Effects of seasonality and previous logging on faecal helminth-microbiota associations in wild lemurs.

Gastrointestinal helminth-microbiota associations are shaped by various ecological processes. The effect of the ecological context of the host on the bacterial microbiome and gastrointestinal helminth parasites has been tested in a number of ecosystems and experimentally. This study takes the important step to look at these two groups at the same time and to start to examine how these communities interact in a changing host environment. Fresh faecal samples (N = 335) from eight wild Eulemur populations were collected over 2 years across Madagascar. We used 16S ribosomal RNA gene sequencing to characterise the bacterial microbiota composition, and faecal flotation to isolate and morphologically identify nematode eggs. Infections with nematodes of the genera Callistoura and Lemuricola occurred in all lemur populations. Seasonality significantly contributed to the observed variation in microbiota composition, especially in the dry deciduous forest. Microbial richness and Lemuricola spp. infection prevalence were highest in a previously intensely logged site, whereas Callistoura spp. showed no such pattern. In addition, we observed significant correlations between gastrointestinal parasites and bacterial microbiota composition in these lemurs, with 0.4-0.7% of the variation in faecal bacterial microbiota composition being explained by helminth infections. With this study, we show effects of environmental conditions on gastrointestinal nematodes and bacterial interactions in wild lemurs and believe it is essential to consider the potential role of microbiome-parasite associations on the hosts' GI stability, health, and survival.

Inferring an animal's environment through biologging: quantifying the environmental influence on animal movement.

BACKGROUND: Animals respond to environmental variation by changing their movement in a multifaceted way. Recent advancements in biologging increasingly allow for detailed measurements of the multifaceted nature of movement, from descriptors of animal movement trajectories (e.g., using GPS) to descriptors of body part movements (e.g., using tri-axial accelerometers). Because this multivariate richness of movement data complicates inference on the environmental influence on animal movement, studies generally use simplified movement descriptors in statistical analyses. However, doing so limits the inference on the environmental influence on movement, as this requires that the multivariate richness of movement data can be fully considered in an analysis. METHODS: We propose a data-driven analytic framework, based on existing methods, to quantify the environmental influence on animal movement that can accommodate the multifaceted nature of animal movement. Instead of fitting a simplified movement descriptor to a suite of environmental variables, our proposed framework centres on predicting an environmental variable from the full set of multivariate movement data. The measure of fit of this prediction is taken to be the metric that quantifies how much of the environmental variation relates to the multivariate variation in animal movement. We demonstrate the usefulness of this framework through a case study about the influence of grass availability and time since milking on cow movements using machine learning algorithms. RESULTS: We show that on a one-hour timescale 37% of the variation in grass availability and 33% of time since milking influenced cow movements. Grass availability mostly influenced the cows' neck movement during grazing, while time since milking mostly influenced the movement through the landscape and the shared variation of accelerometer and GPS data (e.g., activity patterns). Furthermore, this framework proved to be insensitive to spurious correlations between environmental variables in quantifying the influence on animal movement. CONCLUSIONS: Not only is our proposed framework well-suited to study the environmental influence on animal movement; we argue that it can also be applied in any field that uses multivariate biologging data, e.g., animal physiology, to study the relationships between animals and their environment. SUPPLEMENTARY INFORMATION: Supplementary information accompanies this paper at 10.1186/s40462-020-00228-4.

Disease transmission in animal transfer networks.

