Coexistence of insect species competing for a pulsed resource: toward a unified theory of biodiversity in fluctuating environments

Background

One major challenge in understanding how biodiversity is organized is finding out whether communities of competing species are shaped exclusively by species-level differences in ecological traits (niche theory), exclusively by random processes (neutral theory of biodiversity), or by both processes simultaneously. Communities of species competing for a pulsed resource are a suitable system for testing these theories: due to marked fluctuations in resource availability, the theories yield very different predictions about the timing of resource use and the synchronization of the population dynamics between the competing species. Accordingly, we explored mechanisms that might promote the local coexistence of phytophagous insects (four sister species of the genus Curculio) competing for oak acorns, a pulsed resource.

Methodology/Principal Findings

We analyzed the time partitioning of the exploitation of oak acorns by the four weevil species in two independent communities, and we assessed the level of synchronization in their population dynamics. In accordance with the niche theory, overall these species exhibited marked time partitioning of resource use, both within a given year and between different years owing to different dormancy strategies between species, as well as distinct demographic patterns. Two of the four weevil species, however, consistently exploited the resource during the same period of the year, exhibited a similar dormancy pattern, and did not show any significant difference in their population dynamics.

Conclusions/Significance

The marked time partitioning of the resource use appears as a keystone of the coexistence of these competing insect species, except for two of them which are demographically nearly equivalent. Communities of consumers of pulsed resources thus seem to offer a promising avenue for developing a unifying theory of biodiversity in fluctuating environments which might predict the co-occurrence, within the same community, of species that are ecologically either very similar, or very different.     

Prey diversity as a driver of resource partitioning between river‐dwelling fish species

Although food resource partitioning among sympatric species has often been explored in riverine systems, the potential influence of prey diversity on resource partitioning is little known. Using empirical data, we modeled food resource partitioning (assessed as dietary overlap) of coexisting juvenile Atlantic salmon (Salmo salar) and alpine bullhead (Cottus poecilopus). Explanatory variables incorporated into the model were fish abundance, benthic prey diversity and abundance, and several dietary metrics to give a total of seventeen potential explanatory variables. First, a forward stepwise procedure based on the Akaike information criterion was used to select explanatory variables with significant effects on food resource partitioning. Then, linear mixed‐effect models were constructed using the selected explanatory variables and with sampling site as a random factor. Food resource partitioning between salmon and bullhead increased significantly with increasing prey diversity, and the variation in food resource partitioning was best described by the model that included prey diversity as the only explanatory variable. This study provides empirical support for the notion that prey diversity is a key driver of resource partitioning among competing species.     

Importance of multi-dimensional analyses of resource partitioning in highly mobile species assemblages

Resource partitioning is an essential mechanism enabling species coexistence. The resources that are used by an animal are linked to its morphology and ecology. Therefore, similar species should use similar resources. The ecological niche of an individual summarizes all used resources and is therefore composed of several dimensions. Many methods are established to study different dimensions of an animal's niche. The aim of this study was to demonstrate that a combination of suitable methods is needed to study spatial and dietary resource partitioning of sympatric species in detail. We hypothesized that, while each individual method might identify differences between species, the combined results of several methods will lead to a more complete picture of spatial and dietary resource partitioning. As model organisms we chose the sympatric insectivorous bat species Myotis bechsteinii, M. nattereri, and P. auritus. We examined horizontal habitat use by telemetry, vertical habitat use by measuring δ¹³C, trophic position by measuring δ¹⁵N in wing membrane, and diet composition by molecular fecal analysis. Our results show that each method is able to provide information about spatial/dietary resource partitioning. However, considering further dimensions by combining several methods allows a more comprehensive assessment of dietary and spatial resource partitioning in bats.     

Avoidance of reproductive interference causes resource partitioning in bean beetle females

Reproductive interference is any interspecific sexual interaction that adversely affects female fitness through indiscriminate reproductive activities. It can be a driving force of resource partitioning in conjunction with resource competition. We previously showed that the bean beetle Callosobruchus maculatus is superior in larval resource competition, but vulnerable in reproductive interference, compared with its congener C. chinensis. We hypothesized that these two species might use two resources differently if one of the resources modified the intensity of reproductive interference or resource competition. We observed that C. maculatus females often enter gaps between beans to avoid mating attempts of heterospecific males, and hypothesized that removing bean gaps would strengthen reproductive interference. Therefore, we provided normal beans with gaps and split beans without gaps to females of the two species housed with conspecific or heterospecific males or no males and compared the number of eggs on each bean type among treatments. Callosobruchus maculatus females housed with heterospecific males were more likely to oviposit on normal beans than C. chinensis females. As a result, more C. chinensis adults hatched from split beans and more C. maculatus hatched from normal beans when females and males of both species were housed together. Thus, oviposition resource partitioning resulted from the combination of female avoidance of reproductive interference and resource competition.     

