The auths have no conflict of interest to declare.

Predators directly impact prey populations through lethal encounters, but understanding nonlethal, indirect effects is also critical because foraging animals often face trade-offs between predator avoidance and energy intake. Quantifying these indirect effects can be difficult even when it is possible to monitor individuals that regularly interact. Our goal was to understand how movement and resource selection of a predator (wolves; Canis lupus) influence the movement behavior of a prey species (moose; Alces alces). We tested whether moose avoided areas with high predicted wolf resource use in two study areas with differing prey compositions, whether avoidance patterns varied seasonally, and whether daily activity budgets of moose and wolves aligned temporally. We deployed GPS collars on both species at two sites in northern Minnesota. We created seasonal resource selection functions (RSF) for wolves and modeled the relationship between moose first-passage time (FPT), a method that discerns alterations in movement rates, and wolf RSF values. Larger FPT values suggest rest/foraging, whereas shorter FPT values indicate travel/fleeing. We found that the movements of moose and wolves peaked at similar times of day in both study areas. Moose FPTs were 45% lower in areas most selected for by wolves relative to those avoided. The relationship between wolf RSF and moose FPT was nonlinear and varied seasonally. Differences in FPT between low and high RSF values were greatest in winter (-82.1%) and spring (-57.6%) in northeastern Minnesota and similar for all seasons in the Voyageurs National Park ecosystem. In northeastern Minnesota, where moose comprise a larger percentage of wolf diet, the relationship between moose FPT and wolf RSF was more pronounced (ave. across seasons: -60.1%) than the Voyageurs National Park ecosystem (-30.4%). These findings highlight the role wolves can play in determining moose behavior, whereby moose spend less time in areas with higher predicted likelihood of wolf resource selection.

Amphibian populations are in decline worldwide as they face a barrage of challenges, including infectious diseases caused by ranaviruses and the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd). Here we describe seasonal dynamics of Bd and ranavirus detection in free-ranging post-metamorphic wood frogs Lithobates sylvaticus, boreal chorus frogs Pseudacris maculata/triseriata, and gray treefrogs Hyla versicolor/chrysoscelis, sampled over a 3 season gradient in Minnesota (USA) wetlands. We detected Bd in 36% (n = 259) of individuals sampled in 3 wetlands in 2014, and 33% (n = 255) of individuals sampled in 8 wetlands in 2015. We also detected ranavirus in 60% and 18% of individuals sampled in 2014 and 2015, respectively. Ranavirus and Bd were detected concurrently in 26% and 2% of animals sampled in 2014 and 2015, respectively. We report clinical signs and associated infection status of sampled frogs; of the clinical signs observed, skin discoloration was significantly associated with ranavirus infection. Using generalized estimating equations, we found that species, season, wetland, and a species × season interaction term were significant predictors of Bd detection, whereas test year approached significance as a predictor of ranavirus detection. The odds of detecting both pathogens concurrently was significantly influenced by species, season, a species × season interaction term, year, and environmental ammonia. We propose an amphibian health monitoring scheme that couples population size surveys with seasonal molecular surveys of pathogen presence. This information is crucial to monitoring the health of remaining strongholds of healthy amphibian populations, as they face an uncertain future of further anthropogenic change.

[This corrects the article DOI: 10.1093/cz/zox047.]

Ungulates that are adapted to cold climates may use bed sites as thermal refuges during summer. At the southern edge of their distribution moose Alces alces often encounter ambient summer temperatures above their upper critical temperature. Summer is also when moose increase food consumption and metabolism, which increases heat generation that must typically be lost at bed sites. To determine if moose use bed sites that enable heat loss when temperatures are hot, we randomly sampled bed sites of moose from across the entire range of ambient summer temperatures. We calculated kernel density estimates for each day and night using GPS locations collected each 20 min for an entire summer to identify bed sites. Kernel density estimates identified bed sites accurately. During the day, moose bedded under lowland forest canopies where substrates had high water content. At night, bed sites were in openings which are associated with greater browse availability and net heat loss. Lowland forests interspersed with openings should help moose to maintain thermal balance during summer. Because thermoregulatory behavior is linked with fitness, thermal refuges should be especially important in areas where moose population declines have been positively correlated with warming temperatures.

