Review: A theoretical framework to define foraging behaviour syndromes in ruminants using wearable technologies.

Due to intensification processes that have had negative impacts on environmental externalities, pastoral farmers, worldwide, are facing increasing scrutiny and pressure from consumers, governments, and the public to reduce the environmental footprint of their operations. Developing tools and systems that farmers can use to maintain profitability and productivity while decreasing the negative externalities of their operations is important for the vitality of rural sectors. Capitalising on individual animal variation has been promoted as an opportunity to increase animal productivity and enhance welfare while decreasing the negative environmental impacts of pastoral farming. Of particular interest are behaviours that are associated with foraging, as these are the primary drivers of variation in animal performance in pastoral farming. Developing a methodology that can identify consistent foraging behavioural variations across individuals is a critical step in making this a practical solution for farmers and herders. As with all behavioural research, the fundamental challenge is selecting the appropriate behaviours to measure. Understanding the contextual drivers of behavioural expression is a major development in this process. Herd management and composition, environmental variables and many more contexts alter the expression of behaviours, so how do we capture behaviours of interest? We propose the use of a systematic methodology to capture behaviours of significance from large groups of foraging ruminants using wearable technology, namely Global Positioning System and accelerometers. This contrasts with traditional reductionist methodologies used in behaviour research and has the benefit of providing large objective datasets from undisturbed animals. Statistical analysis of the data will inform behaviours of interest that are clustered together to inform a three-factor foraging behaviour syndrome model adapted from the animal five-factor model (activity, aggression, boldness, exploration, sociability) of personality. Syndromes, unlike personalities, include correlated suites of behaviours that are expressed across spatial and temporal contexts. By capturing foraging behaviour syndromes, selection can be used to match appropriate syndromes to different pastoral farming landscapes, thereby potentially improving the system's productivity while reducing their negative environmental impact.

Review: Livestock production increasingly influences wildlife across the globe.

With the growing human population, and their improving wealth, it is predicted that there will be significant increases in demand for livestock products (mainly meat and milk). Recent years have demonstrated that the growth in livestock production has generally had significant impacts on wildlife worldwide; and these are, usually, negative. Here I review the interactions between livestock and wildlife and assess the mechanisms through which these interactions occur. The review is framed within the context of the socio-ecological system whereby people are as much a part of the interaction between livestock and wildlife as the animal species themselves. I highlight areas of interaction that are mediated through effects on the forage supply (vegetation) - neutral, positive and negative - however, the review broadly analyses the impacts of livestock production activities. The evidence suggests that it is not the interaction between the species themselves but the ancillary activities associated with livestock production (e.g. land use change, removal of predators, provision of water points) that are the major factors affecting the outcome for wildlife. So in future, there are two key issues that need to be addressed - first, we need to intensify livestock production in areas of 'intensive' livestock production in order to reduce the pressure for land use change to meet the demand for meat (land sparing). And second, if wildlife is to survive in areas where livestock production dominates, it will have to be the people part of the socio-ecological system that sees the benefits of having wildlife co-exist with livestock on farming lands (land sharing and win-win).

State-Space Modelling of the Drivers of Movement Behaviour in Sympatric Species.

