Life History Variation Research Articles

Host genomic influence on bacterial composition in the switchgrass rhizosphere.

Host genetic variation can shape the diversity and composition of associated microbiomes, which may reciprocally influence host traits and performance. While the genetic basis of phenotypic diversity of plant populations in nature has been studied, comparatively little research has investigated the genetics of host effects on their associated microbiomes. Switchgrass (Panicum virgatum) is a highly outcrossing, perennial, grass species with substantial locally adaptive diversity across its native North American range. Here, we compared 383 switchgrass accessions in a common garden to determine the host genotypic influence on rhizosphere bacterial composition. We hypothesized that the composition and diversity of rhizosphere bacterial assemblages would differentiate due to genotypic differences between hosts (potentially due to root phenotypes and associated life history variation). We observed higher alpha diversity of bacteria associated with upland ecotypes and tetraploids, compared to lowland ecotypes and octoploids, respectively. Alpha diversity correlated negatively with flowering time and plant height, indicating that bacterial composition varies along switchgrass life history axes. Narrow-sense heritability (h2 ) of the relative abundance of 21 core bacterial families was observed. Overall compositional differences among tetraploids, due to genetic variation, supports widespread genotypic influence on the rhizosphere microbiome. Tetraploids were only considered due to complexities associated with the octoploid genomes. Lastly, a genome-wide association study identified 1861 single-nucleotide polymorphisms associated with 110 families and genes containing them related to potential regulatory functions. Our findings suggest that switchgrass genomic and life-history variation influences bacterial composition in the rhizosphere, potentially due to host adaptation to local environments.

High within-clutch repeatability of eggshell phenotype in Barn Swallows despite less maculated last-laid eggs

Abstract Ecological and life-history variation and both interspecific and intraspecific brood parasitism contribute to diversity in egg phenotype within the same species. In this study, Barn Swallows (Hirundo rustica erythrogaster) laid eggs with high intraclutch repeatability in egg size, shape, and maculation. Despite this high intraclutch repeatability, last-laid eggs had consistently less of the eggshell covered in spots and fewer spots than earlier-laid eggs in the clutch. We examined sources of interclutch and intraclutch variation using both direct measurements and custom software (SpotEgg, NaturePatternMatch) that provide detailed information on egg characteristics, especially maculation measures. In addition to our main findings, maculation on different sides of the egg was highly repeatable; however, only shape, proportion of the eggshell maculated, and average spot size were repeatable between first and replacement clutches. Low intraclutch variation in maculation could allow females to recognize their clutch and this may be adaptive for colonial nesting species, such as the Barn Swallow. Characterizing intraspecific variation in egg size, shape, and maculation is the first step in understanding whether intraclutch variation is low enough—and interclutch variation high enough—such that eggs could serve as identity signals.

Diverse migration tactics of fishes within the large tropical Mekong River system

AbstractFish often migrate to feed, reproduce and seek refuge from predators and prevailing environmental conditions. As a result, migration tactics often vary among species based on a diversity of life history needs, although variation within species is increasingly being recognised as important to population resilience. In this study, within‐ and among‐species diversity in life history migratory tactics of six Mekong fish genera was examined using otolith microchemistry to explore diadromous and potamodromous traits. Two species were catadromous and one species was an estuarine resident, while the remaining three species were facultative in their migration strategies, with up to four tactics within a single species. Migrant and resident contingents co‐existed within the same species. Management, conservation and mitigation strategies that maintain connectivity in large tropical rivers, such as effective fishway design, should consider a diversity of migration tactics at the individual level for improved outcomes.