Interactions among resource partitioning, sampling effect, and facilitation on the biodiversity effect: a modeling approach

Resource partitioning, facilitation, and sampling effect are the three mechanisms behind the biodiversity effect, which is depicted usually as the effect of plant-species richness on aboveground net primary production. These mechanisms operate simultaneously but their relative importance and interactions are difficult to unravel experimentally. Thus, niche differentiation and facilitation have been lumped together and separated from the sampling effect. Here, we propose three hypotheses about interactions among the three mechanisms and test them using a simulation model. The model simulated water movement through soil and vegetation, and net primary production mimicking the Patagonian steppe. Using the model, we created grass and shrub monocultures and mixtures, controlled root overlap and grass water-use efficiency (WUE) to simulate gradients of biodiversity, resource partitioning and facilitation. The presence of shrubs facilitated grass growth by increasing its WUE and in turn increased the sampling effect, whereas root overlap (resource partitioning) had, on average, no effect on sampling effect. Interestingly, resource partitioning and facilitation interacted so the effect of facilitation on sampling effect decreased as resource partitioning increased. Sampling effect was enhanced by the difference between the two functional groups in their efficiency in using resources. Morphological and physiological differences make one group outperform the other; once these differences were established further differences did not enhance the sampling effect. In addition, grass WUE and root overlap positively influence the biodiversity effect but showed no interactions.     

Specialization and noncompetitive resource partitioning among sponge-eating dorid nudibranchs

Summary Habitat and food resource partitioning ecologically isolate six species of Pacific Northwest dorid nudibranchs. Food resources along a gradient of sponge skeletal structure are partitioned between two exploitive guilds. The guilds are characterized by mutually exclusive predatory and digestive adaptations which allow efficient processing of sponges with poorly- or well-organized skeletons. Habitats along a depth gradient are partitioned within guilds. For a dorid species, feeding rates, extraction efficiencies and food quality are virtually identical for sponges with the appropriate extreme (either poorly- or well-organized) and intermediate skeletal organizations, but growth and reproductive rates supported by the former prey type are twice those supported by the latter prey type. Prey types with the appropriate extreme skeletal organization are thus optimal food and specialization to that food is expected. When two divergent specialist species co-occur, food resource partitioning is demonstrable but arises from self-stabilizing specializations to maximize net energy accumulation and not from competitive interactions. Habitat partitioning is viewed as arising from prey distributions and dorid physiological tolerances. This system represents an example of morphological and behavioral specializations giving rise to resource partitioning as opposed to competition giving rise to resource partitioning and subsequent morphological and behavioral specializations.     

Alternative trait combinations and secondary resource partitioning in sexually selected color polymorphism

Resource partitioning within a species, trophic polymorphism is hypothesized to evolve by disruptive selection when intraspecific competition for certain resources is severe. However, in this study, we reported the secondary partitioning of oviposition resources without resource competition in the damselfly Ischnura senegalensis. In this species, females show color polymorphism that has been evolved as counteradaptation against sexual conflict. One of the female morphs is a blue‐green (andromorph, male‐like morph), whereas the other morph is brown (gynomorph). These female morphs showed alternative preferences for oviposition resources (plant tissues); andromorphs used fresh (greenish) plant tissues, whereas gynomorphs used decaying (brownish) plants tissues, suggesting that they chose oviposition resources on which they are more cryptic. In addition, the two‐color morphs had different egg morphologies. Andromorphs have smaller and more elongated eggs, which seemed to adapt to hard substrates compared with those of gynomorphs. The resource partitioning in this species is achieved by morphological and behavioral differences between the color morphs that allow them to effectively exploit different resources. Resource partitioning in this system may be a by‐product of phenotypic integration with body color that has been sexually selected, suggesting an overlooked mechanism of the evolution of resource partitioning. Finally, we discuss the evolutionary and ecological consequences of such resource partitioning.     

