CSIRO PUBLISHING Review www.publish.csiro.au/journals/an Animal Production Science, 2011, 51, 277–291 Intraspecific variation in biology and ecology of deer: magnitude and causation Rory Putman A,D and Werner T. Flueck B,C AKeil House, Ardgour, by Fort William, Inverness-shire, Scotland, PH33 7AH, UK. BSwiss Tropical Institute, University Basel. CNational Council of Scientific and Technological Research, Buenos Aires; Institute of Natural Resources Analysis – Patagonia, Universidad Atlantida, Argentina. C.C. 592, 8400 Bariloche, Argentina. DCorresponding author. Email: [email protected] Abstract. It has been noted that the search for patterns in biology to assist our understanding, often leads to over-simplification. That is, we are satisfied with statements that ‘the species as a rule does this’ or, ‘males of this species do that’. But within such generalisations are masked what are often important variations from that supposed norm and in practice there is tremendous variation in morphology, physiology, social organisation and behaviour of any one species. The focus on a supposedly mean optimal phenotype has diverted attention away from variation around that mean, which is regularly regarded as a kind of ‘noise’ stemming merely from stochastic effects, and thus irrelevant to evolution. Yet it is becoming increasingly clear that this variation is by converse extremely significant and of tremendous importance both to evolutionary biologists and to managers. Such intraspecific variation (IV) may be directly due to underlying genetic differences between individuals or populations within a species, but equally may include a degree of phenotypic plasticity whether as ‘non-labile’, traits which are expressed once in an individual’s lifetime, as fixed characteristics inherited from the parents or as more labile traits which are expressed repeatedly and reversibly in a mature individual according to prevailing conditions. Recognition of the extraordinary degree of IV which may be recorded within species has important consequences for management of cervids and conservation of threatened species. We review the extent of IV in diet, in morphology, mature bodyweight, reproductive physiology, in population demography and structure (sex ratio, fecundity, frequency of reproduction) before also reviewing the striking variation to be observed in behaviour: differences between individuals or populations in ranging behaviour, migratory tendency, differences in social and sexual organisation. In each case we explore the factors which may underlie the variation observed, considering the extent to which variation described has a primarily genetic basis or is a more plastic response to more immediate social and ecological cues. Additional keywords: cervids, phenotypic plasticity. Introduction is by converse extremely significant and of tremendous Barash1 has noted that the search for patterns in biology to assist importance both to evolutionary biologists and to managers. our understanding, often leads to over-simplification. That is, we Such intraspecific variation (IV) may be directly due to are satisfied with statements that ‘the species as a rule does this’ underlying genetic differences between individuals or or, ‘males of this species do that’. But within such generalisations populations within a species, but equally, phenotypic variation are masked what are often important variations from that between individuals of a common genotype may result from supposed norm and in practice there is tremendous variation in differences in their ontogeny under rather distinct environmental morphology, physiology, social organisation and behaviour of conditions.* Such phenotypic plasticity2 (hereafter PP) includes any one species, as it adapts feeding habits, social behaviour – ‘non-labile’ traits, which are expressed once in an individual’s even reproductive behaviour – to changing environmental lifetime, as fixed characteristics inherited from the parents or as circumstances. The focus on a supposedly mean optimal part of ontogenetic development. But in addition, PP also includes phenotype has diverted attention away from variation around labile traits, which are expressed repeatedly and reversibly in a that mean, which is regularly regarded as a kind of ‘noise’ mature individual according to prevailing conditions. stemming merely from stochastic effects and thus irrelevant to Thus it is clear that, especially in relation to aspects of evolution. Yet it is becoming increasingly clear that this variation behaviour or ecology, there may be considerable plasticity of *Differences in ontogeny among similar genotypes are also sometimes referred to as ‘developmental plasticity’. Ó CSIRO 2011 10.1071/AN10168 1836-0939/11/040277 278 Animal Production Science R. Putman and W. T. Flueck response even within a given individual, if exposed to different below –60 to >40C – although it is perhaps unclear in this environmental circumstances – and that many aspects of instance whether or not such wide tolerances are a species-wide behaviour and ecology are not fixed elements of an phenomenon or actually reflect more specific local adaptation in individual’s response, but may show significant variation in different temperature zones. expression under different circumstances. Such individual As another example, compensatory extension of the gestation variation (often referred to more formally as phenotypic length is known for several deer species, with differences being flexibility3), while more commonly recorded in relation to almost twice the oestrous cycle length (moose Alces alces;11 red behavioural or ecological responses, may also relate to deer Cervus elaphus;12,13 sika C. nippon;14 reindeer Rangifer reproduction (e.g. timing of reproduction and the number or tarandus15). size of offspring produced), or morphological characters that Alongside such gross variability in habitats occupied, are regularly regrown.4 Such plasticity may influence enzyme individual patterns of habitat use even within a given locality products, morphological development, learned behaviours and will also show significant inter-individual variation,16,17 even an organism’s response to the effects of disease.5 As influenced by availability and disposition of habitats, as well environmental conditions include both external surroundings as intra- and interspecific competition, and presence of predators of an organism and the internal conditions affecting gene which may affect the spatial distribution.18,19 expression, PP clearly encompasses a tremendous diversity of In exactly the same way, it is clear that, for widely distributed kinds of variability.6 species, the diet must vary from place to place since relative Recognition of the extraordinary degree of IV which may be and absolute availability of different forage species varies recorded within species has important consequences for geographically. Thus, individual studies of the diet management of cervids and conservation of threatened species. composition of European roe deer (Capreolus capreolus)in In this paper we aim to review some of the extent of IV shown the UK show enormous variation in actual species by different species of deer. In a short paper we must necessarily composition or relative importance of different forage species be selective both of topic and of the species used to illustrate of animals in different geographic areas, or different contexts particular examples. In addition: since differences in social (continuous forest, farmland with scattered woodland areas behaviour (grouping tendency, group size, group structure, etc.20–22 and, to a lesser extent, season,23 and throughout degree of sexual and social segregation, mating strategy) are their European range they may consume literally hundreds of often the most notable, and also the ones most relevant to different species. The same is broadly true for other species; in managers, we will focus primarily in this paper on variation in essence, while, within any particular area, deer may indeed social and sexual behaviour. It would be wrong, however, show feeding preferences for certain species of plants among completely to ignore other contexts of variation, and we will those available, dietary intake must otherwise respond start with a brief review of recorded variation in habitat use, opportunistically to availability, within the constraints imposed diet, morphology and reproductive physiology. In each case we by physiology, foraging ‘style’, competition and predation explore the factors which may underlie the variation observed, pressure. However, we must recognise that deer can adapt to considering the extent to which variation described has a changing forage quality, to some extent at least, by altering primarily genetic basis or is a more plastic response to more the extent of selective feeding, by increasing forage retention immediate social and ecological cues. in the rumen, by varying gut length and gastrointestinal anatomy, by changing gut microbial communities, by adjusting body size and reproductive output, among others.24–26 For instance, Variation in habitat occupied and diet as the vegetation changes, feeding behaviour in some deer It is almost a sine qua non – that deer species with a wide species can change substantially, moving from pure ‘grazers’ geographic distribution will show gross variation in the range through ‘intermediate’ feeding to pure ‘browsers27,28.’ Once of habitats occupied and in their adaptation to different abiotic again, variation in feeding