An inter‐species protein–protein interaction network across vast evolutionary distance

In cellular systems, biophysical interactions between macromolecules underlie a complex web of functional interactions. How biophysical and functional networks are coordinated, whether all biophysical interactions correspond to functional interactions, and how such biophysical‐versus‐functional network coordination is shaped by evolutionary forces are all largely unanswered questions. Here, we investigate these questions using an “inter‐interactome” approach. We systematically probed the yeast and human proteomes for interactions between proteins from these two species and functionally characterized the resulting inter‐interactome network. After a billion years of evolutionary divergence, the yeast and human proteomes are still capable of forming a biophysical network with properties that resemble those of intra‐species networks. Although substantially reduced relative to intra‐species networks, the levels of functional overlap in the yeast–human inter‐interactome network uncover significant remnants of co‐functionality widely preserved in the two proteomes beyond human–yeast homologs. Our data support evolutionary selection against biophysical interactions between proteins with little or no co‐functionality. Such non‐functional interactions, however, represent a reservoir from which nascent functional interactions may arise.     

N‐glycosylation proteomic characterization and cross‐species comparison of milk fat globule membrane proteins from mammals

Glycosylation of proteins has been implicated in various biological functions and has received much attention; however, glycoprotein components and inter‐species complexity have not yet been elucidated fully in milk proteins. N‐linked glycosylation sites and glycoproteins in milk fat globule membrane (MFGM) fractions were investigated by combining N‐glycosylated peptides enrichment and high‐accuracy Q Exactive identification, to map the N‐glycoproteome profiles in Holstein and Jersey cows, buffaloes, yaks, goats, camels, horses, and humans. A total of 399 N‐glycoproteins with 677 glycosylation sites were identified in the MFGM fractions of the studied mammals. Most glycosylation sites in humans were classified as known and those in the other studied mammals as unknown, according to Swiss‐Prot annotations. Functionally, most of the identified glycoproteins were associated with the ‘response to stimulus’ GO category. N‐glycosylated protein components of MFGM fractions from Holstein and Jersey cows, buffaloes, yaks, and goats were more similar to each other compared with those of camels, horses and human. The findings increased the number of known N‐glycosylation sites in the milk from dairy animal species, revealed the complexity of the MFGM glycoproteome, and provided useful information to further explore the mechanism of MFGM glycoproteins biosynthesis among the studied mammals.     

An empirical evaluation of the African elephant as a focal species for connectivity planning in East Africa

Aim Large, charismatic and wide‐ranging animals are often employed as focal species for prioritizing landscape linkages in threatened ecosystems (i.e. ‘connectivity conservation’), but there have been few efforts to assess empirically whether focal species co‐occur with other species of conservation interest within potential linkages. We evaluated whether the African elephant (Loxodonta africana), a world‐recognized flagship species, would serve as an appropriate focal species for other large mammals in a potential linkage between two major protected area complexes. Location A 15,400 km² area between the Ruaha and Selous ecosystems in central Tanzania, East Africa. Methods We used walking transects to assess habitat, human activity and co‐occurrence of elephants and 48 other large mammal species (> 1 kg) at 63 sites using animal sign and direct sightings. We repeated a subset of transects to estimate species detectability using occupancy modelling. We used logistic regression and AIC model selection to characterize patterns of elephant occurrence and assessed correlation of elephant presence with richness of large mammals and subgroups. We considered other possible focal species, compared habitat‐based linear regression models of large mammal richness and used circuit theory to examine potential connectivity spatially. Results Elephants were detected in many locations across the potential linkage. Elephant presence was highly positively correlated with the richness of large mammals, as well as ungulates, carnivores, large carnivores and species > 45 kg in body mass (‘megafauna’). Outside of protected areas, both mammal richness and elephant presence were negatively correlated with human population density and distance from water. Only one other potential focal species was more strongly correlated with species richness than elephants, but detectability was highest for elephants. Main conclusions Although African elephants have dispersal abilities that exceed most other terrestrial mammals, conserving elephant movement corridors may effectively preserve habitat and potential landscape linkages for other large mammal species among Tanzanian reserves.     