Comparison of light harvesting and resource allocation strategies between two rhizomatous herbaceous species inhabiting deciduous forests

Light conditions on the floor of deciduous forests are determined by the leaf dynamics of canopy trees and gap formation. Such spatiotemporal variations of light availability should affect the resource partitioning strategies of understory herbs. Although rhizomatous species are common in understory, relationships between rhizome structure, vegetative growth, and sexual reproduction are unclear in terms of carbon allocation. We compared the photosynthetic characteristics and carbon translocation patterns in the under-canopy and light-gap sites between two summer-green perennial species: Cardamine leucantha with an annual long rhizome, and Smilacina japonica with a perennial short rhizome system. Flowering of both species occurs in early summer under decreasing light availability. In the light-gap, C. leucantha maintained high photosynthetic activity due to continuous leaf production, resulting in higher seed production than in the under-canopy. In contrast, the photosynthetic rate of S. japonica, producing leaves simultaneously, decreased with time irrespective of light conditions, resulting in stable seed production in both sites. Although seasonally decreasing light availability commonly restricts carbon assimilation of understory herbs, the responses of resource partitioning to variations in light availability depend greatly on the belowground structure of individual species.     

Rising temperature reduces divergence in resource use strategies in coexisting parasitoid species

Coexistence of species sharing the same resources is often possible if species are phylogenetically divergent in resource acquisition and allocation traits, decreasing competition between them. Developmental and life-history traits related to resource use are influenced by environmental conditions such as temperature, but thermal trait responses may differ among species. An increase in ambient temperature may, therefore, affect trait divergence within a community, and potentially species coexistence. Parasitoids are interesting models to test this hypothesis, because multiple species commonly attack the same host, and employ divergent larval and adult host use strategies. In particular, development mode (arrested or continued host growth following parasitism) has been recognized as a major organiser of parasitoid life histories. Here, we used a comparative trait-based approach to determine thermal responses of development time, body mass, egg load, metabolic rate and energy use of the coexisting Drosophila parasitoids Asobara tabida, Leptopilina heterotoma, Trichopria drosophilae and Spalangia erythromera. We compared trait values between species and development modes, and calculated trait divergence in response to temperature, using functional diversity indices. Parasitoids differed in their thermal response for dry mass, metabolic rate and lipid use throughout adult life, but only teneral lipid reserves and egg load were affected by developmental mode. Species-specific trait responses to temperature were probably determined by their adaptations in resource use (e.g. lipogenesis or ectoparasitism). Overall, trait values of parasitoid species converged at the higher temperature. Our results suggest that local effects of warming could affect host resource partitioning by reducing trait diversity in communities.     

The relative importance of spatial aggregation and resource partitioning on the coexistence of mycophagous insects

The relative importance of spatial aggregation and resource partitioning on coexistence was investigated for mycophagous insects in central Japan. The effects of spatial aggregation and resource partitioning were separated by a randomization procedure. From 124 patches of macrosporophores belonging to 37 species, 3275 individuals belonging to 14 families of Diptera and 11 individuals to Lepidoptera emerged. Since the level of identification varied among insect taxa, the analysis was made in three ways; 1) for all taxa to assess the stability of the whole community, 2) for drosophilid species to assess their persistence in the community, and 3) for species of Drosophila and Mycodrosophila to assess their persistence against congeneric and heterogeneric species. Both spatial aggregation and resource partitioning functioned for the stability of whole mycophagous insect community, and spatial aggregation played a more important role than resource partitioning. On the other hand, only spatial aggregation functioned for the persistence of drosophilid species in the community. According to the analysis on species of Drosophila and Mycodrosophila against congeneric and heterogeneric species, the relative importance of resource partitioning was smaller for the coexistence of within-genus species pairs than for that of between-genus species pairs. These results suggest that the relative importance of these two mechanisms depends on the phylogenetic and guild diversity of community.     

