Compensatory extension of gestation length with advance of conception in red deer (Cervus elaphus)

Calving date in many mammals is matched to the time of greatest food availability. Out of season calving results in heavy penalties in terms of own and offspring survival or body condition. This study examined whether gestation length is affected by advancing fertilisation. Thirty-six red deer hinds (of the Iberian and Scottish subspecies) were subjected to a synchronisation treatment of oestrus, ovulation, and artificial insemination on three dates, with remaining non-pregnant females mated with an intact male in a last group. Gestation was longer the more the fertilisation was advanced; gestation lasted 241.5+/-1.3 days (d) in the first group, 237.4+/-1.2 d in the second, 235.1+/-1.3 d in the third, and 231.2+/-1.6 d in the last. Mean gestation lasted 234.2+/-0.7 d. Hinds gained less weight during gestation the more the fertilisation was advanced. The difference was due at least in part to net body weight of the hind after calving compared to that at mating, and calves did not differ in birth weight. As early born calves suffer greater mortality in the field, this enlargening of gestation might be a compensatory response of the hinds to match calving with food availability. Under natural conditions, similar small modifications of gestation length may help hinds to overcome short-term adverse conditions for calving. Because calf mortality is correlated with birth weight, hinds may have kept calf birth weight constant at the expense of greater body weight loss.     

The gestation length of wapiti (Cervus elaphus) revisited

As an ancillary activity to an artificial insemination program in farmed wapiti, the length of gestation of 28 wapiti hinds that delivered single calves of established parentage was calculated. Estrus was synchronized in 47 wapiti using progesterone impregnated devices (controlled internal drug release, CIDR) and an injection of PMSG. All hinds were artificially inseminated between 60 and 63h after CIDR removal. Pregnancy was determined between 45 and 65 days by ultrasound. A verifiable figure for gestation length was obtained based both upon timed-artificial insemination, date of parturition, and confirmation of sire identity through microsatellite DNA technology. The calculated gestational length of 247 +/- 5 days was significantly (P < 0.0001) shorter than the generally quoted figure of 255 +/- 7 days.     

Malignant melanoma in a captive red deer (Cervus elaphus elaphus)

We report a case of malignant melanoma in a captive red deer (Cervus elaphus elaphus). The primary lesion was on the plantar aspect of the right pastern and infiltrated the surrounding skin, but not underlying tendons or bone. Diffuse metastasis to the regional lymph nodes had occurred. Histologically, lesions were characterized by large numbers of variably pigmented epithelioid cells with a high degree of nuclear atypia and many mitotic figures. This is the first reported case of this neoplasm in red deer.     

Mitochondrial DNA phylogeography of red deer (Cervus elaphus)

In order to understand the origin, phylogeny, and phylogeography of the species Cervus elaphus, we examined the DNA sequence variation of the mitochondrial cytochrome b gene of 51 populations of deer from the entire distribution area of Cervinae with an emphasis on Europe and Asia. Several methods, including maximum parsimony, maximum likelihood, and nested clade analysis, revealed that red deer originated from the area between Kyrgyzstan and Northern India. We found two distinct groups of red deer: a western group consisting of four subgroups and an eastern group consisting of three subgroups. Our mtDNA data do not support the traditional classification of red deer as only one species nor its division into numerous subspecies. The discrepancies between the geographical pattern of differentiation based on mtDNA cytochrome b and the existing specific and subspecific taxonomy based on morphology are discussed.     

Phylogeography of red deer (Cervus elaphus) in Europe

Aim To investigate the phylogeographical patterns of red deer (Cervus elaphus) in Europe, and to disentangle the influence of ancient (e.g. Pleistocene ice ages) from more recent processes (e.g. human translocations). Location Europe. Methods In this study we provide by far the most extensive analysis of genetic structure in European red deer, based on analyses of variation at two mitochondrial markers (cyt b and D‐loop) in a large number of individuals from 39 locations. Relationships of mitochondrial DNA haplotypes were determined using minimum spanning networks and phylogenetic analyses. Population structure was examined by analyses of molecular variance. Historical processes shaping the present patterns were inferred from nested clade analysis and nucleotide diversity statistics. Results Within Europe, we detected three deeply divergent mitochondrial DNA lineages. The three lineages displayed a phylogeographical pattern dividing individuals into western European, eastern European and Mediterranean (Sardinia, Spain and Africa) groups, suggesting contraction into three separate refugia during the last glaciation. Few haplotypes were shared among these three groups, a finding also confirmed by F_ST values. Calculations of divergence times suggest that the groups probably split during the Pleistocene. Main conclusions The observed pattern is interpreted to result from isolation in different refugia during the last glaciation. The western and eastern European lineages could be linked to an Iberian and Balkan refugium, respectively. The third lineage might originate from a Sardinian or African refugium. We link local phylogeographical patterns observed in Europe to the post‐glacial recolonization process, shaped by the geographical localization of refugia and barriers to gene flow. Regardless of the importance of red deer as a game species and the tradition of translocating red deer in Europe, we detected few individuals that did not match the trichotomous pattern, suggesting that translocations have occurred mainly at smaller spatial scales.     