Life history consequences of climate change in hibernating mammals: a review

Climatic shifts to warmer and often drier conditions are challenging terrestrial species worldwide. These shifts are occurring more rapidly at higher elevations and latitudes, likely causing disproportionate effects to mammalian hibernators there. While there is some information about how these species' ranges are responding to climatic shifts, we lack an understanding of how climate components are affecting species' life history variation, which is key to individual success and population‐level resilience. We reviewed the literature to identify the direction of life history responses to climate change in mammalian hibernators along three axes: latitudinal, elevational and temporal. We found 39 studies involving 27 species that reported climate effects on our four target life history traits – phenology, body mass/condition and growth, reproduction and survival. We found warmer temperatures are advancing hibernator phenology and increasing reproductive success. By contrast, warming and drying trends are having uncertain effects on body condition, and complex effects on survival – depending on season, age class, latitude and elevation. We found no pattern of significant climate‐trait outcomes by duration or decade of study. More research on drought conditions – particularly in relation to resource availability – would help inform hibernator susceptibility to increased drying trends expected to intensify globally. Notably, our results are highly biased towards small mammal hibernators in Northern Hemisphere alpine/mountain ecosystems, with few long‐term studies conducted on Southern Hemisphere hibernators. This review highlights that phenological shifts constitute one of the most obvious consequences of climate change, yet, the timing of life history events (e.g. timing of migration, reproduction, hibernation) remains poorly understood. Further integration of insights from physiologists, evolutionary biologists and population ecologists working on wild populations will improve our collective understanding of the effects of seasonal climatic shifts on mammalian hibernator life history traits, key drivers of their population‐level persistence.

Intraspecific variation in migration timing of green sturgeon in the Sacramento River system

AbstractUnderstanding movement patterns of anadromous fishes is critical to conservation and management of declining wild populations and preservation of habitats. Yet, the duration of observations for individual animals can constrain accurate descriptions of movements. In this study, we synthesized over a decade (2006–2018) of acoustic telemetry tracking observations of green sturgeon (Acipenser medirostris) in the Sacramento River system to describe major anadromous movement patterns. We observed that green sturgeon exhibited a unimodal in‐migration during the spring months but had a bimodal distribution of out‐migration timing, split between an “early” out‐migration (32%) group during May–June, or, alternatively, holding in the river until a “late” out‐migration (68%), November–January. Focusing on these out‐migration groups, we found that river discharge, but not water temperature, may cue the timing of migration and that fish showed a tendency to maintain out‐migration timing between subsequent spawning migration events. We recommend that life history descriptions of green sturgeon in this region reflect the distinct out‐migration periods described here. Furthermore, we encourage the continued use of biotelemetry to describe migration timing and life history variation, in not only this population but also other green sturgeon populations and other species.

Human pathogenic RNA viruses establish noncompeting lineages by occupying independent niches

Many pathogenic viruses are endemic among human populations and can cause a broad variety of diseases, some potentially leading to devastating pandemics. How virus populations maintain diversity and what selective pressures drive population turnover is not thoroughly understood. We conducted a large-scale phylodynamic analysis of 27 human pathogenic RNA viruses spanning diverse life history traits, in search of unifying trends that shape virus evolution. For most virus species, we identify multiple, cocirculating lineages with low turnover rates. These lineages appear to be largely noncompeting and likely occupy semiindependent epidemiological niches that are not regionally or seasonally defined. Typically, intralineage mutational signatures are similar to interlineage signatures. The principal exception are members of the family Picornaviridae, for which mutations in capsid protein genes are primarily lineage defining. Interlineage turnover is slower than expected under a neutral model, whereas intralineage turnover is faster than the neutral expectation, further supporting the existence of independent niches. The persistence of virus lineages appears to stem from limited outbreaks within small communities, so that only a small fraction of the global susceptible population is infected at any time. As disparate communities become increasingly connected through globalization, interaction and competition between lineages might increase as well, which could result in changing selective pressures and increased diversification and/or pathogenicity. Thus, in addition to zoonotic events, ongoing surveillance of familiar, endemic viruses appears to merit global attention with respect to the prevention or mitigation of future pandemics.

Polygenic discrimination of migratory phenotypes in an estuarine forage fish.

Migration is a complex phenotypic trait with some species containing migratory and nonmigratory individuals. Such life history variation may be attributed in part to plasticity, epigenetics, or genetics. Although considered semianadromous, recent studies using otolith geochemistry have revealed life history variation within the critically endangered Delta Smelt. Broadly categorizable as migratory or freshwater residents, we examined Restriction site Associated DNA sequencing data to test for a relationship between genetic variation and migratory behaviors. As previously shown, we found no evidence for neutral population genetic structure within Delta Smelt; however, we found significant evidence for associations between genetic variants and life history phenotypes. Furthermore, discriminant analysis of principal components, hierarchical clustering, and machine learning resulted in accurate assignment of fish into the freshwater resident or migratory classes based on their genotypes. These results suggest the presence of adaptive genetic variants relating to life history variation within a panmictic population. Mechanisms that may lead to this observation are genotype dependent habitat choice and spatially variable selection, both of which could operate each generation and are not exclusive. Given that the population of cultured Delta Smelt are being used as a refugial population for conservation, as a supply for wild population supplementation, and currently represent the majority of all living individuals of this species, we recommend that the hatchery management strategy consider the frequencies of life history-associated alleles and how to maintain this important aspect of Delta Smelt biological variation while under captive propagation.

