Temperature alters the relative abundance and population growth rates of species within the Dendroctonus frontalis (Coleoptera: Curculionidae) community

Temperature has strong effects on metabolic processes of individuals and demographics of populations, but effects on ecological communities are not well known. Many economically and ecologically important pest species have obligate associations with other organisms; therefore, effects of temperature on these species might be mediated by strong interactions. The southern pine beetle (Dendroctonus frontalis Zimmermann) harbors a rich community of phoretic mites and fungi that are linked by many strong direct and indirect interactions, providing multiple pathways for temperature to affect the system. We tested the effects of temperature on this community by manipulating communities within naturally infested sections of pine trees. Direct effects of temperature on component species were conspicuous and sometimes predictable based on single-species physiology, but there were also strong indirect effects of temperature via alteration of species interactions that could not have been predicted based on autecological temperature responses. Climatic variation, including directional warming, will likely influence ecological systems through direct physiological effects as well as indirect effects through species interactions.     

Indirect interactions in aphid–parasitoid communities

Indirect interactions between populations of different species can be important in structuring natural communities. Indirect effects are either mediated by changes in population densities (trophic or density-mediated effects) or by changes in the behavior of species that are not trophically connected (behavioral or trait-mediated effects). We reviewed the literature on aphids and their parasitoids to explore the various possible indirect interactions that can occur in such communities. The review was motivated by our study of a particular aphid–parasitoid community in a natural (i.e., nonagricultural) habitat, and by the wealth of information that exists about aphid–parasitoid systems in agricultural settings. We focused our review on aphid–parasitoid interactions, but considered how these were influenced by the other aphid natural enemies and also by aphid mutualists and host plants. We conclude that indirect effects are likely to have a major effect in structuring aphid–parasitoid communities, and that the latter are a valuable model system for testing ideas about community interactions. Received: December 20, 1998 / Accepted: January 12, 1999     

Positive interactions in plant communities and the individualistic-continuum concept

The individualistic nature of communities is held as a fundamental ecological tenet by many ecologists. The empirical rationale for the individualistic hypothesis is largely based on gradient analyses in which plant species are almost always found to be arranged independently of one another in “continua” along environmental gradients. However, continua are correlative patterns and do not identify the processes that determine them, and so they do not necessarily preclude the possibility of interdependent interactions within plant communities. For example, the common occurrence of positive interactions suggests that plant species may not always be distributed independently of each other. If the distributions and abundances of species are enhanced by the presence of other species, their organization is not merely a coincidence of similar adaptation to the abiotic environment. Interpretations of gradient analyses also appear to assume that interactions among species should be similar at all points along environmental axes, and that groups of species should be associated at all points on a gradient if interdependence is to be accepted. However, virtually all types of ecological interactions have been shown to vary with changes in the abiotic environment, and a number of field experiments indicate that positive effects become stronger as abiotic stress increases. Furthermore, interactions among plants have been shown to shift from competition to facilitation along environmental continua. Thus, significant interdependence may occur even when species do not fully overlap in distribution. Higher-order, indirect interactions between animals and plants, and among plants, also suggest that interdependence within communities occurs. Eliminating a species involved in an indirect interaction may not necessarily mean that its beneficiary will be eliminated from a community, but the prospect that the distribution and abundance of any species in a plant community may be positively affected by the effects that other species have on their competitors suggests that communities are organized by much more than “the fluctuating and fortuitous immigration of plants and an equally fluctuating and variable environment” as stated by Henry Gleason. The ubiquity of direct and indirect positive interactions within plant communities provides a strong argument that communities are more interdependent than current theories allow. Received: 17 February 1997 / Accepted: 23 May 1997     

Understanding and predicting effects of modified interactions through a qualitative analysis of community structure

Models of ecological communities are traditionally based on relationships between pairs of species, where the strengths of per capita interactions are fixed and independent of population abundance. A growing body of literature, however; describes interactions whose strength is modified by the density of either a third species or by one of the species involved in a pairwise interaction. These modified interactions have been treated as indirect effects, and the terminology addressing them is diverse and overlapping. In this paper we develop a general analytical framework based on a qualitative analysis of community structure to account for the consequence of modified interactions in complex ecological communities. Modified interactions are found to create both direct and indirect effects between species. The sign of a direct effect can change in some instances depending on the magnitude of a key variable or parameter, which leads to a threshold change in system structure and dynamics. By considering alternative structures of a community, we extend our ability to model perturbations that move the system far from a previous equilibrium. Using specific examples, we reinterpret existing results, develop hypotheses to guide experiments or management interventions, and explore the role of modified interactions and positive feedback in creating and maintaining alternative stable states. Through a qualitative analysis of community structure, system feedback is demonstrated as being key in understanding and predicting the dynamics of complex ecological communities.     

