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

Basic considerations on seasonal breeding in mammals including their testing by comparing natural habitats and zoos

Seasonal reproduction is common in mammals. Whereas specific conditions triggering a seasonal response can only be identified in controlled experiments, large-scale comparisons of reproduction in natural habitats and zoos can advance knowledge for taxa unavailable for experimentation. We outline how such a comparison can identify species whose seasonal physiology is linked to photoperiodic triggers, and those whose perceived seasonality in the wild is the consequence of fluctuating resources without a photoperiodic trigger. This concept groups species into those that do not change their aseasonal pattern between natural habitats and zoos because they are not constrained by resources in the wild, those that do not change a seasonal pattern between natural habitats and zoos because they are triggered by photoperiod irrespective of resources, and those that change from a more seasonal pattern in the natural habitat to an aseasonal pattern in zoos because the zoo environment alleviates resource limitations experienced in the wild. We explain how detailed comparisons of mating season timing in both environments can provide clues whether a specific daylength or a specific number of days after an equinox or solstice is the likely phototrigger for a taxon. We outline relationships between life history strategies and seasonality, with special focus on relative shortening of gestation periods in more seasonal mammals. Irrespective of whether such shortening results from the adaptive value of fitting a reproductive cycle within one seasonal cycle (minimizing ‘lost opportunity’), or from benefits deriving from separating birth and mating (to optimize resource use, or to reduce infanticide), reproductive seasonality may emerge as a relevant driver of life history acceleration. Comparisons of data from natural habitats and zoos will facilitate testing some of the resulting hypotheses

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, BM1.00) and food intake (with BM0.75) should theoretically result in a scaling of digesta retention time with BM0.25 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 BM1.07 and dry matter intake to BM0.76, digesta mean retention time (MRT) scaled to BM0.17; 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

Comparing life expectancy of three deer species between captive and wild populations

Life in zoological gardens provides a number of benefits to captive animals, resulting in an artificial reduction of the “struggle for life” compared to their free-ranging counterparts. These advantages should result in a higher chance of surviving from one year to the next, and thus in longer average life expectancies for captive animals, given that the biological requirements of the species are adequately met. Here, we compare the life expectancy of captive and free-ranging populations of three deer species (reindeer Rangifer tarandus, red deer Cervus elaphus, and roe deer Capreolus capreolus). Whereas captive reindeer and red deer had life expectancies equal to or longer than free-ranging individuals, the life expectancy of captive roe deer was shorter than that of free-ranging animals. These results support the impression that roe deer are difficult to keep in zoos, whereas reindeer and red deer perform well under human care. We suggest that the mean life expectancy of captive populations relative to that of corresponding free-ranging populations is a reliable indicator to evaluate the husbandry success of a species in captivity

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

Chewing, dental morphology and wear in tapirs (Tapirus spp.) and a comparison of free-ranging and captive specimens

Feeding practice in herbivorous mammals can impact their dental wear, due to excessive or irregular abrasion. Previous studies indicated that browsing species display more wear when kept in zoos compared to natural habitats. Comparable analyses in tapirs do not exist, as their dental anatomy and chewing kinematics are assumed to prevent the use of macroscopic wear proxies such as mesowear. We aimed at describing tapir chewing, dental anatomy and wear, to develop a system allowing comparison of free-ranging and captive specimens even in the absence of known age. Video analyses suggest that in contrast to other perissodactyls, tapirs have an orthal (and no lateral) chewing movement. Analysing cheek teeth from 74 museum specimens, we quantified dental anatomy, determined the sequence of dental wear along the tooth row, and established several morphometric measures of wear. In doing so, we showcase that tapir maxillary teeth distinctively change their morphology during wear, developing a height differential between less worn buccal and more worn lingual cusps, and that quantitative wear corresponds to the eruption sequence. We demonstrate that mesowear scoring shows a stable signal during initial wear stages but results in a rather high mesowear score compared to other browsing herbivores. Zoo specimens had lesser or equal mesowear scores as specimens from the wild; additionally, for the same level of third molar wear, premolars and other molars of zoo specimens showed similar or less wear compared specimens from the wild. While this might be due to the traditional use of non-roughage diet items in zoo tapirs, these results indicate that in contrast to the situation in other browsers, excessive tooth wear appears to be no relevant concern in ex situ tapir management

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

Low scaling of a life history variable: Analysing eutherian gestation periods with and without phylogeny-informed statistics

Traditionally, biological times (gestation period, longevity) are proposed to scale to body mass M as M0.25. Although phylogeny-informed statistics have become widespread, it is still sometimes assumed that in datasets comprising a very large number of species, analyses that do not and that do account for phylogeny will yield similar results. Here we show, in a large dataset on gestation period length in eutherian mammals (1214 species from 20 orders), that the allometric scaling exponent is about twice as high using conventional statistics (Ordinary Least Squares OLS, M0.18-0.20) as when using Phylogenetic Generalized Least Squares (PGLS, M0.07-0.10), indicating that among closely related taxa, the scaling of gestation is much lower than generally assumed. This matches the well-known absence of scaling among different-sized breeds of domestic animal species, and indicates that changes in M must be more related to changes in development speed rather than development time among closely related species, which has implications for interpreting life history-consequences of insular dwarfism and gigantism. Only when allowing just one species per order (simulated in 100 randomized datasets of n=20 species across 20 orders) is 0.25 included in the scaling exponent confidence interval in both OLS and PGLS. Differences in scaling at different taxonomic levels in comparative datasets may indicate evolutionary trends where successive taxonomic groups compete by fundamental variation in organismal design not directly linked to changes in M. Allometries then do not necessarily represent universal scaling rules, but snapshots of evolutionary time that depend on diversification and extinction events before the picture was taken. It is either by analysing subsets separately, or by using PGLS in large datasets, that the underlying relationships with M can then be unveiled

Spinodal Decomposition in a Binary Polymer Mixture: Dynamic Self Consistent Field Theory and Monte Carlo Simulations

We investigate how the dynamics of a single chain influences the kinetics of early stage phase separation in a symmetric binary polymer mixture. We consider quenches from the disordered phase into the region of spinodal instability. On a mean field level we approach this problem with two methods: a dynamical extension of the self consistent field theory for Gaussian chains, with the density variables evolving in time, and the method of the external potential dynamics where the effective external fields are propagated in time. Different wave vector dependencies of the kinetic coefficient are taken into account. These early stages of spinodal decomposition are also studied through Monte Carlo simulations employing the bond fluctuation model that maps the chains -- in our case with 64 effective segments -- on a coarse grained lattice. The results obtained through self consistent field calculations and Monte Carlo simulations can be compared because the time, length, and temperature scales are mapped onto each other through the diffusion constant, the chain extension, and the energy of mixing. The quantitative comparison of the relaxation rate of the global structure factor shows that a kinetic coefficient according to the Rouse model gives a much better agreement than a local, i.e. wave vector independent, kinetic factor. Including fluctuations in the self consistent field calculations leads to a shorter time span of spinodal behaviour and a reduction of the relaxation rate for smaller wave vectors and prevents the relaxation rate from becoming negative for larger values of the wave vector. This is also in agreement with the simulation results.Comment: Phys.Rev.E in prin