Soil resource availability is much more important than soil resource heterogeneity in determining the species diversity and abundance of karst plant communities

Resource availability and heterogeneity are recognized as two essential environmental aspects to determine species diversity and community abundance. However, how soil resource availability and heterogeneity determine species diversity and community abundance in highly heterogeneous and most fragile karst landscapes is largely unknown. We examined the effects of soil resource availability and heterogeneity on plant community composition and quantified their relative contribution by variation partitioning. Then, a structural equation model (SEM) was used to further disentangle the multiple direct and indirect effects of soil resource availability on plant community composition. Species diversity was significantly influenced by the soil resource availability in shrubland and woodland but not by the heterogeneity in woodland. Abundance was significantly affected by both soil resource availability and heterogeneity, whereas variation partitioning results showed that soil resource availability explained the majority of the variance in abundance, and the contribution of soil resource heterogeneity was marginal. These results indicated that soil resource availability plays a more important role in determining karst plant community composition than soil resource heterogeneity. Our SEMs further found that the multiple direct and indirect processes of soil resource availability in determining karst species diversity and abundance were different in different vegetation types. Soil resource availability and heterogeneity both played a certain role in determining karst plant community composition, while the importance of soil resource availability far exceeded soil resource heterogeneity. We propose that steering community restoration and reconstruction should be highly dependent on soil resource availability, and multiple direct and indirect pathways of soil resource availability for structuring karst plant communities need to be taken into account.     

Phenology and resource use in three co-occurring grassland annuals

Water resource partitioning among three co-occurring species of the California annual grassland was investigated. Plantago erecta, Clarkia rubicunda and Hemizonia luzulifolia differ in lifespan. The lifespan of Plantago is coincident with the October–May rainy season, but the other two species reproduce during summer when no precipitation occurs, and thus depend on stored water. Field studies indicated differential access to stored water commensurate with the phenology of each species. Studies of artificial stands under controlled conditions showed no difference in the species' ability to exploit stored water in the soil. However there was a striking difference in root behavior between Plantago and Hemizonia when plants were grown in a soil layer above a non-nutritive, waterstoring substrate. We concluded that Hemizonia, the longest lived species, survives on water stored in decomposed rock below the soil layer. Clarkia is restricted to cooler slope faces where a slightly longer growing season appears just suficient to complete reproduction. Productivity is enhanced by addition of later blooming species to the community, but there is no indication that the mixture is the most productive system.     

Multidimensional stable isotope analysis illuminates resource partitioning in a sub‐Antarctic island bird community

A central theme in community ecology is understanding how similar species co‐exist and how their interactions may evolve in the context of climate change. Most studies of resource partitioning among central place foragers, particularly birds, focus on the offspring‐rearing period, when they are accessible, but breeding success may be determined earlier and little is known about how such species partition resources at the onset of breeding. We used a non‐invasive approach to evaluate resource partitioning in co‐existing females at a sub‐Antarctic island during their pre‐laying periods. Three hypotheses were tested using carbon, nitrogen and oxygen stable isotope ratios measured in shells and membranes of hatched eggs as ecological tracers: 1) resource partitioning by geographic location and trophic level will exist among the 12 bird species and will be enhanced within taxonomic groups; 2) given the absence of strong oxygen gradients in the Southern Ocean we will not detect spatial structuring based on oxygen isotopes, but differences will exist between resident and oceanic species as the former may use meteoric water; 3) capital and income breeder strategies can be differentiated using stable isotopes of egg remains. Two and three dimensional isotopic data showed resource partitioning among species. As predicted, segregation was evident within the four main taxonomic groups: penguins, albatrosses, burrowing petrels and giant petrels. Unexpectedly, oxygen isotopes revealed widespread use of meteoric water among a suite of sub‐Antarctic birds. Stable isotopes allowed us to identify females of most species as income breeders at the onset of breeding, with the exception of the females of the two crested penguin exhibiting a mix of income and capital resources use. Multidimensional isotopic analyses revealed that resource partitioning exists at multiple stages of the annual cycle in ways likely to be important under global change, exhibiting wide potential for ecosystem analysis.     