Inclusion of trophic interactions increases the vulnerability of an alpine butterfly species to climate change

Climate change is expected to have significant and complex impacts on ecological communities. In addition to direct effects of climate on species, there can also be indirect effects through an intermediary species, such as in host–plant interactions. Indirect effects are expected to be more pronounced in alpine environments because these ecosystems are sensitive to temperature changes and there are limited areas for migration of both species (i.e. closed systems), and because of simpler trophic interactions. We tested the hypothesis that climate change will reduce the range of an alpine butterfly (Parnassius smintheus) because of indirect effects through its host plant (Sedum sp.). To test for direct and indirect effects, we used the simulations of climate change to assess the distribution of P. smintheus with and without Sedum sp. We also compared the projected ranges of P. smintheus to four other butterfly species that are found in the alpine, but that are generalists feeding on many plant genera. We found that P. smintheus gained distributional area in climate‐only models, but these gains were significantly reduced with the inclusion of Sedum sp. and in dry‐climate scenarios which resulted in a reduction in net area. When compared to the more generalist butterfly species, P. smintheus exhibited the largest loss in suitable habitat. Our findings support the importance of including indirect effects in modelling species distributions in response to climate change. We highlight the potentially large and still neglected impacts climate change can have on the trophic structure of communities, which can lead to significant losses of biodiversity. In the future, communities will continue to favour species that are generalists as climate change induces asynchronies in the migration of species.     

Estimating co-extinction threats in terrestrial ecosystems

The biosphere is changing rapidly due to human endeavour. Because ecological communities underlie networks of interacting species, changes that directly affect some species can have indirect effects on others. Accurate tools to predict these direct and indirect effects are therefore required to guide conservation strategies. However, most extinction-risk studies only consider the direct effects of global change—such as predicting which species will breach their thermal limits under different warming scenarios—with predictions of trophic cascades and co-extinction risks remaining mostly speculative. To predict the potential indirect effects of primary extinctions, data describing community interactions and network modelling can estimate how extinctions cascade through communities. While theoretical studies have demonstrated the usefulness of models in predicting how communities react to threats like climate change, few have applied such methods to real-world communities. This gap partly reflects challenges in constructing trophic network models of real-world food webs, highlighting the need to develop approaches for quantifying co-extinction risk more accurately. We propose a framework for constructing ecological network models representing real-world food webs in terrestrial ecosystems and subjecting these models to co-extinction scenarios triggered by probable future environmental perturbations. Adopting our framework will improve estimates of how environmental perturbations affect whole ecological communities. Identifying species at risk of co-extinction (or those that might trigger co-extinctions) will also guide conservation interventions aiming to reduce the probability of co-extinction cascades and additional species losses.     

Motifs in bipartite ecological networks: uncovering indirect interactions

Indirect interactions play an essential role in governing population, community and coevolutionary dynamics across a diverse range of ecological communities. Such communities are widely represented as bipartite networks: graphs depicting interactions between two groups of species, such as plants and pollinators or hosts and parasites. For over thirty years, studies have used indices, such as connectance and species degree, to characterise the structure of these networks and the roles of their constituent species. However, compressing a complex network into a single metric necessarily discards large amounts of information about indirect interactions. Given the large literature demonstrating the importance and ubiquity of indirect effects, many studies of network structure are likely missing a substantial piece of the ecological puzzle. Here we use the emerging concept of bipartite motifs to outline a new framework for bipartite networks that incorporates indirect interactions. While this framework is a significant departure from the current way of thinking about bipartite ecological networks, we show that this shift is supported by analyses of simulated and empirical data. We use simulations to show how consideration of indirect interactions can highlight differences missed by the current index paradigm that may be ecologically important. We extend this finding to empirical plant–pollinator communities, showing how two bee species, with similar direct interactions, differ in how specialised their competitors are. These examples underscore the need to not rely solely on network‐ and species‐level indices for characterising the structure of bipartite ecological networks.     