Di‐ and tetranucleotide microsatellite markers for the Alpine newt (Triturus alpestris): characterization and cross‐priming in five congeners

We developed a set of di‐ and tetranucleotide microsatellite markers for the Alpine newt, Triturus alpestris. Polymorphism as detected in 39 individuals ranged from 3 to 32 alleles at a locus. Cross‐priming with samples of five other Triturus species showed extremely poor levels of cross‐species utility. Still, these markers are suitable for studies of inter‐ and intrapopulation genetic diversity in the focal species.     

Incorporating biotic interactions in the distribution models of African wild silk moths (Gonometa species,Lasiocampidae) using different representations of modelled host tree distributions

Biotic interactions influence species niches and may thus shape distributions. Nevertheless, species distribution modelling has traditionally relied exclusively on environmental factors to predict species distributions, while biotic interactions have only seldom been incorporated into models. This study tested the ability of incorporating biotic interactions, in the form of host plant distributions, to increase model performance for two host‐dependent lepidopterans of economic interest, namely the African silk moth species, Gonometa postica and Gonometa rufobrunnea (Lasiocampidae). Both species are dependent on a small number of host tree species for the completion of their life cycle. We thus expected the host plant distribution to be an important predictor of Gonometa distributions. Model performance of a species distribution model trained only on abiotic predictors was compared to four species distribution models that additionally incorporated biotic interactions in the form of four different representations of host plant distributions as predictors. We found that incorporating the moth–host plant interactions improved G. rufobrunnea model performance for all representations of host plant distribution, while for G. postica model performance only improved for one representation of host plant distribution. The best performing representation of host plant distribution differed for the two Gonometa species. While these results suggest that incorporating biotic interactions into species distribution models can improve model performance, there is inconsistency in which representation of the host tree distribution best improves predictions. Therefore, the ability of biotic interactions to improve species distribution models may be context‐specific, even for species which have obligatory interactions with other organisms.     

Carving out turf in a biodiversity hotspot: multiple,previously unrecognized shrew species co‐occur on Java Island,Indonesia

In theory, competition among species in a shared habitat results in niche separation. In the case of small recondite mammals such as shrews, little is known about their autecologies, leaving open questions regarding the degree to which closely related species co‐occur and how or whether ecological niches are partitioned. The extent to which species are able to coexist may depend on the degree to which they exploit different features of their habitat, which may in turn influence our ability to recognize them as species. We explored these issues in a biodiversity hotspot, by surveying shrew (genus Crocidura) diversity on the Indonesian island of Java. We sequenced portions of nine unlinked genes in 100–117 specimens of Javan shrews and incorporated homologous data from most known Crocidura species from other parts of island South‐East Asia. Current taxonomy recognizes four Crocidura species on Java, including two endemics. However, our phylogenetic, population genetic and species delimitation analyses identify five species on the island, and all are endemic to Java. While the individual ranges of these species may not overlap in their entirety, we found up to four species living syntopically and all five species co‐occurring on one mountain. Differences in species' body size, use of above ground‐level habitats by one species and habitat partitioning along ecological gradients may have facilitated species diversification and coexistence.     

Habitat and introduced predators influence the occupancy of small threatened macropods in subtropical Australia

Australia has had the highest rate of mammal extinctions in the past two centuries when compared to other continents. Frequently cited threats include habitat loss and fragmentation, changed fire regimes and the impact of introduced predators, namely the red fox (Vulpes vulpes) and the feral cat (Felis catus). Recent studies suggest that Australia's top predator, the dingo (Canis dingo), may have a suppressive effect on fox populations but not on cat populations. The landscape of fear hypothesis proposes that habitat used by prey species comprises high to low risk patches for foraging as determined by the presence and ubiquity of predators within the ecosystem. This results in a landscape of risky versus safe areas for prey species. We investigated the influence of habitat and its interaction with predatory mammals on the occupancy of medium‐sized mammals with a focus on threatened macropodid marsupials (the long‐nosed potoroo [Potorous tridactylous] and red‐legged pademelon [Thylogale stigmatica]). We assumed that differential use of habitats would reflect trade‐offs between food and safety. We predicted that medium‐sized mammals would prefer habitats for foraging that reduce the risk of predation but that predators would have a positive relationship with medium‐sized mammals. We variously used data from 298 camera trap sites across nine conservation reserves in subtropical Australia. Both dingoes and feral cats were broadly distributed, whilst the red fox was rare. Long‐nosed potoroos had a strong positive association with dense ground cover, consistent with using habitat complexity to escape predation. Red‐legged pademelons showed a preference for open ground cover, consistent with a reliance on rapid bounding to escape predation. Dingoes preferred areas of open ground cover whereas feral cats showed no specific habitat preference. Dingoes were positively associated with long‐nosed potoroos whilst feral cats were positively associated with red‐legged pademelons. Our study highlights the importance of habitat structure to these threatened mammals and also the need for more detailed study of their interactions with their predators.     