Recently, considerable intraspecific variation in the diets and ranging behavior of colobine monkeys has been described, although in most cases this has involved documenting variation between, not within, sites. Some African colobines, such as guerezas (Colobus guereza), are relatively abundant in disturbed habitats that are very heterogeneous, raising the intriguing possibility that even groups with overlapping home ranges may exhibit large behavioral differences. If such differences occur, it will be important to understand what temporal and spatial scales adequately portray a species' or population's diet and ranging behavior. This study documents within-site variation in the diet and ranging behavior of guerezas in the habitat types in which they are described to be most successful-forest edge and regenerating forest. We collected data on eight groups of guerezas with overlapping home ranges for 3-5 months each in Kibale National Park, Uganda. The guerezas were highly folivorous, with leaves constituting 78.5-94.0% of the groups' diets. The percentage of mature leaves and fruit in the diet varied widely among and within groups. We show that differences among groups in the intensity with which they fed on specific tree species were not just related to phenology, but also to differences in the forest compositions of groups' core areas. Range size estimates varied more than fivefold among groups and the minimum distance from groups' core areas to eucalyptus forest (which all groups regularly fed in) was a better predictor of range size than was group size. These results reveal considerable variation in the diet and ranging behavior among groups with overlapping ranges and have implications for comparative studies, investigations of within- and between-group feeding competition, and the potential for populations to adapt to anthropogenic or natural environmental change.

Understanding factors that influence reproduction and offspring survival in zoo populations is critical for management of threatened and endangered species. Examination of long-term data (1989–2011) compiled from the Association of Zoos and Aquarium's zoo-managed tiger breeding program provides the basis for a more thorough understanding of reproduction and scientifically based decisions for effective population management in this endangered felid. Biological and management-related factors that could influence tiger breeding success and cub survival were evaluated using logistic mixed models. Breeding success improved with female age until approximately age five, then declined thereafter. Experienced female breeders had greater breeding success than inexperienced females. Litter size was most predictive of cub survival, with average-sized litters (3–4 cubs) experiencing the highest proportional survival. Management-related factors, such as whether the breeding institution had a recent tiger litter and whether both animals were already located at the same institution, also influenced breeding success and cub survival. These results highlight the importance of institutional husbandry experience and the need to retain knowledge through staff turnovers to achieve optimal reproductive success. Using fecal estrogen data, frequency of ovarian cyclicity and mean cycle length did not differ by female age or parity; thus, lack of cyclicity and/or increased cycle duration are not likely explanations for declining breeding success with age. These results provide valuable reproductive information that should improve scientific management of zoo-based tiger populations.

The influence of diet and food distribution on the socioecology of group-living species has long been debated, particularly for primates. It has typically been assumed that folivorous primates experience relatively little feeding competition due to the abundant, widespread nature of their food, freeing them to form large groups in response to predation, to disperse with relative ease, and to have egalitarian female social relationships. Recent studies, however, have come to different conclusions about the extent to which folivorous primates are limited by food and experience food competition and how these factors affect folivore socioecology. To better understand the selective pressures that diet places on folivores, we investigated how 2 small highly folivorous groups of colobus monkeys (Colobus guereza) in Kibale National Park, Uganda, responded behaviorally and physiologically to a steep reduction in availability of their most important foods. The monkeys decreased their reliance on their 2 most frequently eaten food species and increased their daily path length, number of feeding patches visited/day, size of individual feeding areas, percentage of time spent feeding, and dietary diversity. They also showed evidence of physiological costs, in that lactating females' urinary C-peptide levels (i.e., insulin production) declined as top foods became scarce, and parasite loads slightly, but significantly, increased in 2 of 3 adult females examined. These results suggest that highly folivorous primates, even in very small groups, may experience behavioral and physiological effects of food limitation, within-group scramble competition for food, and possibly substantial selective pressures during periods of food scarcity. Copyright 2009, Oxford University Press.

