Effects of warming on predator–prey interactions – a resource‐based approach and a theoretical synthesis

We theoretically explore consequences of warming for predator–prey dynamics, broadening previous approaches in three ways: we include beyond‐optimal temperatures, predators may have a type III functional response, and prey carrying capacity depends on explicitly modelled resources. Several robust patterns arise. The relationship between prey carrying capacity and temperature can range from near‐independence to monotonically declining/increasing to hump‐shaped. Predators persist in a U‐shaped region in resource supply (=enrichment)‐temperature space. Type II responses yield stable persistence in a U‐shaped band inside this region, giving way to limit cycles with enrichment at all temperatures. In contrast, type III responses convey stability at intermediate temperatures and confine cycles to low and high temperatures. Warming‐induced state shifts can be predicted from system trajectories crossing stability and persistence boundaries in enrichment‐temperature space. Results of earlier studies with more restricted assumptions map onto this graph as special cases. Our approach thus provides a unifying framework for understanding warming effects on trophic dynamics.     

A high‐throughput FTIR spectroscopy approach to assess adaptive variation in the chemical composition of pollen

The two factors defining male reproductive success in plants are pollen quantity and quality, but our knowledge about the importance of pollen quality is limited due to methodological constraints. Pollen quality in terms of chemical composition may be either genetically fixed for high performance independent of environmental conditions, or it may be plastic to maximize reproductive output under different environmental conditions. In this study, we validated a new approach for studying the role of chemical composition of pollen in adaptation to local climate. The approach is based on high‐throughput Fourier infrared (FTIR) characterization and biochemical interpretation of pollen chemical composition in response to environmental conditions. The study covered three grass species, Poa alpina, Anthoxanthum odoratum, and Festuca ovina. For each species, plants were grown from seeds of three populations with wide geographic and climate variation. Each individual plant was divided into four genetically identical clones which were grown in different controlled environments (high and low levels of temperature and nutrients). In total, 389 samples were measured using a high‐throughput FTIR spectrometer. The biochemical fingerprints of pollen were species and population specific, and plastic in response to different environmental conditions. The response was most pronounced for temperature, influencing the levels of proteins, lipids, and carbohydrates in pollen of all species. Furthermore, there is considerable variation in plasticity of the chemical composition of pollen among species and populations. The use of high‐throughput FTIR spectroscopy provides fast, cheap, and simple assessment of the chemical composition of pollen. In combination with controlled‐condition growth experiments and multivariate analyses, FTIR spectroscopy opens up for studies of the adaptive role of pollen that until now has been difficult with available methodology. The approach can easily be extended to other species and environmental conditions and has the potential to significantly increase our understanding of plant male function.     

CHIIMP: An automated high‐throughput microsatellite genotyping platform reveals greater allelic diversity in wild chimpanzees

Short tandem repeats (STRs), also known as microsatellites, are commonly used to noninvasively genotype wild‐living endangered species, including African apes. Until recently, capillary electrophoresis has been the method of choice to determine the length of polymorphic STR loci. However, this technique is labor intensive, difficult to compare across platforms, and notoriously imprecise. Here we developed a MiSeq‐based approach and tested its performance using previously genotyped fecal samples from long‐term studied chimpanzees in Gombe National Park, Tanzania. Using data from eight microsatellite loci as a reference, we designed a bioinformatics platform that converts raw MiSeq reads into locus‐specific files and automatically calls alleles after filtering stutter sequences and other PCR artifacts. Applying this method to the entire Gombe population, we confirmed previously reported genotypes, but also identified 31 new alleles that had been missed due to sequence differences and size homoplasy. The new genotypes, which increased the allelic diversity and heterozygosity in Gombe by 61% and 8%, respectively, were validated by replicate amplification and pedigree analyses. This demonstrated inheritance and resolved one case of an ambiguous paternity. Using both singleplex and multiplex locus amplification, we also genotyped fecal samples from chimpanzees in the Greater Mahale Ecosystem in Tanzania, demonstrating the utility of the MiSeq‐based approach for genotyping nonhabituated populations and performing comparative analyses across field sites. The new automated high‐throughput analysis platform (available at https://github.com/ShawHahnLab/chiimp ) will allow biologists to more accurately and effectively determine wildlife population size and structure, and thus obtain information critical for conservation efforts.     