A review of ecological interactions between native frogs and invasive cane toads in Australia

Translocated from their native range in the Americas in 1935, cane toads (Rhinella marina, Bufonidae) have now spread through much of tropical and subtropical Australia. The toad's invasion and impact have attracted detailed study. In this paper, I review information on ecological interactions between cane toads and Australian anurans. The phylogenetic relatedness and ecological similarity between frogs and toads creates opportunities for diverse interactions, ranging from predation to competition to parasite transfer, plus a host of indirect effects mediated via impacts of toads on other species, and by people's attempts to control toads. The most clear‐cut effect of toads on frogs is a positive one: reducing predator pressure by fatally poisoning anuran‐eating varanid lizards. However, toads also have a wide range of other effects on frogs, some positive (e.g. taking up parasites that would otherwise infect native frogs) and others negative (e.g. eating frogs, poisoning frogs, competing with tadpoles). Although information on such mechanisms predicts intense interactions between toads and frogs, field surveys show that cane toad invasion has negligible overall impacts on frog abundance. That counter‐intuitive result is because of a broad balancing of negative and positive impacts, coupled with stochastic (weather‐induced) fluctuations in anuran abundance that overwhelm any impacts of toads. Also, the impacts of toads on frogs differ among frog species and life‐history stages, and depend upon local environmental conditions. The impacts of native frogs on cane toads have attracted much less study, but may well be important: frogs may impose biotic resistance to cane toad colonization, especially via competition in the larval phase. Overall, the interactions between native frogs and invasive toads illustrate the diverse ways in which an invader's arrival can perturb the native fauna by both direct and indirect mechanisms, and by which the native species can curtail an invader's success. These studies also offer a cautionary tale about the difficulty of predicting the impact of an invasive species, even with a clear understanding of mechanisms of direct interaction.     

Revealing kleptoparasitic and predatory tendencies in an African mammal community using camera traps: a comparison of spatiotemporal approaches

Camera trap data are increasingly being used to characterise relationships between the spatiotemporal activity patterns of sympatric mammal species, often with a view to inferring inter‐specific interactions. In this context, we attempted to characterise the kleptoparasitic and predatory tendencies of spotted hyaenas Crocuta crocuta and lions Panthera leo from photographic data collected across 54 camera trap stations and two dry seasons in Tanzania's Ruaha National Park. We applied four different methods of quantifying spatiotemporal associations, including one strictly temporal approach (activity pattern overlap), one strictly spatial approach (co‐occupancy modelling), and two spatiotemporal approaches (co‐detection modelling and temporal spacing at shared camera trap sites). We expected a kleptoparasitic relationship between spotted hyaenas and lions to result in a positive spatiotemporal association, and further hypothesised that the association between lions and their favourite prey in Ruaha, the giraffe Giraffa camelopardalis and the zebra Equus quagga, would be stronger than those observed with non‐preferred prey species (the impala Aepyceros melampus and the dikdik Madoqua kirkii). Only approaches incorporating both the temporal and spatial components of camera trap data resulted in significant associative patterns. The latter were particularly sensitive to the temporal resolution chosen to define species detections (i.e. occasion length), and only revealed a significant positive association between lion and spotted hyaena detections, as well as a tendency for both species to follow each other at camera trap sites, during the dry season of 2013, but not that of 2014. In both seasons, observed spatiotemporal associations between lions and each of the four herbivore species considered provided no convincing or consistent indications of any predatory preferences. Our study suggests that, when making inferences on inter‐specific interactions from camera trap data, due regards should be given to the potential behavioural and methodological processes underlying observed spatiotemporal patterns.     