Stream size, temperature, and density explain body sizes of freshwater salmonids across a range of climate conditions

Climate change and anthropogenic activities are altering the body sizes of fishes, yet our understanding of factors influencing body size for many taxa remains incomplete. We evaluated the relationships between climate, environmental, and landscape attributes and the body size of different taxa of freshwater trout (Salmonidae) in the USA. Hierarchical spatial modeling across a gradient of habitats (5221 sites) illustrated the importance of watershed effects, which explained 17%–45% of the of the variation in body size across taxa. Stream size had a strong, positive relationship with body size, yet there was approximately tenfold difference in the strength of the relationship across taxa. Trout body size consistently declined with increasing density across taxa. Despite reliance on cold water, we found positive relationships between summer stream temperature and trout body size across most taxa. Our results highlight how providing trout access to larger, productive rivers for the expression of growth and life-history variation would promote body size diversity within and across populations.

Huntsman spider phylogeny informs evolution of life history, egg sacs, and morphology

Huntsman spiders (Araneae: Sparassidae) are among the most speciose spider families, with a near-worldwide distribution, diverse habitats, equally diverse life histories, and five prolonged subsocial species. Previous molecular phylogenies have focused on individual subfamilies or clades. Here, we provide a phylogenetic inference with broadened sampling from 37 genera and eight of the eleven sparassid subfamilies. We increased taxon sampling by including species not previously sequenced and most available data on GenBank of two mitochondrial (COI, 16S rRNA) and two nuclear (H3, 28S rRNA) genes for a total of 262 ingroup taxa and nine outgroup taxa. Divergence dates were estimated using outgroup fossil taxa suggesting the sparassids evolved ∼ 100 mya (stem age), while the clade containing all subfamilies except Sparianthinae evolved ∼ 90 mya (stem age). Using a stochastic map approach with 40 species, this is the first sparassid phylogeny to incorporate extensive biology and life history data. Correlations of life history traits with solitary, subsocial, and prolonged subsocial behavior are examined using the D-test. Sparassid sociality is associated with life history traits that allow developing spiders to remain in their natal retreat longer (e.g., larger permanent retreats, plastered egg sacs, and ontogenetically delayed foraging), but is unrelated to body size or lifespan. Detailed morphological scoring of the endemic Australian subfamily Deleninae contextualizes existing molecular data, including in the Isopeda-Holconia-Isopedella complex. This study supports the monophyly of many major lineages, including for the first time, the Sparianthinae, but indicates multiple clades (Sparassinae and Eusparassinae) are paraphyletic and need further revision.

Neocalanus cristatus (Copepoda) From a Deep Sediment-Trap: Abundance and Implications for Ecological and Biogeochemical Studies

We studied seasonal variations of the mesozooplankton swimmer community collected by a sediment trap moored at 873 m in the Kuroshio–Oyashio Transition region off the east coast of Japan from 5 August 2011 to 23 June 2013, with sampling bottles rotating at 26-day intervals. The total flux of mesozooplankton swimmers varied between 0 and 11.1 individuals m–2 d–1, with a mean of 3.1 individuals m–2 d–1 during the sampling period. In total, 89 taxa were found in the trap material, of which copepods comprised 87.1% of all swimmers on average. Among the Copepoda, Neocalanus cristatus was the most dominant taxon (76.2% of copepods on average during the sampling period), and all of them were stage C5 copepodite to adult. The species composition of the swimmers closely reflected the mesopelagic mesozooplankton of the Oyashio region. Because all N. cristatus observed in the trap were stage C5 to adult, its flux represents a time series of variations in life history and response to environmental changes at the depth of the sediment trap. The fluxes of Neocalanus species (N. cristatus, N. flemingeri, and N. plumchrus) reflected ontogenetic vertical migration, but may have been overestimates of active fluxes if they included dormant individuals that accidentally entered the sediment trap. The apparent active carbon flux of Neocalanus species ranged from 0 to 22.3 mg C m–2 d–1 during the sampling period, with a mean value of 4.9 mg C m–2 d–1.