Mismatch in microbial food webs: predators but not prey perform better in their local biotic and abiotic conditions

Understanding how trophic levels respond to changes in abiotic and biotic conditions is key for predicting how food webs will react to environmental perturbations. Different trophic levels may respond disproportionately to change, with lower levels more likely to react faster, as they typically consist of smaller‐bodied species with higher reproductive rates. This response could cause a mismatch between trophic levels, in which predators and prey will respond differently to changing abiotic or biotic conditions. This mismatch between trophic levels could result in altered top‐down and bottom‐up control and changes in interaction strength. To determine the possibility of a mismatch, we conducted a reciprocal‐transplant experiment involving Sarracenia purpurea food webs consisting of bacterial communities as prey and a subset of six morphologically similar protozoans as predators. We used a factorial design with four temperatures, four bacteria and protozoan biogeographic origins, replicated four times. This design allowed us to determine how predator and prey dynamics were altered by abiotic (temperature) conditions and biotic (predators paired with prey from either their local or non‐local biogeographic origin) conditions. We found that prey reached higher densities in warmer temperature regardless of their temperature of origin. Conversely, predators achieved higher densities in the temperature condition and with the prey from their origin. These results confirm that predators perform better in abiotic and biotic conditions of their origin while their prey do not. This mismatch between trophic levels may be especially significant under climate change, potentially disrupting ecosystem functioning by disproportionately affecting top‐down and bottom‐up control.     

A novel approach to parasite population genetics: Experimental infection reveals geographic differentiation,recombination and host‐mediated population structure in Pasteuria ramosa,a bacterial parasite of Daphnia

The population structure of parasites is central to the ecology and evolution of host‐parasite systems. Here, we investigate the population genetics of Pasteuria ramosa, a bacterial parasite of Daphnia. We used natural P. ramosa spore banks from the sediments of two geographically well‐separated ponds to experimentally infect a panel of Daphnia magna host clones whose resistance phenotypes were previously known. In this way, we were able to assess the population structure of P. ramosa based on geography, host resistance phenotype and host genotype. Overall, genetic diversity of P. ramosa was high, and nearly all infected D. magna hosted more than one parasite haplotype. On the basis of the observation of recombinant haplotypes and relatively low levels of linkage disequilibrium, we conclude that P. ramosa engages in substantial recombination. Isolates were strongly differentiated by pond, indicating that gene flow is spatially restricted. Pasteuria ramosa isolates within one pond were segregated completely based on the resistance phenotype of the host—a result that, to our knowledge, has not been previously reported for a nonhuman parasite. To assess the comparability of experimental infections with natural P. ramosa isolates, we examined the population structure of naturally infected D. magna native to one of the two source ponds. We found that experimental and natural infections of the same host resistance phenotype from the same source pond were indistinguishable, indicating that experimental infections provide a means to representatively sample the diversity of P. ramosa while reducing the sampling bias often associated with studies of parasite epidemics. These results expand our knowledge of this model parasite, provide important context for the large existing body of research on this system and will guide the design of future studies of this host‐parasite system.     

A robust,high‐throughput method for computing maize ear,cob, and kernel attributes automatically from images

Grain yield of the maize plant depends on the sizes, shapes, and numbers of ears and the kernels they bear. An automated pipeline that can measure these components of yield from easily‐obtained digital images is needed to advance our understanding of this globally important crop. Here we present three custom algorithms designed to compute such yield components automatically from digital images acquired by a low‐cost platform. One algorithm determines the average space each kernel occupies along the cob axis using a sliding‐window Fourier transform analysis of image intensity features. A second counts individual kernels removed from ears, including those in clusters. A third measures each kernel's major and minor axis after a Bayesian analysis of contour points identifies the kernel tip. Dimensionless ear and kernel shape traits that may interrelate yield components are measured by principal components analysis of contour point sets. Increased objectivity and speed compared to typical manual methods are achieved without loss of accuracy as evidenced by high correlations with ground truth measurements and simulated data. Millimeter‐scale differences among ear, cob, and kernel traits that ranged more than 2.5‐fold across a diverse group of inbred maize lines were resolved. This system for measuring maize ear, cob, and kernel attributes is being used by multiple research groups as an automated Web service running on community high‐throughput computing and distributed data storage infrastructure. Users may create their own workflow using the source code that is staged for download on a public repository.     