Understanding animal movement behaviour is key to furthering our knowledge on intra- and inter-specific competition, group cohesion, energy expenditure, habitat use, the spread of zoonotic diseases or species management. We used a radial basis function surface approximation subject to minimum description length constraint to uncover the state-space dynamical systems from time series data. This approximation allowed us to infer structure from a mathematical model of the movement behaviour of sheep and red deer, and the effect of density, thermal stress and vegetation type. Animal movement was recorded using GPS collars deployed in sheep and deer grazing a large experimental plot in winter and summer. Information on the thermal stress to which animals were exposed was estimated using the power consumption of mechanical heated models and meteorological records of a network of stations in the plot. Thermal stress was higher in deer than in sheep, with less differences between species in summer. Deer travelled more distance than sheep, and both species travelled more in summer than in winter; deer travel distance showed less seasonal differences than sheep. Animal movement was better predicted in deer than in sheep and in winter than in summer; both species showed a swarming behaviour in group cohesion, stronger in deer. At shorter separation distances swarming repulsion was stronger between species than within species. At longer separation distances inter-specific attraction was weaker than intra-specific; there was a positive density-dependent effect on swarming, and stronger in deer than in sheep. There was not clear evidence which species attracted or repelled the other; attraction between deer at long separation distances was stronger when the model accounted for thermal stress, but in general the dynamic movement behaviour was hardly affected by the thermal stress. Vegetation type affected intra-species interactions but had little effect on inter-species interactions. Our modelling approach is useful in interpreting animal interactions, in order to unravel complex cooperative or competitive behaviours, and to the best of our knowledge is the first modelling attempt to make predictions of multi-species animal movement under different habitat mosaics and abiotic environmental conditions.

Long-term density-dependent changes in habitat selection in red deer (Cervus elaphus).

Understanding how habitat selection changes with population density is a key concept in population regulation, community composition and managing impacts on biodiversity and ecosystem services. At low density, it is expected that individuals select habitats in terms of their preference, but as population density increases, the availability of resources per individual declines on preferred habitats, leading to competition which forces some individuals to exploit less preferred habitats. Using spatial information of Scottish red deer (Cervus elaphus) winter counts, carried out in 110 areas across Scotland between 1961 and 2004 (a total of 1,206,495 deer observations), we showed how winter habitat niche breadth in red deer has widened with increasing population density. Heather moorland and montane habitats were most and least preferred for deer, respectively. Increasing density favoured the selection of grassland, to the detriment of the selection of heather moorland. The selection of heather and grassland decreased when temperature increased, while the selection of montane and peatland habitats increased. These findings are important for understanding how habitat use, density and population are likely to be affected by weather, and allow us to predict habitat impacts by large mammal herbivory and climate.

Influenza virus h5 DNA vaccination is immunogenic by intramuscular and intradermal routes in humans.

Avian influenza virus causes outbreaks in domestic and wild birds around the world, and sporadic human infections have been reported. A DNA vaccine encoding hemagglutinin (HA) protein from the A/Indonesia/5/05 (H5N1) strain was initially tested in two randomized phase I clinical studies. Vaccine Research Center study 304 (VRC 304) was a double-blinded study with 45 subjects randomized to placebo, 1 mg of vaccine, or 4 mg of vaccine treatment groups (n = 15/group) by intramuscular (i.m.) Biojector injection. VRC 305 was an open-label study to evaluate route, with 44 subjects randomized to intradermal (i.d.) injections of 0.5 mg by needle/syringe or by Biojector or 1 mg delivered as two 0.5-mg Biojector injections in the same deltoid or as 0.5 mg in each deltoid (n = 11/group). Injections were administered at weeks 0, 4, and 8 in both studies. Antibody responses to H5 were assessed by hemagglutination inhibition (HAI) assay, enzyme-linked immunosorbent assay (ELISA), and neutralization assay, and the H5 T cell responses were assessed by enzyme-linked immunospot and intracellular cytokine staining assays. There were no vaccine-related serious adverse events, and the vaccine was well tolerated in all groups. At 1 mg, i.d. vaccination compared to i.m. vaccination induced a greater frequency and magnitude of response by ELISA, but there were no significant differences in the frequency or magnitude of response between the i.d. and i.m. routes in the HAI or neutralization assays. T cell responses were more common in subjects who received the 1- or 4-mg dose i.m. These studies demonstrated that the DNA vaccine encoding H5 is safe and immunogenic and served to define the proper dose and route for further studies. The i.d. injection route did not offer a significant advantage over the i.m. route, and no difference was detected by delivery to one site versus splitting the dose between two sites for i.d. vaccine administration. The 4-mg dose (i.m) was further investigated in prime-boost regimens.