Infectious diseases transmission is strongly determined by who contacts whom. Bovine tuberculosis (bTB) caused by Mycobacterium bovis is a worldwide burden for animal populations. One of the major transmission mechanism between herd is the transfer of infectious animal. In East Africa, pastoralists may receive or bestow livestock to create and strengthen social relationships. Here, we used a network approach to examine the relative importance of such cattle transfer in the transmission of bTB. First, a total of 2550 cattle from 102 herds were tested using the comparative intradermal tuberculin test to assess the presence of bTB infected cattle in the herd. A herd was considered bTB positive if it had at least one tuberculin reactor animal. Next, we calculated the centrality of each herd in the cattle transfer network using four established measures of social network centralization: degree, betweenness, closeness and fragmentation. The relationships between the network centrality measures and bTB infection were examined using generalized linear mixed models (GLMM). We found that a herd's in-degree in the social network was positively correlated with the risk of being infected with bTB (b=4.2, 95%CI=2.1-5.7; p<0.001). A herd that was close to many others (i.e., had a higher closeness index) had a larger chance of acquiring bTB infection (b=2.1, 95%CI=1.4-2.8; p<0.001). Betweenness centrality was also positively associated with the presence of bTB infection. There was a negative relationship between the fragmentation index and bTB infection (b=-2.7, 95%CI=-4.9-1.3; p<0.001). The study clearly demonstrated that the extent to which a herd is connected within a network has significant implications for its probability of being infected. Further, the results are in accordance with our expectation that connectivity and the probability that a herd will transmit the disease to other herds in the network are related.

Competition between a Lawn-Forming Cynodon dactylon and a Tufted Grass Species Hyparrhenia hirta on a South-African Dystrophic Savanna.

South African savanna grasslands are often characterised by indigestible tufted grass species whereas lawn grasses are far more desirable in terms of herbivore sustenance. We aimed to investigate the role of nutrients and/or the disturbance (grazing, trampling) by herbivores on the formation of grazing lawns. We conducted a series of common garden experiments to test the effect of nutrients on interspecific competition between a typical lawn-forming grass species (Cynodon dactylon) and a species that is frequently found outside grazing lawns (Hyparrhenia hirta), and tested for the effect of herbivore disturbance in the form of trampling and clipping. We also performed a vegetation and herbivore survey to apply experimentally derived insights to field observations. Our results showed that interspecific competition was not affected by soil nutrient concentrations. C. dactylon did show much more resilience to disturbance than H. hirta, presumably due to the regenerative capacity of its rhizomes. Results from the field survey were in line with these findings, describing a correlation between herbivore pressure and C. dactylon abundance. We conclude that herbivore disturbance, and not soil nutrients, provide C. dactylon with a competitive advantage over H. hirta, due to vegetative regeneration from its rhizomes. This provides evidence for the importance of concentrated, high herbivore densities for the creation and maintenance of grazing lawns.

Dilution effect and identity effect by wildlife in the persistence and recurrence of bovine tuberculosis.

Current theories on disease-diversity relationships predict a strong influence of host richness on disease transmission. In addition, identity effect, caused by the occurrence of particular species, can also modify disease risk. We tested the richness effect and the identity effects of mammal species on bovine tuberculosis (bTB), based on the regional bTB outbreak data in cattle from 2005-2010 in Africa. Besides, we also tested which other factors were associated with the regional bTB persistence and recurrence in cattle. Our results suggested a dilution effect, where higher mammal species richness (MSR) was associated with reduced probabilities of bTB persistence and recurrence in interaction with cattle density. African buffalo had a positive effect on bTB recurrence and a positive interaction effect with cattle density on bTB persistence, indicating an additive positive identity effect of buffalo. The presence of greater kudu had no effect on bTB recurrence or bTB persistence. Climatic variables only act as risk factors for bTB persistence. In summary, our study identified both a dilution effect and identity effect of wildlife and showed that bTB persistence and recurrence were correlated with different sets of risk factors. These results are relevant for more effective control strategies and better targeted surveillance measures in bTB.

Larger antelopes are sensitive to heat stress throughout all seasons but smaller antelopes only during summer in an African semi-arid environment.