Future warmer seas: increased stress and susceptibility to grazing in seedlings of a marine habitat‐forming species

Increases in seawater temperature are expected to have negative consequences for marine organisms. Beyond individual effects, species‐specific differences in thermal tolerance are predicted to modify species interactions and increase the strength of top‐down effects, particularly in plant–herbivore interactions. Shifts in trophic interactions will be especially important when affecting habitat‐forming species such as seagrasses, as the consequences on their abundance will cascade throughout the food web. Seagrasses are a major component of coastal ecosystems offering important ecosystem services, but are threatened by multiple anthropogenic stressors, including warming. The mechanistic understanding of seagrass responses to warming at multiple scales of organization remains largely unexplored, especially in early‐life stages such as seedlings. Yet, these early‐life stages are critical for seagrass expansion processes and adaptation to climate change. In this study, we determined the effects of a 3 month experimental exposure to present and predicted mean summer SST of the Mediterranean Sea (25°C, 27°C, and 29°C) on the photophysiology, size, and ecology (i.e., plant‐herbivore interactions) of seedlings of the seagrass Posidonia oceanica. Warming resulted in increased mortality, leaf necrosis, and respiration as well as lower carbohydrate reserves in the seed, the main storage organ in seedlings. Aboveground biomass and root growth were also limited with warming, which could hamper seedling establishment success. Furthermore, warming increased the susceptibility to consumption by grazers, likely due to lower leaf fiber content and thickness. Our results indicate that warming will negatively affect seagrass seedlings through multiple direct and indirect pathways: increased stress, reduced establishment potential, lower storage of carbohydrate reserves, and increased susceptibly to consumption. This work provides a significant step forward in understanding the major mechanisms that will drive the capacity of seagrass seedlings to adapt and survive to warming, highlighting the potential additive effects that herbivory will have on ultimately determining seedling success.     

Silicon amendment to rice plants contributes to reduced feeding in a phloem‐sucking insect through modulation of callose deposition

Silicon (Si) uptake by Poaceae plants has beneficial effects on herbivore defense. Increased plant physical barrier and altered herbivorous feeding behaviors are documented to reduce herbivorous arthropod feeding and contribute to enhanced plant defense. Here, we show that Si amendment to rice (Oryza sativa) plants contributes to reduced feeding in a phloem feeder, the brown planthopper (Nilaparvata lugens, BPH), through modulation of callose deposition. We associated the temporal dynamics of BPH feeding with callose deposition on sieve plates and further with callose synthase and hydrolase gene expression in plants amended with Si. Biological assays revealed that BPH feeding was lower in Si‐amended than in nonamended plants in the early stages post‐BPH infestation. Histological observation showed that BPH infestation triggered fast and strong callose deposition in Si‐amended plants compared with nonamended plants. Analysis using qRT‐PCR revealed that expression of the callose synthase gene OsGSL1 was up‐regulated more and that the callose hydrolase (β‐1,3‐glucanase) gene Gns5 was up‐regulated less in Si‐amended than in nonamended plants during the initial stages of BPH infestation. These dynamic expression levels of OsGSL1 and Gns5 in response to BPH infestation correspond to callose deposition patterns in Si‐amended versus nonamended plants. It is demonstrated here that BPH infestation triggers differential gene expression associated with callose synthesis and hydrolysis in Si‐amended and nonamended rice plants, which allows callose to be deposited more on sieve tubes and sieve tube occlusions to be maintained more thus contributing to reduced BPH feeding on Si‐amended plants.     

Linking predator–prey interactions with exposure to a trophically transmitted parasite using PCR‐based analyses

Parasite transmission is determined by the rate of contact between a susceptible host and an infective stage and susceptibility to infection given an exposure event. Attempts to measure levels of variation in exposure in natural populations can be especially challenging. The level of exposure to a major class of parasites, trophically transmitted parasites, can be estimated by investigating the host's feeding behaviour. Since the parasites rely on the ingestion of infective intermediate hosts for transmission, the potential for exposure to infection is inherently linked to the definitive host's feeding ecology. Here, we combined epidemiological data and molecular analyses (polymerase chain reaction) of the diet of the definitive host, the white‐footed mouse (Peromyscus leucopus), to investigate temporal and individual heterogeneities in exposure to infection. Our results show that the consumption of cricket intermediate hosts accounted for much of the variation in infection; mice that had consumed crickets were four times more likely to become infected than animals that tested negative for cricket DNA. In particular, pregnant female hosts were three times more likely to consume crickets, which corresponded to a threefold increase in infection compared with nonpregnant females. Interestingly, males in breeding condition had a higher rate of infection even though breeding males were just as likely to test positive for cricket consumption as nonbreeding males. These results suggest that while heterogeneity in host diet served as a strong predictor of exposure risk, differential susceptibility to infection may also play a key role, particularly among male hosts. By combining PCR analyses with epidemiological data, we revealed temporal variation in exposure through prey consumption and identified potentially important individual heterogeneities in parasite transmission.     

