronobiological background of the behaviour has largely been ignored. We studied E. fulvus albifrons and A. a. boliviensis under controlled laboratory conditions to assess whether their activity rhythm is endogenously regulated by a circadian timing system that obeys general rules found in other mammals, or whether there are characteristic differences. To this end, we carried out long-term activity recordings on individuals of both subspecies kept under constant light and various light-dark cycles (LDs) using a PC-controlled electro-acoustic device in combination with telemetric body temperature measurements. Both subspecies developed free-running circadian activity and body temperature rhythms with periods deviating from 24 h in constant light, and LDs turned out to be the most efficient Zeitgeber synchronizing this endogenous rhythmicity to the external 24-hour day. The luminosity prevailing during the dark time of the LD had a decisive effect on levels of activity in the lemurs and induced strong masking effects on their circadian activity pattern. The results indicate that, from a chronobiological viewpoint, both species should be considered as dark active primates. Their diel activity rhythm is regulated by a normally responding circadian timing system and strong activity inhibiting or enhancing direct effects of light intensity. Thus, hypotheses on proximate and/or ultimate factors of cathemerality in primates must also consider its circadian background.