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.

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.

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.

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.

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.

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.

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.

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.

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.

Gross intestinal morphometry and allometry in ruminants.

While some descriptions of ruminants' dietary adaptations suggest that the length of the intestinal tract reflects the proportion of grass or browse in the diet, this assumption has been questioned. We collated data on body mass (BM), as well as small intestine, caecum, colon/rectum, large and total intestine length in 68 ruminant species, and, while accounting for the phylogenetic structure of the dataset, evaluated both allometric scaling and the potential influence of diet, digestive physiology or climate proxies on measures of intestine length. Intestinal length generally scaled to BM at an exponent higher than the 0.33 expected due to geometry. Diet or digestive physiology proxies did not have an influence on any intestinal length measures, though some proxies indicating more arid natural habitats were positively correlated with measures of the large intestine. The relative size of a forestomach compartment, the omasum, was negatively correlated with intestine length. The results indicate that intestine length measures provide little indication of feeding type or digestive physiology, but rather indicate adaptations to aridity. Higher-than-geometry scaling of intestinal length may be related to the necessity of maintaining geometric (or metabolic) scaling of intestinal surface area while keeping gut diameter, and hence the diffusion distances, small. The way in which space trade-offs determine the macroanatomy of different organs in the abdominal cavity, such as the omasum and the intestine, deserves further investigation.

Root growth compensates for molar wear in adult goats (Capra aegagrus hircus).

One reason for the mammalian clade's success is the evolutionary diversity of their teeth. In herbivores, this is represented by high-crowned teeth evolved to compensate for wear caused by dietary abrasives like phytoliths and grit. Exactly how dietary abrasives wear teeth is still not understood completely. We fed four different pelleted diets of increasing abrasiveness (L: Lucerne; G: grass; GR: grass and rice husks; GRS: grass, rice husks, and sand) to four groups of a total of 28 adult goats, all with completely erupted third molars, over a six-month period. Tooth morphology was captured by medical computed tomography scans at the beginning and end of the controlled feeding experiment, and separation lines between the crown and root segments were defined in the upper right second molar (M2), to gauge absolute wear. Using bootstrapping, significant differences in volume loss between diets L/G and GR/GRS were detected. A small but nevertheless consistent volume gain was noted in the roots, and there was a significant, positive correlation between crown volume loss and root volume gain. This growth could possibly be attributed to the well-known process of cementum deposition and its relation with a putative feedback mechanism, in place to attenuate wear caused by abrasive diets.

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.

Geographical Origin, Delayed Implantation, and Induced Ovulation Explain Reproductive Seasonality in the Carnivora.

Patterns of reproductive seasonality in the Carnivora are difficult to study comparatively, due to limited numbers of species for which information is available. Long-term databases of captive populations could overcome this difficulty. We apply a categorical description and a quantitative high-resolution measure (birth peak breadth, the number of days in which 80% of all births occur) based on daily observations in captivity to characterize the degree of reproductive seasonality in the Carnivora for 114 species with on average 1357 births per species. We find that the majority of species retained the birth seasonality displayed in the wild. Latitude of natural origin, delayed implantation, and induced ovulation were the main factors influencing reproductive seasonality. Most species were short-day breeders, but there was no evidence of an absolute photoperiodic signal for the timing of mating or conception. The length of the gestation period (corrected for body mass) generally decreased with birth seasonality but increased in species with delayed implantation. Birth seasons become shorter with increasing latitude of geographical origin, likely because the length of the favorable season declines with increasing latitude, exerting a strong selective pressure on fitting both the reproductive cycle and the interval offspring needs for growth following the termination of parental care into the short time window of optimal environmental conditions. Species with induced ovulation exhibit a less seasonal reproductive pattern, potentially because mates do not have to meet during a short time window of a fixed ovulation. Seasonal species of Carnivora shorten their gestation period so reproduction can occur during the short time window of optimal environmental conditions. Alternatively, other Carnivora species lengthen their gestation periods in order to bridge long winters. Interestingly, this occurs not by decelerating intrauterine growth but by delaying implantation.

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.

Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals.

While it is commonly believed that animals live longer in zoos than in the wild, this assumption has rarely been tested. We compared four survival metrics (longevity, baseline mortality, onset of senescence and rate of senescence) between both sexes of free-ranging and zoo populations of more than 50 mammal species. We found that mammals from zoo populations generally lived longer than their wild counterparts (84% of species). The effect was most notable in species with a faster pace of life (i.e. a short life span, high reproductive rate and high mortality in the wild) because zoos evidently offer protection against a number of relevant conditions like predation, intraspecific competition and diseases. Species with a slower pace of life (i.e. a long life span, low reproduction rate and low mortality in the wild) benefit less from captivity in terms of longevity; in such species, there is probably less potential for a reduction in mortality. These findings provide a first general explanation about the different magnitude of zoo environment benefits among mammalian species, and thereby highlight the effort that is needed to improve captive conditions for slow-living species that are particularly susceptible to extinction in the wild.

Does sexual selection shape sex differences in longevity and senescence patterns across vertebrates? A review and new insights from captive ruminants.

