Putting zoo animal cancer into perspective.

As part of a comparative research agenda that promises insights that help extend the human lifespan and combat cancer, cancer prevalence in zoo animals has received recent attention. Here, we want to draw attention to a principle of cancer research that was introduced into the zoo world as early on as 1933, but that seems to have gone somewhat forgotten: Cancer is mainly a disease of old age, and therefore studies aiming at identifying taxa that are particularly susceptible or resistant to cancer must control for whether the respective zoo populations are 'old.' In a comparative context, 'old age' cannot be measured in absolute terms (e.g., years), but only in relation to a species' maximum lifespan: Species that achieve, across zoos, a higher mean lifespan as a percent of their maximum lifespan are 'older.' When applying this metric to former as well as more recently published data on cancer prevalence, it appears that those species that become relatively old in zoos-in particular, the carnivores-have a relatively high cancer prevalence. Any improvement in animal husbandry-which reduces premature deaths-should, by default, lead to more cancer. Cancer in zoo animals, like any other old-age condition, might therefore be embraced as a proxy for good husbandry. Rather than following a sensationalist approach that dramatizes disease and death per se, zoos should be clear about what their husbandry goals are, what relative longevities they want to achieve for which species, and what old-age diseases they should therefore expect: in the end, one has to die of something.

The historical development of zoo elephant survivorship.

In the discussion about zoo elephant husbandry, the report of Clubb et al. (2008, Science 322: 1649) that zoo elephants had a "compromised survivorship" compared to certain non-zoo populations is a grave argument, and was possibly one of the triggers of a large variety of investigations into zoo elephant welfare, and changes in zoo elephant management. A side observation of that report was that whereas survivorship in African elephants (Loxodonta africana) improved since 1960, this was not the case in Asian elephants (Elephas maximus). We used historical data (based on the Species360 database) to revisit this aspect, including recent developments since 2008. Assessing the North American and European populations from 1910 until today, there were significant improvements of adult (≥10 years) survivorship in both species. For the period from 1960 until today, survivorship improvement was significant for African elephants and close to a significant improvement in Asian elephants; Asian elephants generally had a higher survivorship than Africans. Juvenile (<10 years) survivorship did not change significantly since 1960 and was higher in African elephants, most likely due to the effect of elephant herpes virus on Asian elephants. Current zoo elephant survivorship is higher than some, and lower than some other non-zoo populations. We discuss that in our view, the shape of the survivorship curve, and its change over time, are more relevant than comparisons with specific populations. Zoo elephant survivorship should be monitored continuously, and the expectation of a continuous trend towards improvement should be met.

Historical development of the survivorship of zoo rhinoceroses-A comparative historical analysis.

Zoo animal husbandry is a skill that should be developing constantly. In theory, this should lead to an improvement of zoo animal survivorship over time. Additionally, it has been suggested that species that are at a comparatively higher risk of extinction in their natural habitats (in situ) might also be more difficult to keep under zoo conditions (ex situ). Here, we assessed these questions for three zoo-managed rhinoceros species with different extinction risk status allocated by the IUCN: the "critically endangered" black rhino (Diceros bicornis), the "vulnerable" greater one-horned (GOH) rhino (Rhinoceros unicornis), and the "near threatened" white rhino (Ceratotherium simum). Comparing zoo animals ≥1 year of age, the black rhino had the lowest and the white rhino the highest survivorship, in congruence with their extinction risk status. Historically, the survivorship of both black and white rhino in zoos improved significantly over time, whereas that of GOH rhino stagnated. Juvenile mortality was generally low and decreased even further in black and white rhinos over time. Together with the development of population pyramids, this shows increasing competence of the global zoo community to sustain all three species. Compared to the continuously expanding zoo population of GOH and white rhinos, the zoo-managed black rhino population has stagnated in numbers in recent years. Zoos do not only contribute to conservation by propagating ex situ populations, but also by increasing species-specific husbandry skills. We recommend detailed research to understand specific factors responsible for the stagnation but also the general improvement of survivorship of zoo-managed rhinos.

The historical development of juvenile mortality and adult longevity in zoo-kept carnivores.