Many studies in molecular ecology rely upon the genotyping of large numbers of low-quantity DNA extracts derived from noninvasive or museum specimens. To overcome low amplification success rates and avoid genotyping errors such as allelic dropout and false alleles, multiple polymerase chain reaction (PCR) replicates for each sample are typically used. Recently, two-step multiplex procedures have been introduced which drastically increase the success rate and efficiency of genotyping. However, controversy still exists concerning the amount of replication needed for suitable control of error. Here we describe the use of a two-step multiplex PCR procedure that allows rapid genotyping using at least 19 different microsatellite loci. We applied this approach to quantified amounts of noninvasive DNAs from western chimpanzee, western gorilla, mountain gorilla and black and white colobus faecal samples, as well as to DNA from 100-year-old gorilla teeth from museums. Analysis of over 45 000 PCRs revealed average success rates of > 90% using faecal DNAs and 74% using museum specimen DNAs. Average allelic dropout rates were substantially reduced compared to those obtained using conventional singleplex PCR protocols, and reliable genotyping using low (< 25 pg) amounts of template DNA was possible. However, four to five replicates of apparently homozygous results are needed to avoid allelic dropout when using the lowest concentration DNAs (< 50 pg/reaction), suggesting that use of protocols allowing routine acceptance of homozygous genotypes after as few as three replicates may lead to unanticipated errors when applied to low-concentration DNAs.

Intergroup conflict occurs in many social species and involves potentially complex motivations and interactions. To understand its complexity in wild animals more fully, a comprehensive investigative approach is needed, in which the multiple resource values and measures of fighting ability that potentially influence intergroup contests are simultaneously considered and controlled for. This study uses long-term data on eight neighbouring groups of folivorous black and white colobus monkeys, Colobus guereza ('guerezas') in Kibale National Park, Uganda, to investigate the factors influencing intergroup conflict. Adult males were the main participants in intergroup aggression. Of the three resource values investigated, food value had the most unambiguous positive effect on the tendency for males to initiate high-level intergroup aggression and for groups to win. Mate value positively influenced male initiation of high-level intergroup aggression, but not more so for the group that contained high-value mates. The presence of young infants had no obvious effects. Unlike in many other species, males were more likely to initiate intergroup aggression if their groups were smaller and contained fewer adult males than opposing groups. Groups with fewer but larger adult males, and to some extent, smaller groups, were more likely to win encounters. Moreover, the relative number of adult males/group largely affected the degree to which some other factors influenced male initiation of aggression and contest outcome. These findings reveal that a complex interplay between multiple resource values and multiple fighting ability measures can simultaneously influence initiation of and success in intergroup conflict. (C) 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Complex sex-biased dispersal patterns often characterize social-group-living species and may ultimately drive patterns of cooperation and competition within and among groups. This study investigates whether observational data or genetic data alone can elucidate the potentially complex dispersal patterns of social-group-living black and white colobus monkeys (Colobus guereza, "guerezas"), or whether combining both data types provides novel insights. We employed long-term observation of eight neighbouring guereza groups in Kibale National Park, Uganda, as well as microsatellite genotyping of these and two other neighbouring groups. We created a statistical model to examine the observational data and used dyadic relatedness values within and among groups to analyse the genetic data. Analyses of observational and genetic data both supported the conclusion that males typically disperse from their natal groups and often transfer into nearby groups and probably beyond. Both data types also supported the conclusion that females are more philopatric than males but provided somewhat conflicting evidence about the extent of female philopatry. Observational data suggested that female dispersal is rare or nonexistent and transfers into neighbouring groups do not occur, but genetic data revealed numerous pairs of closely related adult females among neighbouring groups. Only by combining both data types were we able to understand the complexity of sex-biased dispersal patterns in guerezas and the processes that could explain our seemingly conflicting results. We suggest that the data are compatible with a scenario of group dissolution prior to the start of this study, followed by female transfers into different neighbouring groups.

Understanding the relationship between bone strain and bone growth is critical for interpreting variations in skeletal robusticity. Recently we presented a model for interactions between estrogen, strain, and periosteal bone growth, in which high estrogen (E2) increases, and low (E2) decreases, osteogenic responses to strain. We compared cortical growth in expercised and sedentary sheep (Ovis aries) with higher vs. lower estrogen levels, and showed that exercised animals with high E2 added substantially more bone than those with lower E2. However, without normal controls, it was unclear whether exercise-induced cortical growth was stimulated by high E2, suppressed by lower E2, or both. Here we present a broader test of interactions between E2 levels (normal, low, high) and loading (exercised and sedentary). Low E2 animals were vaccinated against GnRH to suppress estrogen, while high E2 animals received estrogen implants. After 45 days, periosteal bone growth was measured at hindlimb midshafts. The results support the hypothesis that estrogen upregulates strain-induced cortical bone growth: exercised, high-E2 animals grew 6-27% more bone than exercised animals with lower E2 levels, or sedentary animals (p<.05). The effects of the anti-GnRH vaccine on bone growth are more complex. Assays showed that vaccinated animals had normal, not decreased, E2 levels, but grew 34-39% less bone in response to exercise than normal controls (p<.05). This suggests the vaccine affected strain-induced bone growth without changing circulating E2, an unexpected finding. These results demonstrate that variation in E2 levels may produce differential growth response to similar mechanical loading through complex mechanisms.