The influence of birth date on the development of seasonal cycles in red deer hinds (Cervus elaphus)

The relative importance of age and photoperiod in the timing of seasonal cycles was studied in red deer during the first 18 months of life. Seasonal cycles of appetite, live-weight change, coat growth, oestrus and metabolic rate were examined in two groups of seven hind calves born in early May (group E) or nine weeks later in July (group L).
There was no difference between groups in the timing or amplitude of the seasonal voluntary food intake (VFI) cycle, or in the timing of seasonal changes in rate of live-weight gain, although mean live-weight gain was significantly greater for group L than group E during the first winter of life.
Four animals in group L retained their calf coats throughout the first winter. In group L, the first summer coat fibres appeared approximately four weeks earlier, and mean fibre length for the subsequent winter coat was longer in group L than in group E. There was no difference between groups in the timing or amplitude of the seasonal cycle of plasma prolactin concentration, or in the incidence and mean time of onset of puberty.
There was no difference between groups in mean energy expenditure per unit of live weight at any time of the year. Mean daily energy expenditure was significantly higher in summer than in winter, but values measured when the animals were resting and corrected for differences in VFI were similar throughout the year.
It is concluded that the seasonal cycles of appetite, live-weight change and oestrus in young red deer hinds are not modified by age, although the normal cycle of coat replacement can be disturbed in animals born towards the end of the calving season.     

Genetic structure of the Danish red deer (Cervus elaphus)

The red deer (Cervus elaphus) population in Denmark became almost extinct in recent historical times due to over‐hunting. The species has subsequently recovered within remote areas, but non‐Danish individuals have been introduced at several localities. To assess genetic structure, past demographic history, and the possibility of a still existing original stock, we analysed 349 specimens from 11 geographically separate areas and from three enclosed areas, genotyping 11 microsatellite loci. Moreover, an 826‐bp fragment of the control region of the mitochondrial DNA was sequenced for 116 recent specimens and seven museum specimens. There was a significant difference in mean expected heterozygosity (H_E) between the three enclosed areas and the 11 unenclosed areas. Significant departures from Hardy–Weinberg equilibrium were observed in the three enclosed areas and in nine of the unenclosed areas. The overall degree of genetic differentiation among all 14 areas was significant (F_ST = 0.09, P < 0.01), primarily because the mean pairwise F_ST for the three enclosed areas was significantly higher than that for the 11 unenclosed areas. A Bayesian clustering procedure detected three genetically distinct populations and indicated reduced gene flow between the enclosed and unenclosed areas. The individuals in the unenclosed areas show genotypic mixture, presumably as a result of gene flow among them. Markov Chain Monte Carlo simulations, based on the genealogical history of the microsatellite alleles, suggest a drastic decline in the effective population size of the enclosed areas some 188–474 years ago. Mitochondrial DNA analysis of the recent specimens showed seven haplotypes. Individuals from the enclosed Jægersborg Dyrehave contain haplotypes that occur all over Denmark and also are found in Western Europe. A close relationship between Scandinavian and Western European red deer is most likely. Only individuals from the unenclosed Lindenborg Estate and the enclosed Tofte Skov did not group with any other Danish individuals. As six of seven museum specimens had haplotypes also found in modern Danish samples, the current population of red deer in Denmark is genetically close to the original Danish red deer. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 688–701.     

Onchocercosis in red deer (Cervus elaphus) from Spain.

Onchocercosis, caused by Onchocerca flexuosa, was observed in red deer (Cervus elaphus) from Spain for the first time. Adult specimens of P. flexuosa were found in nodules in subcutaneous tissues in 42 of 125 (33%) red deer between October 1994 and September 1995; intensity of infection +/- SD was 3.93 +/- 5.26 nodules per infected host. A clear seasonal pattern in the distribution of nodules was observed, with higher values of prevalence and intensity in fall and winter in contrast to spring and summer. Significant differences were found among age groups in prevalence, but not in the mean intensity. No differences in infection were apparent between male and female adult red deer.     

Freemartinism in red deer (Cervus elaphus L.)

Several mixed-sex twins were produced by red deer treated with progesterone and pregnant mare's serum gonadotrophin. Of seven females karyotyped, two were 68,XX/68,XY chimeras. One male had the same chimeric karyotype as its female co-twin. These are the first reported cases of freemartinism in deer.     