Exceptional longevity in northern peripheral populations of Wels catfish (Silurus glanis)

Studies of life-history variation across a species range are crucial for ecological understanding and successful conservation. Here, we examined the growth and age of Wels catfish (Silurus glanis) in Sweden, which represent the northernmost populations in Europe. A total of 1183 individuals were captured, marked and released between 2006 and 2020. Mark-recapture data from 162 individuals (size range: 13–195 cm) were used to estimate von Bertalanffy growth curve parameters which revealed very slow growth rates compared to catfish within the core distribution area (central Europe). The fitted von Bertalanffy growth curve predicted a 150 cm catfish to be around 40 years old, while the largest recaptured individual (length 195 cm) was estimated to be 70 (95% CI 50–112) years old. This was substantially older than the previously documented maximum age of a catfish. The weight at length relationships in these northern peripheral populations were similar to those documented for catfish in central Europe indicating that resources did not constrain growth. This indicates that the slow growth and exceptional high age in the northern catfish populations are the result of lower temperatures and/or local adaptations.

Maternally transferred thyroid hormones and life-history variation in birds.

In vertebrates, thyroid hormones (THs) play an important role in the regulation of growth, development, metabolism, photoperiodic responses and migration. Maternally transferred THs are important for normal early phase embryonic development when embryos are not able to produce endogenous THs. Previous studies have shown that variation in maternal THs within the physiological range can influence offspring phenotype.Given the essential functions of maternal THs in development and metabolism, THs may be a mediator of life‐history variation across species.We tested the hypothesis that differences in life histories are associated with differences in maternal TH transfer across species. Using birds as a model, we specifically tested whether maternally transferred yolk THs covary with migratory status, developmental mode and traits related to pace‐of‐life (e.g. basal metabolic rate, maximum life span).We collected un‐incubated eggs (n = 1–21 eggs per species, median = 7) from 34 wild and captive bird species across 17 families and six orders to measure yolk THs [both triiodothyronine (T3) and thyroxine (T4)], compiled life‐history trait data from the literature and used Bayesian phylogenetic mixed models to test our hypotheses.Our models indicated that both concentrations and total amounts of the two main forms of THs (T3 and T4) were higher in the eggs of migratory species compared to resident species, and total amounts were higher in the eggs of precocial species, which have longer prenatal developmental periods, than in those of altricial species. However, maternal yolk THs did not show clear associations with pace‐of‐life‐related traits, such as fecundity, basal metabolic rate or maximum life span.We quantified interspecific variation in maternal yolk THs in birds, and our findings suggest higher maternal TH transfer is associated with the precocial mode of development and migratory status. Whether maternal THs represent a part of the mechanism underlying the evolution of precocial development and migration or a consequence of such life histories is currently unclear. We therefore encourage further studies to explore the physiological mechanisms and evolutionary processes underlying these patterns.

Strontium isotopes reveal diverse life history variations, migration patterns, and habitat use for Broad Whitefish (Coregonus nasus) in Arctic, Alaska.

Conservation of Arctic fish species is challenging partly due to our limited ability to track fish through time and space, which constrains our understanding of life history diversity and lifelong habitat use. Broad Whitefish (Coregonus nasus) is an important subsistence species for Alaska’s Arctic Indigenous communities, yet little is known about life history diversity, migration patterns, and freshwater habitat use. Using laser ablation Sr isotope otolith microchemistry, we analyzed Colville River Broad Whitefish 87Sr/86Sr chronologies (n = 61) to reconstruct movements and habitat use across the lives of individual fish. We found evidence of at least six life history types, including three anadromous types, one semi-anadromous type, and two nonanadromous types. Anadromous life history types comprised a large proportion of individuals sampled (collectively, 59%) and most of these (59%) migrated to sea between ages 0–2 and spent varying durations at sea. The semi-anadromous life history type comprised 28% of samples and entered marine habitat as larvae. Nonanadromous life history types comprised the remainder (collectively, 13%). Otolith 87Sr/86Sr data from juvenile and adult freshwater stages suggest that habitat use changed in association with age, seasons, and life history strategies. This information on Broad Whitefish life histories and habitat use across time and space will help managers and conservation planners better understand the risks of anthropogenic impacts and help conserve this vital subsistence resource.