The symmetry of competitive interactions in mixed Norway spruce,silver fir and European beech forests

Questions

We aim for a better understanding of the different modes of intra‐ and inter‐specific competition in two‐ and three‐species mixed‐forests. How can the effect of different modes of competitive interactions be detected and integrated into individual tree growth models? Are species interactions in spruce–fir–beech forests more associated with size‐symmetric or size‐asymmetric competition? Do competitive interactions between two of these species change from two‐ to three‐species mixtures?

Location

Temperate mixed‐species forests in Central Europe (Switzerland).

Methods

We used data from the Swiss National Forest Inventory to fit basal area increment models at the individual tree level, including the effect of ecological site conditions and indices of size‐symmetric and size‐asymmetric competition. Interaction terms between species‐specific competition indices were used to disentangle significant differences in species interactions from two‐ to three‐species mixtures.

Results

The growth of spruce and fir was positively affected by increasing proportions of the other species in spruce–fir mixtures, but negative effects were detected with increasing presence of beech. We found that competitive interactions for spruce and fir were more related to size‐symmetric competition, indicating that species interactions might be more associated with competition for below‐ground resources. Under constant amounts of stand basal area, the growth of beech clearly benefited from the increasing admixture of spruce and fir. For this species, patterns of size‐symmetric and size‐asymmetric competitive interactions were similar, indicating that beech is a strong self‐competitor for both above‐ground and below‐ground resources. Only for silver fir and beech, we found significant changes in species interactions from two‐ to three‐species mixtures, but these were not as prominent as the effects due to differences between intra‐ and inter‐specific competition.

Conclusions

Species interactions in spruce–fir–beech, or other mixed forests, can be characterized depending on the mode of competition, allowing interpretations of whether they occur mainly above or below ground level. Our outcomes illustrate that species‐specific competition indices can be integrated in individual tree growth functions to express the different modes of competition between species, and highlight the importance of considering the symmetry of competition alongside competitive interactions in models aimed at depicting growth in mixed‐species forests.

     

Long‐term and interactive effects of different mammalian consumers on growth,survival, and recruitment of dominant tree species

Throughout the world, numerous tree species are reported to be in decline, either due to increased mortality of established trees or reduced recruitment. The situation appears especially acute for oaks, which are dominant features of many landscapes in the northern hemisphere. Although numerous factors have been hypothesized to explain reductions in tree performance, vertebrate herbivores and granivores may serve as important drivers of these changes. Here, using data from 8‐ and 14‐year‐old exclosure experiments, we evaluated the individual and interactive effects of large and small mammalian herbivores on the performance of three widespread oak species in California—coast live oak (Quercus agrifolia), California black oak (Q. kelloggii), and Oregon white oak (Q. garryana). Although impacts varied somewhat by species and experiment, herbivory by black‐tailed deer (Odocoileus hemionus columbianus) reduced the height and survival of juvenile coast live oaks and altered their architecture, as well as reduced the abundance of black oak seedlings, the richness of woody species and the cover of nonoak woody species. Small mammals (Microtus californicus and Peromyscus maniculatus) had even more widespread effects, reducing the abundance of black oak seedlings and the height and cover of all three oak species. We also detected numerous interactions between small mammals and deer, with one herbivore having positive or negative effects on oak abundance and cover when the other herbivore was either present or absent. For example, deer often had negative effects on seedling abundance only when, or even more so when, small mammals were present. In summary, mammalian consumers play crucial roles in limiting oak recruitment by reducing seedling abundance, maintaining trees in stunted states, and preventing them from reaching sapling stages and becoming reproductive. Interactions between large and small mammals can also alter the intensity and direction of their effects on trees.     

Accuracy of identifications of mammal species from camera trap images: A northern Australian case study

