Moving forward with the primate microbiome: Introduction to a special issue of the American Journal of Primatology

Primate microbiome research is a quickly growing field with exciting potential for informing our understanding of primate biology, ecology, and evolution as well as host‐microbe interactions more broadly. This introductory essay to a special section of the American Journal of Primatology provides a cross‐sectional snapshot of current activity in these areas by briefly summarizing the diversity of contributed papers and their relationships to key themes in host‐associated microbiome research. It then uses this survey as a foundation for consolidating a set of key research questions to broadly guide future research. It also argues for the importance of methods standardization to facilitate comparative analyses and the identification of generalizable patterns and relationships. While primatology will benefit greatly from the integration of microbial datasets, it is uniquely positioned to address important questions regarding microbiology and macro‐ecology and evolution more generally. We are eager to see where the primate microbiome leads us.     

Effects of a participatory approach,with systematic impact matrix analysis in herd health planning in organic dairy cattle herds

The animal health and welfare status in European organic dairy production does not in all aspects meet the organic principles and consumers’ expectations and needs to be improved. To achieve this, tailored herd health planning, targeted to the specific situation of individual farms could be of use. The aim of this study was to apply herd health planning in a structured participatory approach, with impact matrix analysis, not previously used in this context, in European organic dairy farms and to assess changes in animal health and welfare. Herd health planning farm visits were conducted on 122 organic dairy farms in France, Germany and Sweden. The farmer, the herd veterinarian and/or an advisor took part in the farm discussions. The researcher served as facilitator. Baseline data on the animal health status of the individual farm, collected from national milk recording schemes, were presented as an input for the discussion. Thereafter a systematic impact matrix analysis was performed. This was to capture the complexity of individual farms with the aim to identify the farm-specific factors that could have a strong impact on animal health. The participants (i.e. farmer, veterinarian and advisor) jointly identified areas in need of improvement, taking the health status and the interconnected farm system components into account, and appropriate actions were jointly identified. The researcher took minutes during the discussions, and these were shared with the participants. No intervention was made by the researcher, and further actions were left with the participants. The number of actions per farm ranged from 0 to 22. The change in mortality, metabolic diseases, reproductive performance and udder health was assessed at two time points, and potential determinators of the change were evaluated with linear regression models. A significant association was seen between change in udder health, as measured by the somatic cell count, and country. At the first follow-up, a significant association was also found between change in the proportion of prolonged calving interval and the farmers’ desire to improve reproductive health as well as with an increase in herd size, but this was not seen at the second follow-up. The degree of implementation of the actions was good (median 67%, lower quartile 40%, upper quartile 83%). To conclude, the degree of implementation was quite high, improvement of animal health could not be linked to the herd health planning approach. However, the approach was highly appreciated by the participants and deserves further study.     

Co‐occurrence patterns of trees along macro‐climatic gradients and their potential influence on the present and future distribution of Fagus sylvatica L.

Aim During recent and future climate change, shifts in large‐scale species ranges are expected due to the hypothesized major role of climatic factors in regulating species distributions. The stress‐gradient hypothesis suggests that biotic interactions may act as major constraints on species distributions under more favourable growing conditions, while climatic constraints may dominate under unfavourable conditions. We tested this hypothesis for one focal tree species having three major competitors using broad‐scale environmental data. We evaluated the variation of species co‐occurrence patterns in climate space and estimated the influence of these patterns on the distribution of the focal species for current and projected future climates. Location Europe. Methods We used ICP Forest Level 1 data as well as climatic, topographic and edaphic variables. First, correlations between the relative abundance of European beech (Fagus sylvatica) and three major competitor species (Picea abies, Pinus sylvestris and Quercus robur) were analysed in environmental space, and then projected to geographic space. Second, a sensitivity analysis was performed using generalized additive models (GAM) to evaluate where and how much the predicted F. sylvatica distribution varied under current and future climates if potential competitor species were included or excluded. We evaluated if these areas coincide with current species co‐occurrence patterns. Results Correlation analyses supported the stress‐gradient hypothesis: towards favourable growing conditions of F. sylvatica, its abundance was strongly linked to the abundance of its competitors, while this link weakened towards unfavourable growing conditions, with stronger correlations in the south and at low elevations than in the north and at high elevations. The sensitivity analysis showed a potential spatial segregation of species with changing climate and a pronounced shift of zones where co‐occurrence patterns may play a major role. Main conclusions Our results demonstrate the importance of species co‐occurrence patterns for calibrating improved species distribution models for use in projections of climate effects. The correlation approach is able to localize European areas where inclusion of biotic predictors is effective. The climate‐induced spatial segregation of the major tree species could have ecological and economic consequences.     