Morphological observation of antler regeneration in red deer (Cervus elaphus)

Deer antler offers a unique opportunity to explore how nature solves the problem of mammalian appendage regeneration. Annual antler renewal is an example of epimorphic regeneration, which is known to take place through initial blastema formation. Detailed examination of the early process of antler regeneration, however, has thus far been lacking. Therefore, we conducted morphological observations on antler regeneration from naturally cast and artificially created pedicle/antler stumps. On the naturally cast pedicle stumps, early antler regeneration underwent four distinguishable stages (with the Chinese equivalent names): casting of previous hard antlers (oil lamp bowl), early wound healing (tiger eye), late wound healing and early regeneration (millstone), and formation of main beam and brown tine (small saddle). Overall, no cone-shaped regenerate, a common feature to blastema-based regeneration, was observed. Taken together with the examination on the sagittal plane of each regenerating stage sample, we found that there are considerable overlaps between late-stage wound healing and the establishment of posterior and anterior growth centers. Observation of antler regeneration from the artificially created stumps showed that the regeneration potential of antler remnants was significantly reduced compared with that of pedicle tissue. Interestingly, the distal portion of a pedicle stump had greater regeneration potential than the proximal region, although this differential potential may not be constitutive, but rather caused by whether or not pedicle antlerogenic tissue becomes closely associated with the enveloping skin at the cut plane. Antler formation could take place from the distal peripheral tissues of an antler/pedicle stump, without the obvious participation of the entire central bony portion. Overall, our morphological results do not support the notion that antler regeneration takes place through the initial formation of a blastema; rather, it may be a stem cell-based process.     

Physiological effects of hunting red deer (Cervus elaphus).

When red deer (Cervus elaphus) were hunted by humans with hounds the average distance travelled was at least 19 km. This study of 64 hunted red deer provides the first empirical evidence on their state at the time of death. Blood and muscle samples obtained from hunted deer after death were compared with samples from 50 non-hunted red deer that had been cleanly shot with rifles. The effects on deer of long hunts were (i) depletion of carbohydrate resources for powering muscles, (ii) disruption of muscle tissue, and (iii) elevated secretion of beta-endorphin. High concentrations of cortisol, typically associated with extreme physiological and psychological stress, were found. Damage to red blood cells occurred early in the hunts; possible mechanisms are discussed. Taken together, the evidence suggests that red deer are not well-adapted by their evolutionary or individual history to cope with the level of activity imposed on them when hunted with hounds.     

Factors affecting reproduction in red deer (Cervus elaphus) hinds on Rhum

In a population of free-ranging red deer hinds on the Isle of Rhum (Inner Hebrides) we investigated relationships between four aspects of reproductive performance (fertility, calf birth weight, birth sex ratio and calving date) and four variables likely to affect the mother's condition: age, reproductive status, home range area and year of calving. Fertility was significantly related to mother's age, reproductive status and home range area as well as to year of calf's birth. Stag calves were heavier than hind calves and birth weight was significantly related to mother's age, home range area and year of (calf's) birth but not to mother's reproductive status. Birth sex ratio did not differ from parity, and was not significantly associated with any of the four variables examined. Birth date was significantly related to the mother's reproductive status, home range area and year of (calf's) birth but not to mother's age or the sex of the calf.     

Reproductive seasonality in female Iberian red deer (Cervus elaphus hispanicus)

This study characterized the seasonal pattern of luteal cyclicity in Iberian red deer (n=16), by measuring plasma progesterone concentrations in hinds (female red deer) twice per week from calving (May and June) 1996 until May 1997. In eight of these hinds we also examined plasma prolactin profiles to assess seasonal responses to photoperiod. Plasma progesterone concentration in the 16 hinds studied indicated that the reproductive pattern is seasonal, and lasts for 5.73 +/- 0.27 months. After calving, progesterone levels remained basal (no luteal activity) for several months, except in a hind that lost her calf just after calving, and thus did not have to suckle it. This hind showed two consecutive estrus cycles in the month following calving, which suggests that suckling has an inhibiting effect on the resumption of ovarian activity. These results also showed that as long as the hinds do not become pregnant, they show between 5 and 10 estrus cycles per reproductive season (8.06 +/- 0.35), ranging between 105 and 249 days from onset of the first cycle to end of the last one. Uninterrupted cycling lasted for 3.5-6.4 months (mean, 4.6 +/- 0.24). Cyclic luteal activity was found from October to February in all hinds, with a smaller, but notable proportion in September (56.25%) and March (68.8%), whereas it was negligible in the remaining period. Our results show a reproductive season similar to or longer than that recorded by other authors. Prolactin plasma concentrations showed a yearly trend following that of photoperiod, with peak concentrations from April to July, a decrease in August, minimal concentrations from September to February and a sharp increase in March.     