Zoos need to evaluate their aim of high husbandry standards. One way of approaching this is to use the demographic data that has been collected by participating zoos for decades, assessing historical change over time to identify the presence or absence of progress. Using the example of carnivores, with data covering seven decades (1950-2019), 13 carnivore families, and 95 species, we show that juvenile mortality has decreased, and adult longevity increased, over this interval. While no reason for complacency, the results indicate that the commitment of zoos to continuously improve is having measurable consequences.

The uneven weight distribution between predators and prey: Comparing gut fill between terrestrial herbivores and carnivores.

The general observation that secondary consumers ingest highly digestible food and have simple short guts and small abdominal cavities intuitively results in the assumption that mammalian carnivores carry less digesta in their gut compared to herbivores. Due to logistic constraints, this assumption has not been tested quantitatively so far. In this contribution, we estimated the dry matter gut contents (DMC) for 25 species of the order Carnivora (including two strictly herbivorous ones, the giant and the red panda) using the physical 'Occupancy Principle', based on a literature data collection on dry matter intake (DMI), apparent dry matter digestibility (aD DM) and retention time (RT), and compared the results to an existing collection for herbivores. Scaling exponents with body mass (BM) for both carnivores and herbivores were in the same range with DMI ~ BM0.75; aD DM ~ BM0; RT ~ BM0.11 and DMC ~ BM0.88. The trophic level (carnivore vs herbivore) significantly affected all digestive physiology parameters except for RT. Numerically, the carnivore DMI level reached 77%, the RT 32% and DMC only 29% of the corresponding herbivore values, whereas the herbivore aD DM only reached 82% of that of carnivores. Thus, we quantitatively show that carnivores carry less inert mass or gut content compared to herbivores, which putatively benefits them in predator-prey interactions and might have contributed to the evolution towards unguligradism in herbivores. As expected, the two panda species appeared as outliers in the dataset with low aD DM and RT for a herbivore but extremely high DMI values, resulting in DMC in the lower part of the herbivore range. Whereas the difference in DMI and DMC scaling in herbivores might allow larger herbivores to compensate for lower diet quality by ingesting more, this difference may allow larger carnivores not to go for less digestible prey parts, but mainly to increase meal intervals, i.e. not having to hunt on a daily basis.

Controlled feeding experiments with diets of different abrasiveness reveal slow development of mesowear signal in goats (Capra aegagrus hircus).

Dental mesowear is applied as a proxy to determine the general diet of mammalian herbivores based on tooth-cusp shape and occlusal relief. Low, blunt cusps are considered typical of grazers and high, sharp cusps typical of browsers. However, how internal or external abrasives impact mesowear, and the time frame the wear signature takes to develop, still need to be explored. Four different pelleted diets of increasing abrasiveness (lucerne, grass, grass and rice husks, and grass, rice husks and sand) were fed to four groups of a total of 28 adult goats in a controlled feeding experiment over a 6-month period. Tooth morphology was captured by medical CT scans at the beginning and end of the experiment. These scans, as well as the crania obtained post mortem, were scored using the mesowear method. Comparisons between diet groups showed few significant differences after 6 months, irrespective of whether CT scans or the real teeth were scored. Only when assessing the difference in signal between the beginning and the end of the experiment did relevant, significant diet-specific effects emerge. Diets containing lower phytolith content caused a more pronounced change in mesowear towards sharper cusps/higher reliefs, while the feed containing sand did not result in more extreme changes in mesowear when compared with the same feed without sand. Our experiment suggests that the formation of a stable and hence reliable mesowear signal requires more time to develop than 6 months.

Seasonal mortality in zoo ruminants.

While seasonality has often been investigated with respect to reproduction, seasonality of mortality has received less attention. We investigated whether a seasonal signal of mortality exists in wild ruminants kept in zoos, using data from 60,591 individuals of 88 species. We quantified the mortality in the 3 consecutive months with the highest above-baseline mortality (3 MM). 3 MM was not related to relative life expectancy of species, indicating that seasonal mortality does not necessarily impact husbandry success. Although 3 MM was mainly observed in autumn/winter months, there was no evidence for an expected negative relationship with the latitude of the species' natural habitat and no positive relationship between 3 MM and the mean temperature in that habitat, indicating no evidence for species from lower latitudes/warmer climates being more susceptible to seasonal mortality under zoo conditions. 3 MM was related to reproductive biology, with seasonally reproducing species also displaying more seasonal mortality. This pattern differed between groups: In cervids, the onset of seasonal mortality appeared linked to the onset of rut in both sexes. This was less evident in bovids, where in a number of species (especially caprids), the onset of female seasonal mortality was linked to the lambing period. While showing that the origin of a species from warmer climate zones does not constrain husbandry success in ruminants in terms of an increased seasonal mortality, the results suggest that husbandry measures aimed at protecting females from rutting males are important, especially in cervids. Zoo Biol. 36:74-86, 2017. © 2016 Wiley Periodicals, Inc.