Heat stress can limit the activity time budget of ungulates due to hyperthermia, which is relevant for African antelopes in ecosystems where temperature routinely increases above 40 °C. Body size influences this thermal sensitivity as large bodied ungulates have a lower surface area to volume ratio than smaller ungulates, and therefore a reduced heat dissipation capacity. We tested whether the activity pattern during the day of three antelope species of different body size-eland, blue wildebeest and impala-is negatively correlated with the pattern of black globe temperature (BGT) during the day of the ten hottest days and each season in a South African semi-arid ecosystem. Furthermore, we tested whether the larger bodied eland and wildebeest are less active than the smaller impala during the hottest days and seasons. Our results show that indeed BGT was negatively correlated with the diurnal activity of eland, wildebeest and impala, particularly during summer. During spring, only the activity of the larger bodied eland and wildebeest was negatively influenced by BGT, but not for the smallest of the three species, the impala. We argue that spring, with its high heat stress, coupled with poor forage and water availability, could be critical for survival of these large African antelopes. Our study contributes to understanding how endothermic animals can cope with extreme climatic conditions, which are expected to occur more frequently due to climate change.

Genetic consequences of breaking migratory traditions in barnacle geese Branta leucopsis.

Cultural transmission of migratory traditions enables species to deal with their environment based on experiences from earlier generations. Also, it allows a more adequate and rapid response to rapidly changing environments. When individuals break with their migratory traditions, new population structures can emerge that may affect gene flow. Recently, the migratory traditions of the Barnacle Goose Branta leucopsis changed, and new populations differing in migratory distance emerged. Here, we investigate the population genetic structure of the Barnacle Goose to evaluate the consequences of altered migratory traditions. We used a set of 358 single nucleotide polymorphism (SNP) markers to genotype 418 individuals from breeding populations in Greenland, Spitsbergen, Russia, Sweden and the Netherlands, the latter two being newly emerged populations. We used discriminant analysis of principal components, FST , linkage disequilibrium and a comparison of geneflow models using migrate-n to show that there is significant population structure, but that relatively many pairs of SNPs are in linkage disequilibrium, suggesting recent admixture between these populations. Despite the assumed traditions of migration within populations, we also show that genetic exchange occurs between all populations. The newly established nonmigratory population in the Netherlands is characterized by high emigration into other populations, which suggests more exploratory behaviour, possibly as a result of shortened parental care. These results suggest that migratory traditions in populations are subject to change in geese and that such changes have population genetic consequences. We argue that the emergence of nonmigration probably resulted from developmental plasticity.

Genome-wide single nucleotide polymorphism analysis reveals recent genetic introgression from domestic pigs into Northwest European wild boar populations.

Present-day genetic introgression from domestic pigs into European wild boar has been suggested in various studies. However, no hybrids have been identified beyond doubt mainly because available methods were unable to quantify the extent of introgression and rule out natural processes. Genetic introgression from domestic pigs may have far-reaching ecological consequences by altering traits like the reproduction rate or immunology of wild boar. In this study, we demonstrate a novel approach to investigate genetic introgression in a Northwest (NW) European wild boar data set using a genome-wide single nucleotide polymorphism (SNP) assay developed for domestic pigs. We quantified the extent of introgression using allele frequency spectrum analysis, in silico hybridization simulations and genome distribution patterns of introgressed SNPs. Levels of recent introgression in the study area were expected to be low, as pig farming practices are prevailingly intensive and indoors. However, evidence was found for geographically widespread presence of domestic pig SNPs in 10% of analysed wild boar. This was supported by the identification of two different pig mitochondrial DNA haplotypes in three of the identified hybrid wild boar, suggesting that introgression had occurred from multiple sources (pig breeds). In silico hybridization simulations showed that the level of introgression in the identified hybrid wild boar is equivalent to first-generation hybrids until fifth-generation backcrosses with wild boar. The distribution pattern of introgressed SNPs supported these assignments in four of nine hybrids. The other five hybrids are considered advanced-generation hybrids, resulting from interbreeding among hybrid individuals. Three of nine hybrids were genetically associated with a different wild boar population than the one in which they were sampled. This discrepancy suggests that genetic introgression has occurred through the escape or release of an already hybridized farmed wild boar stock. We conclude that genetic introgression from domestic pigs into NW European wild boar populations is more recent and more common than expected and that genome-wide SNP analysis is a promising tool to quantify recent hybridization in free-living populations.

Spatial autocorrelation and the scaling of species-environment relationships.