Seasonal luteal cyclicity of pubertal and adult red deer (Cervus elaphus)

Reproductive failure of rising-two-year-old (R(2)) hinds and seasonal misalignment between calving and pastoral feed production are two factors limiting reproductive productivity of farmed red deer hinds in New Zealand. This study aimed to better understand processes around female puberty and breeding seasonality by describing the potential breeding season (i.e., oestrous cyclicity) of three red deer genotypes. A total of 27 hinds born in December 2005, representing Eastern European (Cervus elaphus hippelaphus), Western European (C.e. scoticus) and F1 crossbred (C.e. hippelaphus×scoticus) red deer, were blood sampled thrice-weekly for 7-8 months (February-September/October) across two years spanning the potential breeding seasons as R(2)'s in 2007 (i.e., puberty) and as adults in 2008. Plasma progesterone profiles were used to construct breeding cycle histories for each hind. Four R(2) hinds failed to initiate oestrous cycles (i.e., puberty failure). The remaining R(2) hinds, including all F1 hinds, exhibited between two and seven oestrous cycles. F1 hinds were significantly earlier to initiate, and later to terminate, cyclic activity, resulting in a longer mean pubertal breeding season (139 days) than for Eastern (86 days) and Western hinds (86 days). However, the data for R(2) hinds are confounded by live-weight, with the F1 hinds being significantly heavier than other genotypes. There were significant correlations between live-weight and seasonality parameters in 2007. All hinds were cyclic as adults in 2008, exhibiting between four and nine oestrous cycles, and a mean breeding season duration of between 132 (Western) and 137 (F1) days. For adult hinds there were no significant genotype differences in cyclic onset and cessation timing, and no observable relationships between live-weight and any reproductive parameter. However, the mean dates for the onset of the breeding season for all genotypes in 2008 were 2-3 weeks later than normally expected for adult hinds in New Zealand. The reasons for this are unclear but may relate to chronic stress of frequent animal handling. The study has demonstrated that puberty in red deer hinds is associated with a shorter potential breeding season than for adult hinds, and that perturbation of breeding activity appears to be quite common, leading to incidences of puberty failure and possibly other aberrant cyclic events. Live-weight×genotype interactions may influence puberty but do not appear to be strongly expressed in adults. However, the relatively late onset of oestrous cyclicity in the adult hinds may be an artefact of the study that has masked genetic influences on seasonal breeding patterns.     

Nocturnal hypometabolism as an overwintering strategy of red deer (Cervus elaphus)

Herbivores of temperate and arctic zones are confronted during winter with harsh climatic conditions and nutritional shortness. It is still not fully understood how large ungulates cope with this twofold challenge. We found that red deer, similar to many other northern ungulates, show large seasonal fluctuations of metabolic rate, as indicated by heart rate, with a 60% reduction at the winter nadir compared with the summer peak. A previously unknown mechanism of energy conservation, i.e., nocturnal hypometabolism associated with peripheral cooling, contributed significantly to lower energy expenditure during winter. Predominantly during late winter night and early morning hours, subcutaneous temperature could decrease substantially. Importantly, during these episodes of peripheral cooling, heart rate was not maintained at a constant level, as to be expected from classical models of thermoregulation in the thermoneutral zone, but continuously decreased with subcutaneous temperature, both during locomotor activity and at rest. This indicates that the circadian minimum of basal metabolic rate and of the set-point of body temperature regulation varied and dropped to particularly low levels during late winter. Our results suggest, together with accumulating evidence from other species, that reducing endogenous heat production is not restricted to hibernators and daily heterotherms but is a common and well-regulated physiological response of endothermic organisms to energetically challenging situations. Whether the temperature of all tissues is affected, or the body shell only, may simply be a result of the duration and degree of hypometabolism and its interaction with body size-dependent heat loss.     

Induction of early breeding in red deer (Cervus elaphus) by melatonin

Lactating (N = 12) and non-lactating (N = 6) red deer hinds and one stag at pasture were given concentrates (500 g/head) containing melatonin (5 mg/head) daily at 16:00 h from 18 June to 16 October. The stag shed the antler velvet and started rutting 5 weeks ahead of untreated stags, and hinds had their first oestrus and ovulation of the breeding season in mid-September, 5 weeks in advance of control lactating (N = 9) and non-lactating (N = 5) hinds. Treated hinds were allowed to mate with the treated stag and control hinds ran in an adjacent paddock with an untreated stag. All hinds became pregnant during the study with all but 2 melatonin-fed hinds (1 lactating, 1 non-lactating) and 1 control hind (lactating) conceiving at the first oestrus. Melatonin-treated hinds lost slightly more live weight than did controls from June to November, but their suckled calves grew throughout at a rate similar to those of control hinds.