Camera traps are a powerful and increasingly popular tool for mammal research, but like all survey methods, they have limitations. Identifying animal species from images is a critical component of camera trap studies, yet while researchers recognize constraints with experimental design or camera technology, image misidentification is still not well understood. We evaluated the effects of a species’ attributes (body mass and distinctiveness) and individual observer variables (experience and confidence) on the accuracy of mammal identifications from camera trap images. We conducted an Internet‐based survey containing 20 questions about observer experience and 60 camera trap images to identify. Images were sourced from surveys in northern Australia and included 25 species, ranging in body mass from the delicate mouse (Pseudomys delicatulus, 10 g) to the agile wallaby (Macropus agilis, >10 kg). There was a weak relationship between the accuracy of mammal identifications and observer experience. However, accuracy was highest (100%) for distinctive species (e.g. Short‐beaked echidna [Tachyglossus aculeatus]) and lowest (36%) for superficially non‐distinctive mammals (e.g. rodents like the Pale field‐rat [Rattus tunneyi]). There was a positive relationship between the accuracy of identifications and body mass. Participant confidence was highest for large and distinctive mammals, but was not related to participant experience level. Identifications made with greater confidence were more likely to be accurate. Unreliability in identifications of mammal species is a significant limitation to camera trap studies, particularly where small mammals are the focus, or where similar‐looking species co‐occur. Integration of camera traps with conventional survey techniques (e.g. live‐trapping), use of a reference library or computer‐automated programs are likely to aid positive identifications, while employing a confidence rating system and/or multiple observers may lead to a collection of more robust data. Although our study focussed on Australian species, our findings apply to camera trap studies globally.     

Strong Competition Does Not Always Predict Play Asymmetry: The Case of South American Sea Lions (Otaria flavescens)

Although play fighting has been studied for over a century in both human and non‐human animals, quantitative data on marine mammals are still scarce. Here, we investigated play fighting in South American sea lions (Otaria flavescens), one of the most sexually dimorphic species with an extreme polygynous mating system, high levels of both intra‐ and inter‐sexual competition. All these features make South American sea lions a good model species to test some predictions on play fighting. Our results indicate play is restricted to juveniles, being inhibited among adults, and as to be expected in a species that shows a high degree of sexual dimorphism, it is mainly expressed in males. Even though playful interactions were punctuated by competitive behaviours, animals played in a highly symmetric way and were able to adjust their competitive playful interactions in a flexible manner and so reduce the risk of escalation to a minimum level. They were highly selective in their choice of playmates by limiting the number of players per session and playing more with age‐matched companions and friends. All these factors taken together are probably at the basis of the low risk of escalation recorded during the study. This result is predictive of a high ability and motivation of these animals to engage in play behaviour which can have a possible role not only in the acquisition of dominance status, but also in establishing and maintaining social relationships, an unexpected role in a so highly competitive species.     

The role of exotic mammals in the diet of native carnivores from South America

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Incidental invertebrate-derived DNA detection of invasive and threatened species in temperate dry Southeast Australian forest

Well-informed biodiversity conservation practice can often be precluded by poor species detectability. For example, populations being missed during surveys can lead to them being omitted from species lists or area management plans. iDNA (invertebrate-derived DNA) is a recently developed set of techniques for improving the detectability of elusive vertebrates by exploiting their associated invertebrates. Parasitic and scavenging invertebrates can be readily collected, and their gut contents DNA barcoded to detect local vertebrate diversity. However, most iDNA surveys have targeted mammals and have been carried out in tropical areas and/or rainforests. We carried out iDNA surveys targeting frogs in temperate dry sclerophyll forests in south-eastern Australia. We set mosquito traps broadcasting recorded frog calls with the aim of collecting frog-biting flies, which are attracted to frog calls. We collected 156 fly specimens, although none were of frog-biting species, and no frogs were detected via iDNA, despite many being observed in the field. However, two mammal and one reptile species were detected via iDNA: the feral cat (Felis catus: Felidae), domestic dog or dingo (Canis lupus: Canidae) and the threatened Rosenberg's monitor (Varanus rosenbergi: Varanidae). Vertebrate-sampling flies are likely highly abundant in the area since they were collected apparently incidentally in traps lacking appropriate attractants; a promising result for further surveys is different attractants are employed. This study is one of the few in which an invasive species has been detected through iDNA, and highlights its potential for improved detectability of threatened species outside of the tropics and early detection of invasive species.     