Issues of residual spatial autocorrelation (RSA) and spatial scale are critical to the study of species-environment relationships, because RSA invalidates many statistical procedures, while the scale of analysis affects the quantification of these relationships. Although these issues independently are widely covered in the literature, only sparse attention is given to their integration. This paper focuses on the interplay between RSA and the spatial scaling of species-environment relationships. Using a hypothetical species in an artificial landscape, we show that a mismatch between the scale of analysis and the scale of a species' response to its environment leads to a decrease in the portion of variation explained by environmental predictors. Moreover, it results in RSA and biased regression coefficients. This bias stems from error-predictor dependencies due to the scale mismatch, the magnitude of which depends on the interaction between the scale of landscape heterogeneity and the scale of a species' response to this heterogeneity. We show that explicitly considering scale effects on RSA can reveal the characteristic scale of a species' response to its environment. This is important, because the estimation of species-environment relationships using spatial regression methods proves to be erroneous in case of a scale mismatch, leading to spurious conclusions when scaling issues are not explicitly considered. The findings presented here highlight the importance of examining the appropriateness of the spatial scales used in analyses, since scale mismatches affect the rigor of statistical analyses and thereby the ability to understand the processes underlying spatial patterning in ecological phenomena.

Tree cover and biomass increase in a southern African savanna despite growing elephant population.

The growing elephant populations in many parts of southern Africa raise concerns of a detrimental loss of trees, resulting in overall reduction of biodiversity and ecosystem functioning. Elephant distribution and density can be steered through artificial waterpoints (AWPs). However, this leaves resident vegetation no relief during dry seasons. We studied how the introduction of eight AWPs in 1996 affected the spatiotemporal tree-structure dynamics in central Chobe National Park, an unfenced savanna area in northern Botswana with a dry-season elephant density of approximately 3.34 individuals per square kilometer. We hypothesized that the impact of these AWPs amplified over time and expanded in space, resulting in a decrease in average tree density, tree height, and canopy volume. We measured height and canopy dimensions of all woody plants around eight artificial and two seasonal waterpoints for 172 plots in 1997, 2000, and 2008. Plots, consisting of 50 x 2 m transects for small trees (0.20-3.00 m tall) nested within 50 x 20 m transects for large trees (> or = 3.0 m tall), were located at 100, 500, 1000, 2000, and 5000 m distance classes. A repeated-measures mixed-effect model showed that tree density, cover, and volume had increased over time throughout the area, caused by a combination of an increase of trees in lower size classes and a decrease in larger size classes. Our results indicate that the decrease of large trees can be attributed to a growing elephant population. Decrease or loss of particular tree size classes may have been caused by a loss of browser-preferred species while facilitating the competitiveness of less-preferred species. In spite of 12 years of artificial water supply and an annual elephant population growth of 6%, we found no evidence that the eight AWPs had a negative effect on tree biomass or tree structure. The decreasing large-tree component could be a remainder of a depleted but currently restoring elephant population.

Hydraulic lift in Acacia tortilis trees on an East African savanna.

Recent studies suggest that savanna trees in semi-arid areas can increase understorey plant production. We hypothesized that one of the mechanisms that explains the facilitation between trees and grasses in East African savannas is hydraulic lift (HL). HL in large Acacia tortilis trees was studied during the first 3 months of the dry season during a relatively wet year (1998) and a very dry year (2000). In 1998, we found distinct diel fluctuation in soil water potential (psi(s)), with increasing values during the night and decreasing again the following day. These fluctuations in psi(s )are consistent with other observations of HL and in A. tortilis were found up to 10 m from the tree. In 2000, during a severe drought, psi(s) measurements indicated that HL was largely absent. The finding that HL occurred in wetter years and not in drier years was supported by data obtained on the delta(18)O values in soil, rain and groundwater. The delta(18)O of water extracted from the xylem water of grasses indicated that when they grew near trees they had values similar to those of groundwater. This could be because they either (1) use water from deeper soil layers or (2) use hydraulically lifted water provided by the tree; this was not seen in the same grass species growing outside tree canopies. While our data indicate that HL indeed occurs under Acacia trees, it is also true that psi(s) was consistently lower under trees when compared to outside tree canopies. We believe that this is because tree-grass mixtures take up more water from the upper soil layers than is exuded by the tree each night. This limits the beneficial effect of HL for understorey grasses and suggests that in savannas both facilitation via HL and competition are active processes. The importance of each process may depend upon how wet or dry that particular site or year is.