Digesta kinetics in gazelles in comparison to other ruminants: Evidence for taxon-specific rumen fluid throughput to adjust digesta washing to the natural diet.

Digesta flow plays an important role in ruminant digestive physiology. We measured the mean retention time (MRT) of a solute and a particle marker in the gastrointestinal tract (GIT) and the reticulorumen (RR) of five gazelles and one dikdik species. Species-specific differences were independent from body mass (BM) or food intake. Comparative evaluations (including up to 31 other ruminant species) indicate that MRT GIT relate positively to BM, and are less related to feeding type (the percentage of grass in the natural diet, %grass) than MRT RR. The MRTparticleRR is related to BM and (as a trend) %grass, matching a higher RR capacity with increasing BM in grazers compared to browsers. MRTsoluteRR is neither linked to BM nor to %grass but shows a consistent phylogenetic signal. Selectivity factors (SF; MRTparticle/MRTsolute, proxies for the degree of digesta washing) are positively related to %grass, with a threshold effect, where species with >20% grass have higher SF. These findings suggest that in different ruminant taxa, morphophysiological adaptations controlling MRTsoluteRR evolved to achieve a similar SF RR in relation to a %grass threshold. A high SF could facilitate an increased microbial yield from the forestomach. Reasons for variation in SF above the %grass threshold might represent important drivers of ruminant diversification and await closer investigation.

Assessing the Jarman-Bell Principle: Scaling of intake, digestibility, retention time and gut fill with body mass in mammalian herbivores.

Differences in allometric scaling of physiological characters have the appeal to explain species diversification and niche differentiation along a body mass (BM) gradient - because they lead to different combinations of physiological properties, and thus may facilitate different adaptive strategies. An important argument in physiological ecology is built on the allometries of gut fill (assumed to scale to BM(1.0)) and energy requirements/intake (assumed to scale to BM(0.75)) in mammalian herbivores. From the difference in exponents, it has been postulated that the mean retention time (MRT) of digesta should scale to BM(1.0-0.75)=BM(0.25). This has been used to argue that larger animals have an advantage in digestive efficiency and hence can tolerate lower-quality diets. However, empirical data does not support the BM(0.25) scaling of MRT, and the deduction of MRT scaling implies, according to physical principles, no scaling of digestibility; basing assumptions on digestive efficiency on the thus-derived MRT scaling amounts to circular reasoning. An alternative explanation considers a higher scaling exponent for food intake than for metabolism, allowing larger animals to eat more of a lower quality food without having to increase digestive efficiency; to date, this concept has only been explored in ruminants. Here, using data for 77 species in which intake, digestibility and MRT were measured (allowing the calculation of the dry matter gut contents (DMC)), we show that the unexpected shallow scaling of MRT is common in herbivores and may result from deviations of other scaling exponents from expectations. Notably, DMC have a lower scaling exponent than 1.0, and the 95% confidence intervals of the scaling exponents for intake and DMC generally overlap. Differences in the scaling of wet gut contents and dry matter gut contents confirm a previous finding that the dry matter concentration of gut contents decreases with body mass, possibly compensating for the less favorable volume-surface ratio in the guts of larger organisms. These findings suggest that traditional explanations for herbivore niche differentiation along a BM gradient should not be based on allometries of digestive physiology. In contrast, they support the recent interpretation that larger species can tolerate lower-quality diets because their intake has a higher allometric scaling than their basal metabolism, allowing them to eat relatively more of a lower quality food without having to increase digestive efficiency.

Fibre digestibility in large herbivores as related to digestion type and body mass--an in vitro approach.