Anthelmintic efficacy of five tropical native Australian plants against Haemonchus contortus and Trichostrongylus colubriformis in experimentally infected goats (Capra hircus).

The study of the anthelmintic properties of plants rich in plant secondary metabolites can provide ecologically sound methods for the treatment of parasites on grazing animals. The purpose of the present study was to evaluate the anthelmintic effect of five tropical native Australian plant species rich in plant secondary metabolites on adult Haemonchus contortus and Trichostrongylus colubriformis in experimentally infected goats. Thirty young, nematode-free goats were infected with 2500 H. contortus and 5000 T. colubriformis infective larvae thrice weekly for a week (day 1-7 of the experiment). On day 27 after first infection, the goats were allocated into six groups of five animals per group. From day 28 to day 35, fresh leaves from Acacia salicina, Acacia nilotica, Eucalyptus corymbia, Casuarina cunninghamiana and Eucalyptus drepanophylla were included in the goats diet. Five groups were offered leaves from one of these plant species and one group, the untreated control, received only the basal diet formulated with 20% Medicago sativa and 80% Avena sativa. Following plant material administration, the goats were monitored daily until day 40 and then slaughtered on day 41. Total faecal worm egg output, total production of larvae recovered from faecal cultures, total post-mortem worm burdens and the per capita fecundity of female worms were estimated. The toxicity of the plant species for the goats was measured by histopathological analyses of liver and kidney samples. Results showed that goats feeding on the plant material rich in plant secondary metabolites had significantly lower egg output compared to the control goats (P<0.05). A similar response was found for larval production in both H. contortus and T. colubriformis supporting that egg output was affected in both species. Although the total worm burdens were not affected by the plant material (P>0.05), the per capita fecundity was significantly reduced by E. corymbia, A. nilotica and A. salicina (P<0.05). No signs of toxicity were detected in the liver or kidney samples. It is concluded that goats can benefit from the short-term ingestion of plant secondary metabolites, which reduce the total faecal egg output and thus decrease the potential for re-infection from the pasture.

Variable extent of sex-biased dispersal in a strongly polygynous mammal.

For mammals with a polygynous mating system, dispersal is expected to be male-biased. However, with the increase in empirical studies, discrepancies are arising between the expected and observed direction/extent of the bias in dispersal. In this study, we assessed sex-biased dispersal in red deer (Cervus elaphus) on 13 estates from the Scottish Highlands. A total of 568 adult individuals were genotyped at 21 microsatellite markers and sequenced for 821 bp of the mitochondrial control region. Estimates of population structure with mitochondrial sequences were eight times larger than that obtained with microsatellite data (F(st'-mtDNA) = 0.831; F(st'-micros) = 0.096) indicating overall male-biased dispersal in the study area. Comparisons of microsatellite data between the sexes indicated a predominance of male-biased dispersal in the study area but values of F(ST) and relatedness were only slighter larger for females. Individual-based spatial autocorrelation analysis generated a similar pattern of relatedness across geographical distances for both sexes, with differences only significant at two distance intervals (25-30 and 70-112 km). Patterns of relatedness differed between estates, male biased-dispersal was detected in eight estates but no sex-biased dispersal was found in the remaining five. Neither population density nor landscape cover was found to be associated with the patterns of relatedness found across the estates. Differences in management strategies that could influence age structure, sex ratio and dispersal behaviour are proposed as potential factors influencing the relatedness patterns observed. This study provides new insights on dispersal of a strongly polygynous mammal at geographical scales relevant for management and conservation.

Influence of sward structure on daily intake and foraging behaviour by horses.