Plant–animal interactions between carnivorous plants,sheet‐web spiders,and ground‐running spiders as guild predators in a wet meadow community

1. Plant–animal interactions are diverse and widespread shaping ecology, evolution, and biodiversity of most ecological communities. Carnivorous plants are unusual in that they can be simultaneously engaged with animals in multiple mutualistic and antagonistic interactions including reversed plant–animal interactions where they are the predator. Competition with animals is a potential antagonistic plant–animal interaction unique to carnivorous plants when they and animal predators consume the same prey.
2. The goal of this field study was to test the hypothesis that under natural conditions, sundews and spiders are predators consuming the same prey thus creating an environment where interkingdom competition can occur.
3. Over 12 months, we collected data on 15 dates in the only protected Highland Rim Wet Meadow Ecosystem in Kentucky where sundews, sheet‐web spiders, and ground‐running spiders co‐exist. One each sampling day, we attempted to locate fifteen sites with: (a) both sheet‐web spiders and sundews; (b) sundews only; and (c) where neither occurred. Sticky traps were set at each of these sites to determine prey (springtails) activity–density. Ground‐running spiders were collected on sampling days. DNA extraction was performed on all spiders to determine which individuals had eaten springtails and comparing this to the density of sundews where the spiders were captured.
4. Sundews and spiders consumed springtails. Springtail activity–densities were lower, the higher the density of sundews. Both sheet‐web and ground‐running spiders were found less often where sundew densities were high. Sheet‐web size was smaller where sundew densities were high.
5. The results of this study suggest that asymmetrical exploitative competition occurs between sundews and spiders. Sundews appear to have a greater negative impact on spiders, where spiders probably have little impact on sundews. In this example of interkingdom competition where the asymmetry should be most extreme, amensalism where one competitor experiences no cost of interaction may be occurring.

     

Haematobia irritans parasitism of F1 yak × beef cattle (Bos grunniens × Bos taurus) hybrids

The horn fly Haematobia irritans (Diptera: Muscidae) is a blood obligate ectoparasite of bovids that causes annual losses to the U.S. beef cattle industry of over US$1.75 billion. Climate warming, the anthropogenic dispersion of bovids and the cross‐breeding of beef cattle with other bovid species may facilitate novel horn fly–host interactions. In particular, hybridizing yaks [Bos grunniens (Artiodactyla: Bovidae)] with beef cows (Bos taurus) for heterosis and carcass improvements may increase the exposure of yak × beef hybrids to horn flies. The present paper reports on the collection of digital images of commingled beef heifers (n = 12) and F1 yak × beef hybrid bovids (heifers, n = 7; steers, n = 5) near Laramie, Wyoming (～ 2200 m a.s.l.) in 2018. The total numbers of horn flies on beef heifers and F1 yak × beef heifers [mean ± standard error (SE): 88 ± 13 and 70 ± 17, respectively] did not differ significantly; however, F1 yak × beef steers had greater total horn fly abundance (mean ± SE: 159 ± 39) than female bovids. The present report of this experiment is the first such report in the literature and suggests that F1 yak × beef bovids are as susceptible as cattle to horn fly parasitism. Therefore, similar monitoring and treatment practices should be adopted by veterinarians, entomologists and producers.     

Providing straw to allow exploratory behaviour in a pig experimental system does not modify putative indicators of positive welfare: peripheral oxytocin and serotonin