Exploring the compass of potential changes induced by climate warming in plant communities

New models are required to predict the impacts of future climate change on biodiversity. A move must be made away from individual models of single species toward approaches with synergistically interacting species. The focus should be on indirect effects due to biotic interactions. Here we propose a new parsimonious approach to simulate direct and indirect effects of global warming on plant communities. The methodology consists of five steps: a) field survey of species abundances, b) quantitative assessment of species co-occurrences, c) assignment of a theorised effect of increased temperature on each species, d) creation of a community model to project community dynamics, and e) exploration of the potential range of temperature change effects on plant communities.We explored the possible climate-driven dynamics in an alpine vegetation community and gained insights into the role of biotic interactions as determinants of plant species response to climate change at local scale. The study area was the uppermost portion of Alpe delle Tre Potenze (Northern Apennines, Italy) from 1500 m up to the summit at 1940 m.Our work shows that: 1) unexpected climate-driven dynamics can emerge, 2) interactive communities with indirect effects among species can overcome direct effects induced by global warming; 3) if just one or few species react to global warming the new community configuration could be unexpected and counter-intuitive; 4) timing of species reactions to global warming is an important driver of community dynamics; 5) using simulation models with a limited amount of data in input, it is possible to explore the full range of potential changes in plant communities induced by climate warming.     

Shifting daylength regimes associated with range shifts alter aphid‐parasitoid community dynamics

With climate change leading to poleward range expansion of species, populations are exposed to new daylength regimes along latitudinal gradients. Daylength is a major factor affecting insect life cycles and activity patterns, so a range shift leading to new daylength regimes is likely to affect population dynamics and species interactions; however, the impact of daylength in isolation on ecological communities has not been studied so far. Here, we tested for the direct and indirect effects of two different daylengths on the dynamics of experimental multitrophic insect communities. We compared the community dynamics under “southern” summer conditions of 14.5‐hr daylight to “northern” summer conditions of 22‐hr daylight. We show that food web dynamics indeed respond to daylength with one aphid species (Acyrthosiphon pisum) reaching much lower population sizes at the northern daylength regime compared to under southern conditions. In contrast, in the same communities, another aphid species (Megoura viciae) reached higher population densities under northern conditions. This effect at the aphid level was driven by an indirect effect of daylength causing a change in competitive interaction strengths, with the different aphid species being more competitive at different daylength regimes. Additionally, increasing daylength also increased growth rates in M. viciae making it more competitive under summer long days. As such, the shift in daylength affected aphid population sizes by both direct and indirect effects, propagating through species interactions. However, contrary to expectations, parasitoids were not affected by daylength. Our results demonstrate that range expansion of whole communities due to climate change can indeed change interaction strengths between species within ecological communities with consequences for community dynamics. This study provides the first evidence of daylength affecting community dynamics, which could not be predicted from studying single species separately.     

The hidden complexity of multi‐species interactions

In this issue of the Journal of Vegetation Science, Michalet et al. used species removal experiments to detect direct and indirect species interactions in a sub‐alpine grassland. They found evidence for competition, facilitation and a range of indirect interactions at the species level, but no measurable effects when aggregated at the community level. Their results raise fundamental questions regarding the role and importance of indirect interactions in structuring ecological communities.     

Assessing the potential for indirect interactions between tropical tree species via shared insect seed predators

Natural enemies of plants have the potential to influence the dynamics of plant populations and the structure of plant communities. In diverse tropical forests, research on the effects of plant enemies has largely focused on the diversity-enhancing effects of highly specialized enemies, while the community-level effects of enemies with broader diets have rarely been considered. We investigated the community of insect seed predators interacting with seven tree species in the family Lauraceae on Barro Colorado Island (Panama). We present one of the first quantitative food webs for pre-dispersal insect seed predators and their host plants, and use the information in the web to assess the potential for indirect interactions between the tree species. Our data suggest that there is high potential for indirect interactions between Lauraceae species via their shared seed predators. The strength and direction of these interactions are largely unrelated to the phylogenetic distance and trait similarity between species but are likely governed by the volume of fruit produced by each tree species.     