The coexistence of different ungulate species in a given ecosystem has been the focus of many studies. Differences between ruminant foregut fermenters and hindgut fermenters were remarkable for example in the way they ingest and digest high fibre diets. Digestion trials based on total collections are difficult to conduct or are sometimes even not possible for wild animals in the field or in zoos. To gain information on the fibre digestion achieved by these animals and the influence of body mass (BM) thereon, a method using spot sampling is desirable. In this study, in vitro fermentation of faecal neutral detergent fibre (NDF) was used as a measure of fibre digestion in large ungulates. Food and faecal samples of 10 ruminant foregut fermenting and 7 hindgut fermenting species/breeds were collected. All animals received 100% grass hay with ad libitum access. The NDF of food and faeces was fermented in vitro in a Hohenheim gas test (HGT) for 96 h. The digestion type generally had an effect on the gas production (GP) of faecal NDF in the HGT with hindgut fermenters showing higher values than ruminant foregut fermenters. At any time interval of incubation, BM had no influence on GP. The results are in accordance with both findings that ruminant foregut fermenters have longer mean retention times and more comprehensive particle reduction and findings of a lack of influence of BM on digesta mean retention time. It can be stated that the HGT (96 h) is a useful and quick method to show also small differences within groups in fibre digestion.

Long-Term Olfactory Memory in African Elephants.

African elephants are capable of discriminating scents up to a single changed molecule and show the largest reported repertoire of olfactory receptor genes. Olfaction plays an important role in family bonding. However, to the best of our knowledge, no empirical data exist on their ability to remember familiar scents long-term. In an ethological experiment, two mother-daughter pairs were presented with feces of absent kin, absent non-kin, and present non-kin. Video recordings showed reactions of elephants recognizing kin after long-term separation but only minor reactions to non-kin. Results give the empirical implication that elephants have an olfactory memory longer than 1 year and up to 12 years and can distinguish between kin and non-kin just by scent. These findings confirm the significance of scent for family bonds in African elephants.

Ontogenetic niche shifts in dinosaurs influenced size, diversity and extinction in terrestrial vertebrates.

Given the physiological limits to egg size, large-bodied non-avian dinosaurs experienced some of the most extreme shifts in size during postnatal ontogeny found in terrestrial vertebrate systems. In contrast, mammals--the other dominant vertebrate group since the Mesozoic--have less complex ontogenies. Here, we develop a model that quantifies the impact of size-specific interspecies competition on abundances of differently sized dinosaurs and mammals, taking into account the extended niche breadth realized during ontogeny among large oviparous species. Our model predicts low diversity at intermediate size classes (between approx. 1 and 1000 kg), consistent with observed diversity distributions of dinosaurs, and of Mesozoic land vertebrates in general. It also provides a mechanism--based on an understanding of different ecological and evolutionary constraints across vertebrate groups--that explains how mammals and birds, but not dinosaurs, were able to persist beyond the Cretaceous-Tertiary (K-T) boundary, and how post-K-T mammals were able to diversify into larger size categories.

Retention of solutes and different-sized particles in the digestive tract of the ostrich (Struthio camelus massaicus), and a comparison with mammals and reptiles.

Ostriches (Struthio camelus) achieve digesta retention times, digesta particle size reduction and digestibilities equal to similar-sized herbivorous mammals, in contrast to some other avian herbivores. The sequence of digestive processes in their gastrointestinal tract, however, is still unexplored. Using two groups of four ostriches (mean body mass 75.1 ± 17.3 kg) kept on fresh alfalfa, we tested the effect of two intake levels (17 and 42 g dry matter kg(-0.75)d(-1)) on the mean retention time (MRT) of a solute and three different-sized (2, 10, 20 mm) particle markers, mean faecal particle size (MPS), and digestibility. Intake level did not affect MRT, but MPS (0.74 vs. 1.52 mm) and dry matter digestibility (81 vs. 78%). The solute marker (MRT 22-26 h) was excreted faster than the particle markers; there was no difference in the MRT of 10 and 20 mm particles (MRT 28-32 h), but 2mm particles were retained longer (MRT 39-40 h). Because the solute marker was not selectively retained, and wet-sieving of gut contents of slaughtered animals did not indicate smaller particles in the caeca, the long MRT of small particles is interpreted as intermittent excretion from the gizzard, potentially due to entrapment in small grit. The marker excretion pattern also showed intermittent peaks for all markers in five of the animals, which indicates non-continuous outflow from the gizzard. When adding our data to literature data on avian herbivores, a dichotomy is evident, with ostrich and hoatzin (Opisthocomus hoazin) displaying long MRTs, high digestibilities, and gut capacities similar to mammalian herbivores, and other avian herbivores such as grouse, geese or emus with shorter MRTs, lower fibre digestibilities and lower gut capacities. In the available data for all avian herbivores where food intake and MRTs were measured, this dichotomy and food intake level, but not body mass, was related to MRT, adding to the evidence that body mass itself may not be sole major determinant of digestive physiology. The most striking difference between mammalian and avian herbivores from the literature is the fundamentally lower methane production measured in the very few studies in birds including ostriches, which appears to be at the level of reptiles, in spite of general food intake levels of a magnitude as in mammals. Further studies in ostriches and other avian herbivores are required to understand the differences in digestive mechanisms between avian and mammalian herbivores.