Phylogeography of the African buffalo based on mitochondrial and Y-chromosomal loci: Pleistocene origin and population expansion of the Cape buffalo subspecies.

Population genetics and phylogeography of the African buffalo (Syncerus caffer) are inferred from genetic diversity at mitochondrial D-loop hypervariable region I sequences and a Y-chromosomal microsatellite. Three buffalo subspecies from different parts of Africa are included. Nucleotide diversity of the subspecies Cape buffalo at hypervariable region I is high, with little differentiation between populations. A mutation rate of 13-18% substitutions/million years is estimated for hypervariable region I. The nucleotide diversity indicates an estimated female effective population size of 17 000-32 000 individuals. Both mitochondrial and Y-chromosomal diversity are considerably higher in buffalo from central and southwestern Africa than in Cape buffalo, for which several explanations are hypothesized. There are several indications that there was a late middle to late Pleistocene population expansion in Cape buffalo. This also seems to be the period in which Cape buffalo evolved as a separate subspecies, according to the net sequence divergence with the other subspecies. These two observations are in agreement with the hypothesis of a rapid evolution of Cape buffalo based on fossil data. Additionally, there appears to have been a population expansion from eastern to southern Africa, which may be related to vegetation changes. However, as alternative explanations are also possible, further analyses with autosomal loci are needed.

Microsatellite analysis of genetic diversity in African buffalo (Syncerus caffer) populations throughout Africa.

Genetic diversity in nine African buffalo (Syncerus caffer) populations throughout Africa was analysed with 14 microsatellites to study the effects of rinderpest epidemics and habitat fragmentation during the 20th century. A gradient of declining expected heterozygosity was observed among populations in Save Valley Conservancy (Zimbabwe), and northern and southern Kruger National Park (South Africa). This was explained by a high mortality in northern Kruger National Park during the rinderpest pandemic at the end of the 19th century followed by recolonization from neighbouring populations, resulting in intermediate heterozygosity levels in northern Kruger National Park. In other populations expected heterozygosity was very high, indicating that rinderpest and recent habitat fragmentation had a limited effect on genetic diversity. From expected heterozygosity, estimates of long-term effective population size were derived. Migration rates among populations in eastern and southern Africa were very high, as shown by a weak isolation by distance and significant correlation in allele frequencies between populations. However, there were indications that dry habitats could limit migration. Genetic distances within buffalo in central Africa were relatively large, supporting their status as distinct subspecies. Finally, it was observed that the higher polymorphic microsatellites were less sensitive at detecting isolation by distance and differences in Ne, which may be a result of the high mutation pressure at these loci.

Applicability of bovine microsatellite markers for population genetic studies on African buffalo (Syncerus caffer).

The applicability of bovine autosomal microsatellite markers for population genetic studies on African buffalo was investigated. A total of 168 microsatellite markers were tested for PCR amplification on a test panel of seven African buffalo. Amplification was observed for 139 markers (83%), and 101 markers were studied further with 91 (90%) being polymorphic. The mean number of alleles per marker was 5.0 (SE = 0.2) and the mean heterozygosity per marker was 0.61 (SE = 0.03). Considering the overall high level of polymorphism, it was concluded that most bovine microsatellite markers are applicable in African buffalo.

African buffalo maintain high genetic diversity in the major histocompatibility complex in spite of historically known population bottlenecks.