Predation risk and resource abundance mediate foraging behaviour and intraspecific resource partitioning among consumers in dominance hierarchies

Dominance hierarchies and the resulting unequal resource partitioning among individuals are key mechanisms of population regulation. The strength of dominance hierarchies can be influenced by size‐dependent tradeoffs between foraging and predator avoidance whereby competitively inferior subdominants can access a larger proportion of limiting resources by accepting higher predation risk. Foraging‐predation risk tradeoffs also depend on resource abundance. Yet, few studies have manipulated predation risk and resource abundance simultaneously; consequently, their joint effect on resource partitioning within dominance hierarchies are not well understood. We addressed this gap by measuring behavioural responses of masu salmon Oncorhynchus masou ishikawae to experimental manipulations of predation risk and resource abundance in a natural temperate forest stream. Responses to predation risk depended on body size and social status such that larger fish (often social dominants) exhibited more risk‐averse behaviour (e.g. lower foraging and appearance rates) than smaller subdominants after exposure to a simulated predator. The magnitude of this effect was lower when resources were elevated, indicating that dominant fish accepted a higher predation risk to forage on abundant resources. However, the influence of resource abundance did not extend to the population level, where predation risk altered the distribution of foraging attempts (a proxy for energy intake) from being skewed towards large individuals to being skewed towards small individuals after predator exposure. Our results imply that size‐dependent foraging–predation risk tradeoffs can weaken the strength of dominance hierarchies by allowing competitively inferior subdominants to access resources that would otherwise be monopolized.     

Food resource partitioning and trophic morphology of Brevoortia gunteri and B. patronus

The menhadens Brevoortia gunteri and B. patronus are sympatric and morphologically similar. The two species are planktophagous and exhibited significant ( P < 0·0001) food resource partitioning, with phytoplankton predominating in B. patronus stomachs and zooplankton in B. gunteri. The branchial apparatus of both species is of the typical alosine form. Brevoortia patronus has significantly more branchiospinules per mm (=19·47) and significantly longer gill rakers (=13·35 mm) than B. gunteri (=14·11, =12·01 mm respectively). B. patronus is characterized by a gill raker system forming a fine-meshed filter capable of retaining smaller food items. The results support the hypothesis that food resource partitioning is related to different morphological features of the branchial apparatus.     

Temporal resource partitioning mitigates interspecific competition and promotes coexistence among insect parasites

A key to understanding life's great diversity is discerning how competing organisms divide limiting resources to coexist in diverse communities. While temporal resource partitioning has long been hypothesized to reduce the negative effects of interspecific competition, empirical evidence suggests that time may not often be an axis along which animal species routinely subdivide resources. Here, we present evidence to the contrary in the world's most biodiverse group of animals: insect parasites (parasitoids). Specifically, we conducted a meta-analysis of 64 studies from 41 publications to determine if temporal resource partitioning via variation in the timing of a key life-history trait, egg deposition (oviposition), mitigates interspecific competition between species pairs sharing the same insect host. When competing species were manipulated to oviposit at (or near) the same time in or on a single host in the laboratory, competition was common, and one species was typically inherently superior (i.e. survived to adulthood a greater proportion of the time). In most cases, however, the inferior competitor could gain a survivorship advantage by ovipositing earlier (or in a smaller number of cases later) into shared hosts. Moreover, this positive (or in a few cases negative) priority advantage gained by the inferior competitor increased as the interval between oviposition times became greater. The results from manipulative experiments were also correlated with patterns of life-history timing and demography in nature: the more inherently competitively inferior a species was in the laboratory, the greater the interval between oviposition times of taxa in co-occurring populations. Additionally, the larger the interval between oviposition times of competing taxa, the more abundant the inferior species was in populations where competitors were known to coexist. Overall, our findings suggest that temporal resource partitioning via variation in oviposition timing may help to facilitate species coexistence and structures diverse insect communities by altering demographic measures of species success. We argue that the lack of evidence for a more prominent role of temporal resource partitioning in promoting species coexistence may reflect taxonomic differences, with a bias towards larger-sized animals. For smaller species like parasitic insects that are specialized to attack one or a group of closely related hosts, have short adult lifespans and discrete generation times, compete directly for limited resources in small, closed arenas and have life histories constrained by host phenology, temporal resource subdivision via variation in life history may play a critical role in allowing species to coexist by alleviating the negative effects of interspecific competition.     