RAD‐sequencing for estimating genomic relatedness matrix‐based heritability in the wild: A case study in roe deer

Estimating the evolutionary potential of quantitative traits and reliably predicting responses to selection in wild populations are important challenges in evolutionary biology. The genomic revolution has opened up opportunities for measuring relatedness among individuals with precision, enabling pedigree‐free estimation of trait heritabilities in wild populations. However, until now, most quantitative genetic studies based on a genomic relatedness matrix (GRM) have focused on long‐term monitored populations for which traditional pedigrees were also available, and have often had access to knowledge of genome sequence and variability. Here, we investigated the potential of RAD‐sequencing for estimating heritability in a free‐ranging roe deer (Capreolous capreolus) population for which no prior genomic resources were available. We propose a step‐by‐step analytical framework to optimize the quality and quantity of the genomic data and explore the impact of the single nucleotide polymorphism (SNP) calling and filtering processes on the GRM structure and GRM‐based heritability estimates. As expected, our results show that sequence coverage strongly affects the number of recovered loci, the genotyping error rate and the amount of missing data. Ultimately, this had little effect on heritability estimates and their standard errors, provided that the GRM was built from a minimum number of loci (above 7,000). Genomic relatedness matrix‐based heritability estimates thus appear robust to a moderate level of genotyping errors in the SNP data set. We also showed that quality filters, such as the removal of low‐frequency variants, affect the relatedness structure of the GRM, generating lower h² estimates. Our work illustrates the huge potential of RAD‐sequencing for estimating GRM‐based heritability in virtually any natural population.     

Integrating stable isotopes,parasite, and ring‐reencounter data to quantify migratory connectivity—A case study with Barn Swallows breeding in Switzerland,Germany, Sweden,and Finland

Ecosystems around the world are connected by seasonal migration. The migrant animals themselves are influenced by migratory connectivity through effects on the individual and the population level. Measuring migratory connectivity is notoriously difficult due to the simple requirement of data conveying information about the nonbreeding distribution of many individuals from several breeding populations. Explicit integration of data derived from different methods increases the precision and the reliability of parameter estimates. We combine ring‐reencounter, stable isotope, and blood parasite data of Barn Swallows Hirundo rustica in a single integrated model to estimate migratory connectivity for three large scale breeding populations across a latitudinal gradient from Central Europe to Scandinavia. To this end, we integrated a non‐Markovian multistate mark‐recovery model for the ring‐reencounter data with normal and binomial mixture models for the stable isotope and parasite data. The integration of different data sources within a mark‐recapture modeling framework enables the most precise quantification of migratory connectivity on the given broad spatial scale. The results show that northern‐breeding populations and Southern Africa as well as southern‐breeding populations and Western–Central Africa are more strongly connected through Barn Swallow migration than central European breeding populations with any of the African wintering areas. The nonbreeding distribution of Barn Swallows from central European breeding populations seems to be a mixture of those populations breeding further north and south, indicating a migratory divide.     

Stage‐dependent responses to emergent habitat heterogeneity: consequences for a predatory insect population in a coffee agroecosystem

Interactions among members of biological communities can create spatial patterns that effectively generate habitat heterogeneity for other members in the community, and this heterogeneity might be crucial for their persistence. For example, stage‐dependent vulnerability of a predatory lady beetle to aggression of the ant, Azteca instabilis, creates two habitat types that are utilized differently by the immature and adult life stages of the beetle. Due to a mutualistic association between A. instabilis and the hemipteran Coccus viridis – which is A. orbigera main prey in the area – only plants around ant nests have high C. viridis populations. Here, we report on a series of surveys at three different scales aimed at detecting how the presence and clustered distribution of ant nests affect the distribution of the different life stages of this predatory lady beetle in a coffee farm in Chiapas, Mexico. Both beetle adults and larvae were more abundant in areas with ant nests, but adults were restricted to the peripheries of highest ant activity and outside the reach of coffee bushes containing the highest densities of lady beetle larvae. The abundance of adult beetles located around trees with ants increased with the size of the ant nest clusters but the relationship is not significant for larvae. Thus, we suggest that A. orbigera undergoes an ontogenetic niche shift, not through shifting prey species, but through stage‐specific vulnerability differences against a competitor that renders areas of abundant prey populations inaccessible for adults but not for larvae. Together with evidence presented elsewhere, this study shows how an important predator is not only dependent on the existence of two qualitatively distinct habitat types, but also on the spatial distribution of these habitats. We suggest that this dependency arises due to the different responses that the predator's life stages have to this emergent spatial pattern.