Historical population collapses caused by rinderpest epidemics are hypothesized to have resulted in notable genetic losses in populations of the African buffalo. Polymorphism in the major histocompatibity complex (MHC) DRB3 gene was probed by means of restriction analysis of the sequence encoding the peptide-binding region. Nucleotide substitution patterns agreed with a positive selection acting on this fitness-relevant locus. Buffalo populations from four National Parks, situated in eastern and southern Africa, each revealed a surprisingly high allelic diversity. Current high levels of heterozygosity may be reconciled with historical bottlenecks by assuming that local extinctions were followed by fast recolonization, in accordance with the high dispersive capabilities of buffalo. The specific amplification of DRB3 alleles also enabled the assignment of individual genotypes. For each population sample a deficiency in the expected number of heterozygous animals was found. As overdominant selection on the MHC is predicted to yield an excess of heterozygous individuals, this may not be a locus-specific effect. Several other explanations are discussed, of which increased homozygosity caused by nonrandom mating of buffalo in populations seems the most probable.

Large herbivores that strive mightily but eat and drink as friends.

Grazing in patches of Cynodon dactylon and of Sporobolus spicatus by four large herbivores, and the interaction between these sedentary herbivores was studied in Lake Manyara National Park, northern Tanzania. The herbivores were the African buffalo, Syncerus caffer; the African elephan, Loxodonta africana; the Burchell's zebra, Equus burchelli; and the wildebeest, Connochaetus taurinus. Four different hypotheses of the interactions between the herbivores were tested, viz., increased predator detection/protection through association of species, facilitation of the food intake through the influence of other species, use by other species of the food manipulation strategy of buffalo, and interspecific competition for food. On the level of a single day, zebra and wildebeest were symbiotic, which could have been caused by an increased chance of predator detection. A similar association between buffalo and wildebeest or zebra was also detected on C. dactylon grasslands. There was no indication of facilitation between any of the herbivores. Buffalo had a despotic relationship with elephant, that is the elephant's consumption was lowered when buffalo had visited a patch prior to their arrival. When elephant and buffalo arrived at the same time there appeared to be scramble competition between them.Habitat overlap was calculated for four pairs of species. In conjunction with the analyses of the patch visits, it was concluded that a small overlap was associated with interspecific competition and a large habitat overlap was associated with symbiosis.

Stability in a multi-species assemblage of large herbivores in East Africa.

Animal census data from Lake Manyara National Park in northern Tanzania are presented. The data refer to large mammalian herbivores, that is individually heavier than twenty kg, of which the numbers were counted in nine different years between 1959 and 1984. The total biomass of these herbivores was comprised mainly of African buffalo and African elephant. Five functional groups of herbivores were distinguished (buffalo, "elephant-as-grazer", "elephant-as-browser", "other grazers", and "other browsers"). The pressures of all these groups were constant over time with the exception of that by buffalo. Buffalo numbers increased since the last outbreak of rinderpest in 1959. There was no correlation between herbivore biomass and rainfall fluctuations. Individual species showed large fluctuations in their numbers but within the total herbivore assemblage the different species compensated the fluctuations of the other species. This resulted in an overall constancy of herbivore biomass, and, thus, the carrying capacity of the system has to be viewed on the level of all species combined and not on that of the individual species. This view is supported by the result that size of the stability index showed that the system of herbivore species was stable.

Vegetation growth and a seasonal habitat shift of the barnacle goose (Branta leucopsis).

Barnacle geese (Branta leucopsis) wintering on the island of Schiermonnikoog in the Netherlands abruptly switch all their foraging activities from a dairy pasture (a 'polder') to an adjacent salt-marsh during the early spring. We present evidence to show that this shift is related to changes in the quality of the diet available in these different habitats. Barnacle geese shift from polder to salt-marsh at the precise time that these are equal in dietary protein availability, which occurs as the food plants on the salt-marsh undergo a sudden spring growth. The dairy pasture undergoes its own spring growth shortly afterwards, and more dietary protein is available there for the rest of the year. We suggest that the salt-marsh is a more preferred habitat, but that low dietary protein during the winter prevents its use by barnacle geese. We hypothesize that the salt-marsh may be more preferred due to a lower level of disturbance which permits geese to graze more slowly, improving the utilization of food plants.