Analyses of plant DNA in feces provides a promising, yet largely unexplored, means of documenting the diets of elusive primates. Here we demonstrate the promise and pitfalls of this approach using DNA extracted from fecal samples of wild western gorillas (Gorilla gorilla) and black and white colobus monkeys (Colobus guereza). From these DNA extracts we amplified, cloned, and sequenced small segments of chloroplast DNA (part of the rbcL gene) and plant nuclear DNA (ITS‐2). The obtained sequences were compared to sequences generated from known plant samples and to those in GenBank to identify plant taxa in the feces. With further optimization, this method could provide a basic evaluation of minimum primate dietary diversity even when knowledge of local flora is limited. This approach may find application in studies characterizing the diets of poorly‐known, unhabituated primate species or assaying consumer–resource relationships in an ecosystem. Am. J. Primatol. 69:699–705, 2007. © 2007 Wiley‐Liss, Inc.

Intergroup aggression is relatively common in many primate species and its functions have long been debated and incorporated as important parts of primate socioecological models. Recent studies have improved upon previous research by empirically testing the potential mate, food/resource and infant defence functions of intergroup aggression. I raise three main issues regarding the predictions and methods that have been used and make suggestions that should improve future studies. First, I address what constitutes evidence of defence and suggest that encounter rates and contexts should generally not be used to help test mate, resource and infant defence hypotheses. Secondly, I address the problem of disentangling mate, resource and infant defence hypotheses and suggest that because they are not mutually exclusive and potentially confound one another, tests of one hypothesis should adequately control for other possible functions, preferably using multiple logistic regression. Lastly, I discuss the importance of examining intergroup aggression using a cost-benefit approach and suggest that measures should be taken to control for species-specific measures of fighting ability, and/or other potential costs or influential factors that might influence participation in intergroup aggression, including groups' identities. For the latter two issues, I provide simulations that illustrate the methodologies I suggest and the potential effects of employing them, relative to previously employed tests.

In theory, between-group contest (BGC) competition for food can greatly influence female social relationships and reproductive success in primates, but few studies have investigated whether such effects occur and, if so, under what ecological conditions. There is evidence that adult male black and white colobus monkeys (Colobus guereza, “guerezas”) defend the food their mates need against other groups, suggesting that BGC competition is important in this species. Using data on feeding, ranging, vegetation patterns, and intergroup encounters between six neighboring guereza groups, I provide evidence that the highly folivorous guerezas at Kanyawara, Kibale National Park, Uganda, engaged in BGC competition over unevenly dispersed, relatively high-quality feeding areas or “core areas”. Intergroup aggression was common, and groups’ home ranges overlapped. Groups were more likely to initiate high-level aggression if they encountered another group within or near their core area, and groups that initiated and won encounters often fed in the same areas in which losing groups had fed. Guerezas fed selectively on species with contagious (clumped) distributions and concentrated their feeding efforts in areas of the forest that contained the most food (core areas). Groups could be ranked in a linear dominance hierarchy, and group rank number was inversely related to the quantity and quality of food in groups’ core areas. This study not only provides good evidence that BGC competition occurs in primates but it also reinforces the idea that folivore food resources may be worth defending.