In most mammals, both sexes display different survival patterns, often involving faster senescence in males. Being under intense sexual competition to secure mating opportunities, males of polygynous species allocate resources to costly behaviors and conspicuous sexual traits, which might explain these observed differences in longevity and senescence patterns. However, comparative studies performed to date have led to conflicting results. We aimed to resolve this problem by first reviewing case studies of the relationship between the strength of sexual selection and age-specific survival metrics. Then, we performed a comprehensive comparative analysis to test whether such relationships exist among species of captive ruminants. We found that the strength of sexual selection negatively influenced the onset of actuarial senescence in males, with males senescing earlier in polygynous than in monogamous species, which led to reduced male longevity in polygynous species. Moreover, males of territorial species senesced earlier but slower, and have a shorter longevity than males of species displaying other mating tactics. We detected little influence of the strength of sexual selection on the rate of actuarial senescence. Our findings demonstrate that the onset of actuarial senescence, rather than its rate, is a side effect of physiological mechanisms linked to sexual selection, and potentially accounts for observed differences in longevity.

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.

Males do not senesce faster in large herbivores with highly seasonal rut.

Patterns of actuarial senescence vary among long-lived species. A proposed explanation of the evolution of species-specific senescence patterns is that increased levels of energy allocation to intra-male competition decrease the amount of energy available for somatic maintenance, leading to earlier or faster actuarial senescence. Previous studies did not provide support for such relationships, but did not focus on the intensity of allocation likely to shape inter-specific variation in actuarial senescence in males. Here, by analyzing data from 56 species of captive large herbivores, we tested whether actuarial senescence is more pronounced in species displaying a well-defined 'rut' period than in species with year-round reproduction. Using an original quantitative metric of the annual duration of reproductive activity, we demonstrated that the length of the mating season has no detectable effect on actuarial senescence. On the other hand, both diet and body mass are important factors shaping actuarial senescence patterns in male captive herbivores.

Detecting inter-cusp and inter-tooth wear patterns in rhinocerotids.

Extant rhinos are the largest extant herbivores exhibiting dietary specialisations for both browse and grass. However, the adaptive value of the wear-induced tooth morphology in rhinos has not been widely studied, and data on individual cusp and tooth positions have rarely been published. We evaluated upper cheek dentition of browsing Diceros bicornis and Rhinoceros sondaicus, mixed-feeding R. unicornis and grazing Ceratotherium simum using an extended mesowear method adapted for rhinos. We included single cusp scoring (EM(R)-S) to investigate inter-cusp and inter-tooth wear patterns. In accordance with previous reports, general mesowear patterns in D. bicornis and R. sondaicus were attrition-dominated and C. simum abrasion-dominated, reflecting their respective diets. Mesowear patterns for R. unicornis were more attrition-dominated than anticipated by the grass-dominated diet, which may indicate a low intake of environmental abrasives. EM(R)-S increased differentiation power compared to classical mesowear, with significant inter-cusp and inter-tooth differences detected. In D. bicornis, the anterior cusp was consistently more abrasion-dominated than the posterior. Wear differences in cusp position may relate to morphological adaptations to dietary regimes. Heterogeneous occlusal surfaces may facilitate the comminution of heterogeneous browse, whereas uniform, broad grinding surfaces may enhance the comminution of physically more homogeneous grass. A negative tooth wear gradient was found in D. bicornis, R. sondaicus and R. unicornis, with wear patterns becoming less abrasion-dominated from premolars to molars. No such gradients were evident in C. simum which displayed a uniform wear pattern. In browsers, premolars may be exposed to higher relative grit loads, which may result in the development of wear gradients. The second premolar may also have a role in food cropping. In grazers, high absolute amounts of ingested abrasives may override other signals, leading to a uniform wear pattern and dental function along the tooth row, which could relate to the observed evolution towards homodonty.

Herbivory and body size: allometries of diet quality and gastrointestinal physiology, and implications for herbivore ecology and dinosaur gigantism.

Digestive physiology has played a prominent role in explanations for terrestrial herbivore body size evolution and size-driven diversification and niche differentiation. This is based on the association of increasing body mass (BM) with diets of lower quality, and with putative mechanisms by which a higher BM could translate into a higher digestive efficiency. Such concepts, however, often do not match empirical data. Here, we review concepts and data on terrestrial herbivore BM, diet quality, digestive physiology and metabolism, and in doing so give examples for problems in using allometric analyses and extrapolations. A digestive advantage of larger BM is not corroborated by conceptual or empirical approaches. We suggest that explanatory models should shift from physiological to ecological scenarios based on the association of forage quality and biomass availability, and the association between BM and feeding selectivity. These associations mostly (but not exclusively) allow large herbivores to use low quality forage only, whereas they allow small herbivores the use of any forage they can physically manage. Examples of small herbivores able to subsist on lower quality diets are rare but exist. We speculate that this could be explained by evolutionary adaptations to the ecological opportunity of selective feeding in smaller animals, rather than by a physiologic or metabolic necessity linked to BM. For gigantic herbivores such as sauropod dinosaurs, other factors than digestive physiology appear more promising candidates to explain evolutionary drives towards extreme BM.