Mating system, feeding type and ex situ conservation effort determine life expectancy in captive ruminants.

Zoo animal husbandry aims at constantly improving husbandry, reproductive success and ultimately animal welfare. Nevertheless, analyses to determine factors influencing husbandry of different species are rare. The relative life expectancy (rLE; life expectancy (LE) as proportion of longevity) describes husbandry success of captive populations. Correlating rLE with biological characteristics of different species, reasons for variation in rLE can be detected. We analysed data of 166 901 animals representing 78 ruminant species kept in 850 facilities. The rLE of females correlated with the percentage of grass in a species' natural diet, suggesting that needs of species adapted to grass can be more easily accommodated than the needs of those adapted to browse. Males of monogamous species demonstrate higher rLE than polygamous males, which matches observed differences of sexual bias in LE in free-living populations and thus supports the ecological theory that the mating system influences LE. The third interesting finding was that rLE was higher in species managed by international studbooks when compared with species not managed in this way. Our method facilitates the identification of biological characteristics of species that are relevant for their husbandry success, and they also support ecological theory. Translating these findings into feeding recommendations, our approach can help to improve animal husbandry.

Herbivorous reptiles and body mass: effects on food intake, digesta retention, digestibility and gut capacity, and a comparison with mammals.

Differences in the allometric scaling between gut capacity (with body mass, BM¹·°°) and food intake (with BM°·75) should theoretically result in a scaling of digesta retention time with BM°·²5 and therefore a higher digestive efficiency in larger herbivores. This concept is an important part of the so-called 'Jarman-Bell principle' (JBP) that explains niche differentiation along a body size gradient in terms of digestive physiology. Empirical data in herbivorous mammals, however, do not confirm the scaling of retention time, or of digestive efficiency, with body mass. Here, we test these concepts in herbivorous reptiles, adding data of an experiment that measured food intake, digesta retention, digestibility and gut capacity in 23 tortoises (Testudo graeca, T. hermanni , Geochelone nigra, G. sulcata, Dipsochelys dussumieri) across a large BM range (0.5-180 kg) to a literature data collection. While dry matter gut fill scaled to BM¹·°7 and dry matter intake to BM°·76, digesta mean retention time (MRT) scaled to BM°·¹7; the scaling exponent was not significantly different from zero for species > 1 kg. Food intake level was a major determinant of MRT across reptiles and mammals. In contrast to dietary fibre level, BM was not a significant contributor to dry matter digestibility in a General Linear Model. Digestibility coefficients in reptiles depended on diet nutrient composition in a similar way as described in mammals. Although food intake is generally lower and digesta retention longer in reptiles than in mammals, digestive functions scale in a similar way in both clades, indicating universal principles in herbivore digestive physiology. The reasons why the theoretically derived JBP has little empirical support remain to be investigated. Until then, the JBP should not be evoked to explain niche differentiation along a body size axis in terms of digestive physiology.

Phylogenetic constraints on digesta separation: Variation in fluid throughput in the digestive tract in mammalian herbivores.