To test hypotheses about loud call function, researchers have typically used playback experiments and/or analyzed the contexts in which calls are produced. Analyzing the variation within and among individuals' loud calls may also provide insights about their function, including advertisement of callers' fighting abilities. This Study tests whether some male black and white colobus monkeys (Colobus guereza 'guerezas') indicate their willingness to defend access to important feeding areas and/or males by increasing the number of roars they produce/chorus, their roar lengths, and/or overall roaring effort. It also tests whether mean values for these roaring variables indicate male fighting ability. My assistants and I followed six guereza groups for three months each at Kanyawara, Kibale National Park, Uganda. I recorded males' morning chorus roars and used data on roars. intergroup aggression. feeding. and proximity of females to Ovulation to test hypotheses about roaring variation. I show that males were the main participants in intergroup aggression, the six study groups can be ranked in a linear dominance hierarchy, and group rank (effectively male rank) predicts and varies positively with how long males roar, as well as overall roaring effort. I provide evidence that some males roar longer when their groups' females are in close proximity to presumptive ovulation. There was relatively little evidence that males roar more when near important feeding areas. Males in higher and lower ranking groups may have different roaring strategies in the presence of important resources, but further studies are needed to fully test this idea. While this study may not provide strong evidence for either a direct mate or food defense function of roars, it shows that roars may advertise a male's ability to defend males and/or food.

Black and white colobus monkeys ( Colobus guereza , “guerezas”) show no external signs of estrus, and little is known about their mating behavior or reproductive endocrinology. To learn more about the life history characteristics and mating system of guerezas, we documented the mating behavior and ovarian hormone profiles of 10 cycling, lactating, and pregnant females in a wild population. We studied six groups of guerezas in Kibale National Park, Uganda, and collected ad libitum data on their mating behavior. We collected urine samples every 1.9±0.2 days from potentially fertile females and quantified conjugated urinary estrogen (E 1 S) and progesterone (PdG) metabolites using enzyme immunoassay (EIA). Females solicited 50.5% of copulations, and most copulations occurred during the interval starting 5 days before presumptive ovulation and ending 2–3 days later, with the highest copulatory levels occurring close to ovulation. We show that the median ovarian cycle length is 24 days, the median gestation length is ∼158 days, the length of lactational amenorrhea is at least 7–8 months, and the median interbirth interval for females with surviving infants is ∼22 months. We also document overlap between females' receptive periods in one‐male, two‐ to three‐female groups, which may mean that male transfer into such groups is potentially profitable. Am. J. Primatol. 68:383–396, 2006.© 2006 Wiley‐Liss, Inc.

Formant dispersion, the average spacing, in Hz, between the resonant frequencies of a vocalization, has been predicted to provide honest information about signaler body size. Previous descriptions of black and white colobus monkey ( Colobus guereza , “guereza”) roars, however, suggest a formant dispersion that is far lower than expected for an animal its size, and could effectively exaggerate its body size. Nonetheless, recent research on red deer shows that even when the formant positions of vocalizations effectively exaggerate body size, they may still provide honest cues within a species. We investigate whether the frequency bands observed in the spectrograms of guereza roars represent formants, and whether roar formant dispersion and/or individual formants provide honest information about body size (specifically, body mass) relative to conspecifics, although perhaps not relative to other species. We document coordinated vertical movements in the frequency bands of guereza roars and show that these bands move independently of fundamental frequency, indicating that they represent formants. We show, for captive adult male guerezas, that signaler body mass significantly predicts roar formant dispersion, even for randomly selected calls. Body mass also predicts formants 2 and 3, but the relationships are not as strong as with formant dispersion. Our roar formant dispersion calculations predict a vocal tract length of approx. 29 cm, but anatomically determined guereza vocal tract length is much smaller: approx. 7–8 cm. Videotaped roars revealed no laryngeal movement during roars, but rather inflation of the subhyoid air sac. We measured the volume of this air sac (approx. 10 cm 3 ) and speculate that it may function in roars to exaggerate body size, relative to other species.

Infanticide has been observed in several colobines, but only one infanticide has previously been documented for black and white colobus monkeys (Colobus guereza). This report describes an infanticide observed in Kibale National Park, Uganda, in the summer of 2001. An adult male from a neighboring group attacked and killed a young infant whose mother subsequently remained in her own group and was observed mating 10 days later. She engaged in two mating periods of several days each, separated by approximately 1 month, during which she copulated frequently with the dominant male within her group. Urinary estrogen (EC) and progesterone metabolite (PdG) excretion patterns demonstrated that the female resumed ovarian cycling soon after the infanticide. Because the infanticidal male did not attempt to mate with the victim's mother, his actions were not consistent with the predictions of the sexual-selection hypothesis. We speculate that infanticide associated with intergroup aggression may help secure access to high-quality resources for the infanticidal male's group.