Frequency-dependent competitive abilities and differential resource use in competition between Drosophila hydei and D. melanogaster

Several experiments, each involving competition between Drosophila melanogaster and D. hydei in population cages, were set up and allowed to run for up to 50 weeks. The population sizes of both species, and hence the species frequencies, were monitored once a fortnight, i.e. approximately once per generation. Coexistence of the two species was observed in cages containing resource bottles with 5 g of food medium; cages whose resource bottles contained only 1.5 g resulted in competitive exclusion of D. hydei. Competitive abilities were frequency-dependent in the former case but not in the latter. Tests of larval depth distributions revealed that D. hydei larvae feed at a deeper level in the food medium than larvae of D. melanogaster. The explanation of the contrasting results of competition when bottles contained 5 g and 1.5 g of resources lies in the production of frequency-dependent competitive abilities by larval resource partitioning in the bottles with 5 g, and the preclusion of such partitioning in the 1.5 g bottles because of the very limited depth of food medium then available. The relevance of these results to a model of competition is discussed, and the potential generality of differential resource use as a stabilizing mechanism in both interspecific and intergenotypic competition is noted.     

Pitcher plant facilitates prey capture in a sympatric congener

Carnivorous plants avoid below-ground competition for nitrogen by utilizing an alternative nitrogen resource—invertebrate prey, but it remains unclear if sympatric carnivorous plants compete for prey resources. The aim of this study was to investigate if exploitative prey-resource competition occurs between the two sympatric pitcher plant species, Nepenthes rafflesiana and N. gracilis in Singapore. We first investigated if prey-resource partitioning occurs between these two species, and then investigated niche shift in N. gracilis by examining its pitcher contents along an in situ gradient of N. rafflesiana interspecific competition. Our results showed clear evidence of resource partitioning between the two species, but contrary to the expectation of competition, proximity to N. rafflesiana pitchers correlated with higher total prey numbers in N. gracilis pitchers. Our multivariate model of prey assemblages further suggested that N. rafflesiana facilitates N. gracilis prey capture, especially in several ant taxa that are trapped by both species. Concurrently, we found strong evidence for intraspecific competition between N. gracilis pitchers, suggesting that prey resources are exhaustible by pitcher-predation. Our results show that resource partitioning can be associated with facilitative interactions, instead of competition as is usually assumed. Facilitation is more typically expected between phylogenetically distant species, but divergences in resource acquisition strategies can permit facilitation between congeners.     

Inter- and intra-guild patterns of food resource utilization by chironomid larvae in a subtropical coastal lagoon

Studies on food preferences provide background information on the mechanisms that allow coexistence and resource exploitation among several species within the same system. In this study, we aimed to identify the trophic guild of chironomid larvae based on their feeding habits using gut content analysis. Larvae were collected using an Eckman-Birge grab in many areas of the subtropical Peri lagoon (southern Brazil) seasonally between March 2008 and April 2009. Null models were used to determine the frequency of co-occurrence of food items in the diets of chironomid larvae and to determine the frequency of co-occurrence of species belonging to a particular guild. Significant differences (seasonal or annual) were observed in patterns of co-occurrence of food items in the larval diets. Animal remains had a lower co-occurrence than would be expected as a result of chance, and plant items had a co-occurrence greater than would be expected by chance. The c scores for co-occurrence of species belonging to both predator and herbivore guilds revealed a higher co-occurrence of species than would be expected by chance. We suggest that the factors responsible for the results of this study were resource partitioning among species, habitat heterogeneity and resource availability in the environment.     

Coexistence via resource partitioning fails to generate an increase in community function

Classic ecological theory suggests that resource partitioning facilitates the coexistence of species by reducing inter-specific competition. A byproduct of this process is an increase in overall community function, because a greater spectrum of resources can be used. In contrast, coexistence facilitated by neutral mechanisms is not expected to increase function. We studied coexistence in laboratory microcosms of the bactivorous ciliates Paramecium aurelia and Colpidium striatum to understand the relationship between function and coexistence mechanism. We quantified population and community-level function (biomass and oxygen consumption), competitive interactions, and resource partitioning. The two ciliates partitioned their bacterial resource along a size axis, with the larger ciliate consuming larger bacteria than the smaller ciliate. Despite this, there was no gain in function at the community level for either biomass or oxygen consumption, and competitive effects were symmetrical within and between species. Because other potential coexistence mechanisms can be ruled out, it is likely that inter-specific interference competition diminished the expected gain in function generated by resource partitioning, leading to a system that appeared competitively neutral even when structured by niche partitioning. We also analyzed several previous studies where two species of protists coexisted and found that the two-species communities showed a broad range of biomass levels relative to the single-species states.