The spatial heterogeneity of grasslands determines the abundance and quality of food resources for grazing animals. As plants mature, they increase in mass, which allows greater instantaneous intake rates, but the cell wall concentrations increase too, reducing diet quality. In ruminants, daily intake rates are often constrained by the time needed for the ingesta to pass through the rumen, which is influenced by the rate of digestion. It has been suggested that the digestive constraint should have much less effect on hindgut fermenters such as equids. Horses play an increasing role in the management of grasslands in Europe, but the data on the influence of the heterogeneity of the vegetation on their daily intake and foraging behaviour are sparse. We report here the results of a preliminary study concerning the effects of sward structure on nutrient assimilation and the use of patches of different heights by horses grazing successively a short immature, a tall mature and a heterogeneous pastures (with short and tall swards). Daily nutrient assimilation was higher in the heterogeneous pasture compared to the short (+35%) and the tall (+55%) ones. The digestive constraints may have limited voluntary intake by horses on the tall swards. In the heterogeneous pasture, the mean height used for feeding (6 to 7 cm) by horses was intermediate between the heights used in the short (4 to 5 cm) and tall pastures (22 to 23 cm), and the animals may thus have benefited from both short swards of high quality and tall swards offering a higher instantaneous intake rate.

Genetic diversity and population structure of Scottish Highland red deer (Cervus elaphus) populations: a mitochondrial survey.

The largest population of red deer (Cervus elaphus) in Europe is found in Scotland. However, human impacts through hunting and introduction of foreign deer stock have disturbed the population's genetics to an unknown extent. In this study, we analysed mitochondrial control region sequences of 625 individuals to assess signatures of human and natural historical influence on the genetic diversity and population structure of red deer in the Scottish Highlands. Genetic diversity was high with 74 haplotypes found in our study area (115 x 87 km). Phylogenetic analyses revealed that none of the individuals had introgressed mtDNA from foreign species or subspecies of deer and only suggested a very few localized red deer translocations among British localities. A haplotype network and population analyses indicated significant genetic structure (Phi(ST)=0.3452, F(ST)=0.2478), largely concordant with the geographical location of the populations. Mismatch distribution analysis and neutrality tests indicated a significant population expansion for one of the main haplogroups found in the study area, approximately dated c. 8200 or 16 400 years ago when applying a fast or slow mutation rate, respectively. Contrary to general belief, our results strongly suggest that native Scottish red deer mtDNA haplotypes have persisted in the Scottish Highlands and that the population retains a largely natural haplotype diversity and structure in our study area.

Landscape features affect gene flow of Scottish Highland red deer (Cervus elaphus).

Landscape features have been shown to strongly influence dispersal and, consequently, the genetic population structure of organisms. Studies quantifying the effect of landscape features on gene flow of large mammals with high dispersal capabilities are rare and have mainly been focused at large geographical scales. In this study, we assessed the influence of several natural and human-made landscape features on red deer gene flow in the Scottish Highlands by analysing 695 individuals for 21 microsatellite markers. Despite the relatively small scale of the study area (115 x 87 km), significant population structure was found using F-statistics (F(ST) = 0.019) and the program structure, with major differentiation found between populations sampled on either side of the main geographical barrier (the Great Glen). To assess the effect of landscape features on red deer population structure, the ArcMap GIS was used to create cost-distance matrices for moving between populations, using a range of cost values for each of the landscape features under consideration. Landscape features were shown to significantly affect red deer gene flow as they explained a greater proportion of the genetic variation than the geographical distance between populations. Sea lochs were found to be the most important red deer gene flow barriers in our study area, followed by mountain slopes, roads and forests. Inland lochs and rivers were identified as landscape features that might facilitate gene flow of red deer. Additionally, we explored the effect of choosing arbitrary cell cost values to construct least cost-distance matrices and described a method for improving the selection of cell cost values for a particular landscape feature.

Voluntary intake and digestibility in horses: effect of forage quality with emphasis on individual variability.