Effects of Tree Genotypic Diversity and Species Diversity on the Arthropod Community Associated with Big‐leaf Mahogany

Despite potential interactive effects of plant species and genotypic diversity (SD and GD, respectively) on consumers, studies have usually examined these effects separately. We evaluated the individual and combined effects of tree SD and mahogany (Swietenia macrophylla) GD on the arthropod community associated with mahogany. We conducted this study within the context of a tree diversity experiment consisting of 74 plots with 64 saplings/plot. We sampled 24 of these plots, classified as monocultures of mahogany or polycultures of four species (including mahogany). Within each plot type, mahogany was represented by either one or four maternal families. We surveyed arthropods on mahogany and estimated total arthropod abundance and species richness, as well as abundance and richness separately for herbivorous and predatory arthropods. Overall tree SD and mahogany GD had positive effects on total arthropod species richness and abundance on mahogany, and also exerted interactive effects on total species richness (but not abundance). Analyses conducted by trophic level group showed contrasting patterns; SD positively influenced herbivore species richness but not abundance, and did not affect either predator richness or abundance. GD influenced predator species richness but not abundance, and did not influence herbivore abundance or richness. There were interactive effects of GD and SD only for predator species richness. These results provide evidence that intra‐ and inter‐specific plant diversity exert interactive controls on associated consumer communities, and that the relative importance of SD and GD may vary among higher trophic levels, presumably due to differences in the underlying mechanisms or consumer traits.     

Do interspecific interactions between females drive shifts in habitat use? A test using the lizards Anolis carolinensis and A. sagrei

An important goal in evolutionary ecology is to understand how and why coexisting closely related species partition habitat among themselves. Although studies of interspecific interactions typically focus on males, interactions between females may also play an important role in shaping habitat use within multi‐species communities. The green anole (Anolis carolinensis) exhibits a wide range of habitat use in south‐eastern Louisiana, but its observed habitat use is restricted and altered in areas where it occurs with the introduced Anolis sagrei. We staged interactions between these two species in the laboratory to test the hypothesis that A. sagrei dominate A. carolinensis in contests over shared habitat. We examined whether species identity, bite force, dewlap size, and body size affected the outcome of interspecific interactions between both males and females, and tested the prediction that bite force and size would be the most important determinants of interaction outcomes in both sexes. In male interspecific interactions, we found that individuals with relatively larger dewlaps tended to score higher on aggressive behaviours regardless of species identity, and that interactions consisted of signalling and rarely escalated to physical combat. However, we found that A. sagrei females achieved higher aggressive scores than A. carolinensis females in almost all cases, lending support to the notion that female interspecific behaviour is probably more important than male behaviour in driving changes in habitat use. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 843–851.     

DNA barcoding of Neotropical bats: species identification and discovery within Guyana

Sequence diversity in the cytochrome c oxidase subunit 1 gene has been shown to be an effective tool for species identification and discovery in various groups of animals, but has not been extensively tested in mammals. We address this gap by examining the performance of DNA barcodes in the discrimination of 87 species of bats from Guyana. Eighty‐one of these species showed both low intraspecific variation (mean = 0.60%), and clear sequence divergence from their congeners (mean = 7.80%), while the other six showed deeply divergent intraspecific lineages suggesting that they represent species complexes. Although further work is needed to examine patterns of sequence diversity at a broader geographical scale, the present study validates the effectiveness of barcoding for the identification of regional bat assemblages, even highly diverse tropical faunas.     

Fire‐mediated niche‐separation between two sympatric small mammal species

Fire is a key ecological process influencing the population dynamics of small mammals. Whilst shifting competitive advantage amongst small mammal species following a single fire event is well‐documented, there has been little investigation of the potential influence of fire frequency on small mammal interspecific interactions. In this study, we investigated the effect of fire frequency on the abundance of two small dasyurid mammals, Antechinus stuartii and A. flavipes, which occur sympatrically in some parts of their range. The two antechinus species are known to have different habitat preferences, so it is possible that fire regimes may promote their coexistence in areas of sympatry by altering vegetation structure. To investigate this possibility, we estimated the abundance of both species using replicate sites which differed in the number of times burnt (1–4) during the last four decades, but with identical time‐since‐fire. Proportionally, we captured greater numbers of A. stuartii in less frequently burnt sites and greater numbers of A. flavipes in more‐frequently burnt sites. Hence, fire may mediate niche‐separation between these two species. To clarify further this pattern of response to fire frequency, we investigated which structural habitat variables differed between fire frequencies, and compared antechinus abundances with structural vegetation characteristics. We found a trend for lower ground cover density under higher fire frequencies. This offers one potential explanation of the patterns of abundance that we observed. Our study provided insights into the complexities of small mammal responses to fire, and strongly suggests that fire could mediate competitive interactions between species.