The relevance of the mean retention time (MRT) of particles through the gastrointestinal tract (GIT) is well understood and MRT(particle)GIT is an important parameter in digestion models. Solute markers have been used to estimate MRT(solute)GIT (or 'fluid passage') in animals, but the relevance of this measure is less evident and is usually sought in its relation to MRT(particle)GIT. The ratio between the two measures indicates the degree of 'digesta washing', with little washing occurring at ratios of 1, aborad washing at ratios >1 (where the solute marker travels faster than the particle marker), and orad (retrograde) washing at ratios <1 (where the solute marker travels slower than the particle marker). We analysed digesta washing in a dataset of 98 mammalian species including man of different digestion types (caecum, colon and nonruminant foregut fermenters, and ruminants), controlling for phylogeny; a subset of 72 species allowed testing for the influence of food intake level. The results indicate that MRT(solute)GIT and the degree of digesta washing are related to digestion type, whereas variation in MRT(particle)GIT is influenced mainly by effects of body mass and food intake. Thus, fluid throughput and digesta washing emerge as important correlates of digestive anatomy. Most importantly, primates appear constrained to little digesta washing compared to non-primate mammalian herbivores, regardless of their digestion type. These results may help explain the absence of primates from certain herbivore niches and represent a drastic example of a physiologic limitation in a phylogenetic group. More experimental research is required to illuminate relative benefits and costs of digesta washing.

Is there an influence of body mass on digesta mean retention time in herbivores? A comparative study on ungulates.

The relation between body mass (BM) and digesta mean retention time (MRT) in herbivores was the focus of several studies in recent years. It was assumed that MRT scaled with BM(0.25) based on the isometric scaling of gut capacity (BM(1.0)) and allometric scaling of energy intake (BM(0.75)). Literature studies that tested this hypothesis produced conflicting results, arriving sometimes at higher or lower exponents than the postulated 0.25. This study was conducted with 8 ruminants (n=2-6 per species) and 6 hindgut fermenting species/breeds (n=2-6, warthog n=1) with a BM range of 60-4000 kg. All animals received a ration of 100% grass hay with ad libitum access. Dry matter intake was measured and the MRT was estimated by the use of a solute and a particle (1-2 mm) marker. No significant scaling of MRT(particle) with BM was observed for all herbivores (32 BM(0.04), p=0.518) and hindgut fermenters (32 BM(0.00), p=1.00). The scaling exponent for ruminants only showed a tendency towards significance (29 BM(0.12), p=0.071). Ruminants on average had an MRT(particle) 1.61-fold longer than hindgut fermenters. Whereas an exponent of 0.25 is reasonable from theoretical considerations, much lower exponents were found in this and other studies. The energetic benefit of increasing MRT is by no means continuous, since the energy released from a given food unit via digestion decreases over time. The low and non-significant scaling factors for both digestion types suggest that in ungulates, MRT is less influenced by BM (maximal allometric exponent ≤0.1) than often reported.

Monitoring Behaviour in African Elephants during Introduction into a New Group: Differences between Related and Unrelated Animals.

The introduction of elephants into new groups is necessary for breeding programmes. However, behavioural studies on the reactions of these animals at first encounters are missing. In the present study, female African elephants (Loxodonta africana) living in zoos were observed during unifications with unfamiliar elephants (introduction of two to one females and one to two females; n = 6) and reunifications with related elephants (two mother-daughter-pairs; n = 4) that were separated for 2 and 12 years, respectively. First encounters of the elephants were observed and recorded by scan sampling. The parameters measured were (a) signs of the characteristic Greeting Ceremony, (b) distance to the fence separating the elephants during first contact, and (c) time until trunks touched for the first time. The data were statistically analysed with SPSS. The results showed that related elephants performed a full Greeting Ceremony on reunifications. Unrelated elephants only expressed a minor greeting. During first encounters, related elephants predominantly showed affiliative behaviour (p = 0.001), whilst unrelated elephants expressed more agonistic behaviour (p = 0.001). The distance to the fence was significantly smaller for related elephants than for unrelated elephants (p = 0.038). first contact of trunks occurred on average after 3.00 s. in related elephants and 1026.25 s. in unrelated elephants. These findings indicate that related elephants recognise their kin after up to 12 years of separation, meet them with a full Greeting Ceremony during reunification, and seek contact to the related elephant, while unrelated elephants are hesitant during unifications with unfamiliar elephants and express more agonistic behaviour. The results testify that zoo elephants show the same species-specific social behaviour as their conspecifics in the wild. It also confirms the cognitive abilities of elephants and the significance of matrilines for breeding programmes.