Food intake is a key biological process in animals, as it determines the energy and nutrients available for the physiological and behavioural processes. In herbivores, the abundance, structure and quality of plant resources are known to influence intake strongly. In ruminants, as the forage quality declines, digestibility and total intake decline. Equids are believed to be adapted to consume high-fibre low-quality forages. As hindgut fermenters, it has been suggested that their response to a reduction in food quality is to increase intake to maintain rates of energy and nutrient absorption. All reviews of horse nutrition show that digestibility declines with forage quality; for intake, however, most studies have found no significant relationship with forage quality, and it has even been suggested that horses may eat less with declining forage quality similarly to ruminants. A weakness of these reviews is to combine data from different studies in meta-analyses without allowing the differences between animals and diets to be controlled for. In this study, we analysed a set of 45 trials where intake and digestibility were measured in 21 saddle horses. The dataset was analysed both at the group (to allow comparisons with the literature) and at the individual levels (to control for individual variability). As expected, dry matter digestibility declined with forage quality in both analyses. Intake declined slightly with increasing fibre contents at the group level, and there were no effects of crude protein or dry matter digestibility on intake. Overall, the analysis for individual horses showed a different pattern: intake increased as digestibility and crude protein declined, and increased with increasing fibre. Our analysis at the group level confirms previous reviews and shows that forage quality explains little of the variance in food intake in horses. For the first time, using mixed models, we show that the variable 'individual' clarifies the picture, as the horses showed different responses to a decrease in forage quality: some compensated for the low nutritional value of the forages by increasing intake, few others responded by decreasing intake with declining forage quality, but not enough to cause any deficit in their energy and protein supplies. On the whole, all the animals managed to meet their maintenance requirements. The individual variability may be a by-product of artificial selection for performance in competition in saddle horses.

How does pattern of feeding and rate of nutrient delivery influence conditioned food preferences?

Ruminant herbivores have been shown to learn about food properties by associating food flavours with the food's post-ingestive consequences. Previous experimentation supporting the conditioned food aversion/preference hypothesis has generally employed very simple diet learning tasks which do not effectively represent the wide range of foods selected within single bouts typical of wild, free-ranging ruminant herbivores. We tested the ability of a ruminant herbivore to associate a food with artificially administered nutrient rewards in a designed experiment where we altered the temporal pattern of encounter with the food as well as the nature (fast or slow reward) of the post-ingestive outcome. Twenty-four goats were offered branches of Sitka spruce (SS) and Norway spruce (NS) for 4 h per day on two days per week for five weeks. The pattern of feeding varied with treatment such that the species on offer changed every hour (short) or every 2 h (long). The energy treatment altered the reward delivered during Sitka consumption so that animals were dosed either with predominantly sugar (rapidly fermented), predominantly starch (slower fermentation rate), or with water (placebo). Preference was measured on the day following each learning day. We expected that goats would find it easier to associate SS with post-ingestive rewards when the duration of encounter was longest, and that associations would be stronger with the most rapidly digested post-ingestive reward. In the event, goats did not alter their consumption of SS in response to the treatments. Our results suggest that at the scale of temporal resolution of encounters with different plant species (1-2 h), and at the different rates of experiencing post-ingestive consequences tested in this experiment, ruminants do not appear to discriminate the nutritive properties of foods predominantly through a post-ingestive feedback mechanism. They must, instead, use a range of cues-including post-ingestive consequences-to assess food properties.

Having it all: historical energy intakes do not generate the anticipated trade-offs in fecundity.

An axiom of life-history theory, and fundamental to our understanding of ageing, is that animals must trade-off their allocation of resources since energy and nutrients are limited. Therefore, animals cannot "have it all"--combine high rates of fecundity with extended lifespans. The idea of life-history trade-offs was recently challenged by the discovery that ageing may be governed by a small subset of molecular processes independent of fitness. We tested the "trade-off" and "having it all" theories by examining the fecundities of C57BL/6J mice placed onto four different dietary treatments that generated caloric intakes from -21 to +8.6% of controls. We predicted body fat would be deposited in relation to caloric intake. Excessive body fat is known to cause co-morbidities that shorten lifespan, while caloric restriction enhances somatic protection and increases longevity. The trade-off model predicts that increased fat would be tolerated because reproductive gain offsets shortened longevity, while animals on a restricted intake would sacrifice reproduction for lifespan extension. The responses of body fat to treatments followed our expectations, however, there was a negative relationship between reproductive performance (fecundity, litter mass) and historical intake/body fat. Our dietary restricted animals had lower protein oxidative damage and appeared able to combine life-history traits in a manner contrary to traditional expectations by having increased fecundity with the potential to have extended lifespans.