Roadkill mortality decreases after road inauguration

The main factors affecting specific road casualty rates are related to life-history traits, road features, and landscape variables. After road inauguration, roadkill rate and spatial and temporal patterns can change substantially due to changes in traffic intensity, avoidance behaviour or local population decline. Despite the Canary Islands constituting a biodiversity hotspot, Canarian ecosystems are highly threatened because of the high human density, and studies on anthropogenic sources of mortality of wildlife are scarce. Here, we counted roadkills during two annual cycles after the inauguration of an 8.8-km-road section on Tenerife, the largest and most densely populated island of the Canaries. We counted 694 roadkills belonging to a minimum of 19 species of birds and six species of introduced mammals. Seasonal variation was apparent during both annual cycles, particularly for birds, being the majority of victims concentrated in May and June. Although traffic intensity increased since road inauguration, the number of roadkills decreased significantly in the second annual cycle. The reduction in road mortality in the second cycle could be related to some non-mutually exclusive factors such as population decline, road avoidance, or weather conditions. As road networks of the Canary Islands are still increasing, further studies quantifying road mortality impacts on Canarian ecosystems and threatened species are urgently needed to guarantee the management and conservation of its fragile wildlife.

The North American Freshwater Migratory Fish Database (NAFMFD): Characterizing the migratory life histories of freshwater fishes of Canada, the United States and Mexico

AbstractAimMigratory freshwater fishes are those that must access discrete habitats to complete their life cycles. Freshwater fish migrations occur around the world and provide numerous ecosystem services for humans and natural systems; however, many migratory species are in decline globally. A limiting factor to successfully conserve freshwater migratory fishes is that the migratory life histories of many species are unknown or only partially described. To provide researchers with critical and comprehensive information to conserve migratory fishes, we developed the North American Freshwater Migratory Fish Database (NAFMFD).LocationCanada, Mexico and the United States.TaxonFreshwater fish.MethodsTo develop this database, we assigned migratory status, pattern and behaviour to a comprehensive list of freshwater fish species found throughout North America. We assembled the database which included assignments (i.e. migratory status, pattern and behaviour) as well as the sources used to make the assignments. Researchers and managers from across North America reviewed the database for completeness and accuracy on the migratory life histories of fishes.ResultsThe database synthesizes current knowledge of migratory status, pattern and behaviour of native and non‐native freshwater fishes throughout North America, including 1250 species representing 79 families and 325 genera. Results showcase the diversity of migratory life histories of freshwater fishes on the continent, including that at least 25% of North American freshwater fishes are migratory, 23% are non‐migratory and 44% have undetermined migratory status.Main conclusionsNAFMFD improves the quality of migratory data accessible to researchers, which supports a more holistic understanding of the threats encountered by migratory fishes, including habitat fragmentation. The approach we used in developing NAFMFD can provide guidance for developing similar databases in other regions. Collectively, our work offers new insights into the range of freshwater fish migratory life histories, stimulating a need to better understand this diversity globally.

Growth variation in the endangered fish Zingel asper: Contribution of substrate quality, hydraulics, prey abundance, and water temperature

Abstract Intraspecific variation in life histories and its environmental correlates can indicate the degree of vulnerability to extinction of endangered taxa and guide conservation actions. Zingel asper (Percidae) is an endangered fish endemic to the Rhône catchment (France and Switzerland), where five populations subsist in separate river systems (Loue, Beaume, Durance, Verdon, and Doubs). Two populations of Z. asper differ in growth and longevity, but the existence of broader intraspecific differentiation in life histories and the environmental origins of this variation (if any) remain unknown. The age structure and growth profile of four populations of Z. asper (Loue, Beaume, Durance, and Verdon) and nine additional sub‐populations within the Durance system were determined by scale‐reading analysis, before evaluating the contribution of measured variation in substrate quality, hydraulics, prey availability, and water temperature to growth differentiation among and within populations. A trade‐off between early growth and longevity largely differentiated the populations of Z. asper along a slow (i.e. slower growth, smaller adult size, longevity of >5 years) to fast (i.e. faster growth, larger adult size, longevity of <4 years) continuum of life histories. This continuum differentiated populations from different river catchments along a south (Durance, Verdon) to north (Beaume, Loue) latitudinal gradient, and mapped onto an upstream–downstream gradient of sub‐populations within the Durance system. Differences in prey availability, hydraulics, and water temperature explained most of the growth variation among populations from different catchments, whereas local variation in prey availability, substrate quality, and water temperature mostly contributed to within‐river growth differentiation. These results indicate that short life cycles strongly expose all populations of Z. asper to extirpation and should motivate additional conservation actions. This study illustrates how quantifying intraspecific variation in life histories and its sensitivity to ecological context can reliably assess extinction risk and guide conservation actions by identifying endangered populations requiring priority management.