Reproductive seasonality in primates: patterns, concepts and unsolved questions.

Primates, like other mammals, exhibit an annual reproductive pattern that ranges from strictly seasonal breeding to giving birth in all months of the year, but factors mediating this variation are not fully understood. We applied both a categorical description and quantitative measures of the birth peak breadth based on daily observations in zoos to characterise reproductive seasonality in 141 primate species with an average of 941 birth events per species. Absolute day length at the beginning of the mating season in seasonally reproducing species was not correlated between populations from natural habitats and zoos. The mid-point of latitudinal range was a major factor associated with reproductive seasonality, indicating a correlation with photoperiod. Gestation length, annual mean temperature, natural diet and Malagasy origin were other important factors associated with reproductive seasonality. Birth seasons were shorter with increasing latitude of geographical origin, corresponding to the decreasing length of the favourable season. Species with longer gestation periods were less seasonal than species with shorter ones, possibly because shorter gestation periods more easily facilitate the synchronisation of reproductive activity with annual cycles. Habitat conditions with higher mean annual temperature were also linked to less-seasonal reproduction, independently of the latitude effect. Species with a high percentage of leaves in their natural diet were generally non-seasonal, potentially because the availability of mature leaves is comparatively independent of seasons. Malagasy primates were more seasonal in their births than species from other regions. This might be due to the low resting metabolism of Malagasy primates, the comparatively high degree of temporal predictability of Malagasy ecosystems, or historical constraints peculiar to Malagasy primates. Latitudinal range showed a weaker but also significant association with reproductive seasonality. Amongst species with seasonal reproduction in their natural habitats, smaller primate species were more likely than larger species to shift to non-seasonal breeding in captivity. The percentage of species that changed their breeding pattern in zoos was higher in primates (30%) than in previous studies on Carnivora and Ruminantia (13 and 10%, respectively), reflecting a higher concentration of primate species in the tropics. When comparing only species that showed seasonal reproduction in natural habitats at absolute latitudes ≤11.75°, primates did not differ significantly from these two other taxa in the proportion of species that changed to a less-seasonal pattern in zoos. However, in this latitude range, natural populations of primates and Carnivora had a significantly higher proportion of seasonally reproducing species than Ruminantia, suggesting that in spite of their generally more flexible diets, both primates and Carnivora are more exposed to resource fluctuation than ruminants.

Retention of fluid and particles in captive tapirs (Tapirus sp.).

The retention of ingesta in the digestive tract is a major characteristic of herbivorous animals. We measured particle and fluid mean retention times (MRT) in 13 lowland tapirs (Tapirus terrestris) and 5 Malayan tapirs (Tapirus indicus) from five zoological institutions on their usual zoo diet and 2 lowland and 4 Malayan tapirs additionally on roughage-only diets (total n of trials=24) with cobalt-EDTA as fluid and chromium-mordanted fibre (<2 mm) as particle markers. MRT for fluid and particles averaged 42+/-16 h and 55+/-18 h in lowland and 40+/-13 h and 56+/-14 h in Malayan tapirs. In a General Linear Model, neither Tapir species, body mass or diet (characterised by the proportion of roughage) was significantly related to MRT, but dry matter intake was, with a steep decline in MRT with higher intake levels. Compared to other hindgut fermenters, tapirs have a low defecation frequency, which might be linked to their comparatively low food intake. Their gastrointestinal capacity (in dry matter: 1.63+/-0.63% of body mass) is similar to that calculated for horses. A comparison of the difference in fluid and particle MRT in large hindgut fermenters (horses, rhinoceroses, elephants, and the tapirs of this study) shows that longer absolute particle MRT are linked to shorter relative fluid MRT, possibly indicating a more thorough 'washing' of particulate ingesta with digestive fluids at longer particle MRT. The only outlier to this general pattern, with an exceptionally high difference between fluid and particle MRT, indicating a particularly efficient ingesta washing, is the white rhinoceros (Ceratotherium simum). If possible, results of this study should be compared to findings in tapirs on natural diets.