Numerous studies have shown that providing straw to pigs can reduce undesirable behaviours such as aggression, tail biting and stereotypy. The measurement of various neuromodulators can be helpful in assessing the development of positive behaviours and overall animal welfare. The oxytocin release is frequently linked to positive emotions and positive welfare. It has been suggested that oxytocin modulates the serotoninergic system. This study aims to investigate the potential effect of straw provision in pigs on peripheral levels of oxytocin and serotonin. In total, 18 mini-pigs were involved in an exploratory study conducted in two parallel groups, Enriched (n=10) and Control (n=8) groups. Pigs were divided by group and housed in pens of two individuals. Straw was provided continuously only in Enriched group and renewed each day for 2 weeks. Two blood samples were drawn from each animal 5 to 10 min before providing the straw, and 15 min after providing straw, during the 1^st week, to analyse peripheral changes in oxytocin and serotonin before and after straw provision, and determine the existence of a putative short-term effect. The same procedure was carried out for Control group, without straw provision. Long-term effects of straw provision were also examined using blood samples drawn at the same hour from each animal in the 2^nd and 3^rd weeks. During this time, animals had the permanent possibility to explore the straw in Enriched group but not in Control group. At the end of each week, one animal-keeper completed two visual analogue scales for each mini-pig regarding the difficulty/ease to work with and handle it and its trust in humans. Results showed peripheral oxytocin increases in both groups after 2 weeks (P=0.02). Results did not demonstrate any effect of providing straw to allow exploratory behaviour on peripheral serotonin. Other results were not significant. This preliminary study explored the relationship between peripheral oxytocin and serotonin and the presence of straw that allow pigs to perform exploratory behaviour, suggesting that there was no relationship between them. Some future studies may include crossing oxytocin and serotonin with other parameters, such as behavioural measures, to obtain more information about the true state of the animal and any possible relationship with pig welfare.     

Messy eaters: Swabbing prey DNA from the exterior of inconspicuous predators when foraging cannot be observed

Complex coevolutionary relationships among competitors, predators, and prey have shaped taxa diversity, life history strategies, and even the avian migratory patterns we see today. Consequently, accurate documentation of prey selection is often critical for understanding these ecological and evolutionary processes. Conventional diet study methods lack the ability to document the diet of inconspicuous or difficult‐to‐study predators, such as those with large home ranges and those that move vast distances over short amounts of time, leaving gaps in our knowledge of trophic interactions in many systems. Migratory raptors represent one such group of predators where detailed diet studies have been logistically challenging. To address knowledge gaps in the foraging ecology of migrant raptors and provide a broadly applicable tool for the study of enigmatic predators, we developed a minimally invasive method to collect dietary information by swabbing beaks and talons of raptors to collect trace prey DNA. Using previously published COI primers, we were able to isolate and reference gene sequences in an open‐access barcode database to identify prey to species. This method creates a novel avenue to use trace molecular evidence to study prey selection of migrating raptors and will ultimately lead to a better understanding of raptor migration ecology. In addition, this technique has broad applicability and can be used with any wildlife species where even trace amounts of prey debris remain on the exterior of the predator after feeding.     

Effects of light-emitting diode light v. fluorescent light on growing performance,activity levels and well-being of non-beak-trimmed W-36 pullets

More energy-efficient, readily dimmable, long-lasting and more affordable light-emitting diode (LED) lights are increasingly finding applications in poultry production facilities. Despite anecdotal evidence about the benefits of such lighting on bird performance and behavior, concrete research data were lacking. In this study, a commercial poultry-specific LED light (dim-to-blue, controllable correlated color temperature (CCT) from 4500 to 5300 K) and a typical compact fluorescent light (CFL) (soft white, CCT=2700 K) were compared with regards to their effects on growing performance, activity levels, and feather and comb conditions of non-beak-trimmed W-36 pullets during a 14-week rearing period. A total of 1280-day-old pullets in two successive batches, 640 birds each, were used in the study. For each batch, pullets were randomly assigned to four identical litter-floor rooms equipped with perches, two rooms per light regimen, 160 birds per room. Body weight, BW uniformity (BWU), BW gain (BWG) and cumulative mortality rate (CMR) of the pullets were determined every 2 weeks from day-old to 14 weeks of age (WOA). Activity levels of the pullets at 5 to 14 WOA were delineated by movement index. Results revealed that pullets under the LED and CFL lights had comparable BW (1140±5 g v. 1135±5 g, P=0.41), BWU (90.8±1.0% v. 91.9±1.0%, P=0.48) and CMR (1.3±0.6% v. 2.7±0.6%, P=0.18) at 14 WOA despite some varying BWG during the rearing. Circadian activity levels of the pullets were higher under the LED light than under the CFL light, possibly resulting from differences in spectrum and/or perceived light intensity between the two lights. No feather damage or comb wound was apparent in either light regimen at the end of the rearing period. The results contribute to understanding the impact of emerging LED lights on pullets rearing which is a critical component of egg production.