Wood anatomical traits mediate life-history variations at the sapling, but not at the adult stage

Wood anatomical traits mediate life-history variations at the sapling, but not at the adult stage

Maximum longevity and juvenile mortality in zoo-housed mangabeys.

Little is known about the biology of grey-cheeked and black crested mangabeys (Lophocebus albigena and Lophocebus aterrimus, respectively). As these primates face threats in the wild, well-monitored zoo-housed populations with up to date registries are becoming increasingly valuable to acquire species knowledge and to support conservation efforts. We used international studbooks to extract demographic and genetic information on 519 mangabeys to investigate how life history and parent-related variables influence maximum longevity and juvenile mortality. Generalized linear mixed models, as well as survival analyses, were applied. Results showed that females lived significantly longer than males, which is not uncommon in primates. Furthermore, our results indicated that the maximum longevity is lower for individuals living in European zoos versus individuals from North American zoos, which may be due to a combination of environmental differences and potential founder effects. We also show that the maternal maximum longevity is positively related to the maximum longevity of the offspring, which may be explained by the inheritance of "good genes". However, the age of the mother at the moment of birth was negatively related to the maximum longevity of the offspring, which contradicts literature that states that, in primates, more experienced and thus older mothers will raise their offspring better than less experienced mothers. Instead, it is more likely that an "optimal age range" exists for breeding mothers. Our study provides insights into the population biology of captive mangabeys and may be helpful for identifying future research priorities to optimize primate health and welfare directly ex situ, and indirectly in situ.

Coevolution of relative brain size and life expectancy in parrots.

Previous studies have demonstrated a correlation between longevity and brain size in a variety of taxa. Little research has been devoted to understanding this link in parrots; yet parrots are well-known for both their exceptionally long lives and cognitive complexity. We employed a large-scale comparative analysis that investigated the influence of brain size and life-history variables on longevity in parrots. Specifically, we addressed two hypotheses for evolutionary drivers of longevity: the cognitive buffer hypothesis, which proposes that increased cognitive abilities enable longer lifespans, and the expensive brain hypothesis, which holds that increases in lifespan are caused by prolonged developmental time of, and increased parental investment in, large-brained offspring. We estimated life expectancy from detailed zoo records for 133 818 individuals across 244 parrot species. Using a principled Bayesian approach that addresses data uncertainty and imputation of missing values, we found a consistent correlation between relative brain size and life expectancy in parrots. This correlation was best explained by a direct effect of relative brain size. Notably, we found no effects of developmental time, clutch size or age at first reproduction. Our results suggest that selection for enhanced cognitive abilities in parrots has in turn promoted longer lifespans.

The broken-wing display across birds and the conditions for its evolution.

The broken-wing display is a well-known and conspicuous deceptive signal used to protect birds' broods against diurnal terrestrial predators. Although commonly associated with shorebirds, it remains unknown how common the behaviour is across birds and what forces are associated with the evolution of the display. Here, we use the broken-wing display as a paradigmatic example to study the evolution of a behaviour across Aves. We show that the display is widespread: it has been described in 52 families spread throughout the phylogeny, suggesting that it independently evolved multiple times. Further, we evaluated the association with 16 ecological and life-history variables hypothesized to be related to the evolution of the broken-wing display. Eight variables were associated with the display. We found that species breeding farther from the equator, in more dense environments, with shorter incubation periods, and relatively little nest cover were more likely to perform the display, as were those in which only one parent incubates eggs, species that mob nest predators and species that are altricial or multi-brooded. Collectively, our comprehensive approach identified forces associated with the repeated evolution of this conspicuous display, thereby providing new insights into how deceptive behaviours evolve in the context of predator–prey interactions.