The evolution of phylogenetic differences in the efficiency of digestion in ruminants.

This study investigates, for the first time (to our knowledge) for any animal group, the evolution of phylogenetic differences in fibre digestibility across a wide range of feeds that differ in potential fibre digestibility (fibre to lignin ratio) in ruminants. Data, collated from the literature, were analysed using a linear mixed model that allows for different sources of random variability, covariates and fixed effects, as well as controlling for phylogenetic relatedness. This approach overcomes the problem of defining boundaries to separate different ruminant feeding styles (browsers, mixed feeders and grazers) by using two covariates that describe the browser-grazer continuum (proportion of grass and proportion of browse in the natural diet of a species). The results indicate that closely related species are more likely to have similar values of fibre digestibility than species that are more distant in the phylogenetic tree. Body mass did not have any significant effect on fibre digestibility. Fibre digestibility is estimated to increase with the proportion of grass and to decrease with the proportion of browse in the natural diet that characterizes the species. We applied an evolutionary model to infer rates of evolution and ancestral states of fibre digestibility; the model indicates that the rate of evolution of fibre digestibility accelerated across time. We suggest that this could be caused by a combination of increasing competition among ruminant species and adaptation to diets rich in fibre, both related to climatically driven environmental changes in the past few million years.

Incomplete sexual isolation in sympatry between subspecies of the butterfly Danaus chrysippus (L.) and the creation of a hybrid zone.

Subspecies chrysippus, dorippus and alcippus of the butterfly Danaus chrysippus differ at three biallelic colour gene loci. They have partially vicariant distributions, but their ranges overlap over a substantial part of central and East Africa, where hybridism is commonplace. We now report that the West African subspecies alcippus differs from other subspecies, not only in nuclear genotype but also in mitochondrial haplotype in both allopatry and sympatry. The maintenance of concordant nuclear and cytoplasmic genetic differences in sympatry, and in the face of hybridisation, is prima facie evidence for sexual isolation. Other evidence that suggests alcippus may be isolated from chrysippus and dorippus include differences in sex ratio (SR), heterozygote deficiency at one site and deduced differences in patterns of migration. We suggest that, within the hybrid zone, differential infection of subspecies by a male-killing Spiroplasma bacterium causes SR differences that restrict female choice, triggering rounds of heterotypic mating and consequent heterozygote excess that is largely confined to females. The absence of these phenomena from hybrid populations that test negative for Spiroplasma supports the hypothesis. The incomplete sexual isolation and partial vicariance of alcippus suggests that it is a nascent species.

The origins of sexual dimorphism in body size in ungulates.

Jarman (1974) proposed a series of relationships between habitat use, food dispersion, and social behavior and hypothesized a series of evolutionary steps leading to sexual dimorphism in body size through sexual selection in African antelope species. The hypothesis states that sexual size dimorphism evolved in a three-step process. Initially, ancestral monomorphic and monogamous ungulate species occupying closed habitats radiated into open grassland habitats. Polygynous mating systems then rapidly evolved in response to the aggregation of males and females, perhaps in relation to the clumped distribution of food resources in open habitats. Subsequently, size dimorphism evolved in those species occupying open habitats, but not in species that remained in closed habitats or retained monogamy. This hypothesis has played an important role in explaining the origins of sexual dimorphism in mammals. However, the temporal sequence of the events that Jarman proposed has never been demonstrated. Here we use a phylogeny of extant ungulate species, along with maximum-likelihood statistical techniques, to provide a test of Jarman's hypothesis.