Interactive effects of mycorrhizae and a root hemiparasite on plant community productivity and diversity

Plant communities can be affected both by arbuscular mycorrhizal fungi (AMF) and hemiparasitic plants. However, little is known about the interactive effects of these two biotic factors on the productivity and diversity of plant communities. To address this question, we set up a greenhouse study in which different AMF inocula and a hemiparasitic plant (Rhinanthus minor) were added to experimental grassland communities in a fully factorial design. In addition, single plants of each species in the grassland community were grown with the same treatments to distinguish direct AMF effects from indirect effects via plant competition. We found that AMF changed plant community structure by influencing the plant species differently. At the community level, AMF decreased the productivity by 15–24%, depending on the particular AMF treatment, mainly because two dominant species, Holcus lanatus and Plantago lanceolata, showed a negative mycorrhizal dependency. Concomitantly, plant diversity increased due to AMF inoculation and was highest in the treatment with a combination of two commercial AM strains. AMF had a positive effect on growth of the hemiparasite, and thereby induced a negative impact of the hemiparasite on host plant biomass which was not found in non-inoculated communities. However, the hemiparasite did not increase plant diversity. Our results highlight the importance of interactions with soil microbes for plant community structure and that these indirect effects can vary among AMF treatments. We conclude that mutualistic interactions with AMF, but not antagonistic interactions with a root hemiparasite, promote plant diversity in this grassland community. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

A highly resolved food web for insect seed predators in a species‐rich tropical forest

The top‐down and indirect effects of insects on plant communities depend on patterns of host use, which are often poorly documented, particularly in species‐rich tropical forests. At Barro Colorado Island, Panama, we compiled the first food web quantifying trophic interactions between the majority of co‐occurring woody plant species and their internally feeding insect seed predators. Our study is based on more than 200 000 fruits representing 478 plant species, associated with 369 insect species. Insect host‐specificity was remarkably high: only 20% of seed predator species were associated with more than one plant species, while each tree species experienced seed predation from a median of two insect species. Phylogeny, but not plant traits, explained patterns of seed predator attack. These data suggest that seed predators are unlikely to mediate indirect interactions such as apparent competition between plant species, but are consistent with their proposed contribution to maintaining plant diversity via the Janzen–Connell mechanism.     

Aphids indirectly increase virulence and transmission potential of a monarch butterfly parasite by reducing defensive chemistry of a shared food plant

Parasites and hosts live in communities consisting of many interacting species, but few studies have examined how communities affect parasite virulence and transmission. We studied a food web consisting of two species of milkweed, two milkweed herbivores (monarch butterfly and oleander aphid) and a monarch butterfly-specific parasite. We found that the presence of aphids increased the virulence and transmission potential of the monarch butterfly's parasite on one milkweed species. These increases were associated with aphid-induced decreases in the defensive chemicals of milkweed plants. Our experiment suggests that aphids can indirectly increase the virulence and transmission potential of monarch butterfly parasites, probably by altering the chemical composition of a shared food plant. These results indicate that species that are far removed from host-parasite interactions can alter such interactions through cascading indirect effects in the food web. As such, indirect effects within ecological communities may drive the dynamics and evolution of parasites.     

Direct and indirect effects in microcosm communities of protists

Increased complexity in biological communities can increase the variety of interactions among species, but the relative strengths and long-term consequences of various direct and indirect interactions require further investigation. I studied interactions among four species of protists by monitoring their population dynamics when they were cultured either together or in seven different subset communities. Two protists were bacterivores (Chilomonas and Tetrahymena) and two were predators (Actinosphaerium and Euplotes). Actinosphaerium was omnivorous, and could eat both predatory Euplotes and bacterivores. Three indirect effects occurred among the four species of protists, including indirect facilitation of one predator by the other, apparent competition between bacterivores, and indirect facilitation of one bacterivore by the omnivorous predator. Community structure and invasibility depended on both direct and indirect effects; thus both can be mechanisms for assembly rules.     

Community heritability measures the evolutionary consequences of indirect genetic effects on community structure

The evolutionary analysis of community organization is considered a major frontier in biology. Nevertheless, current explanations for community structure exclude the effects of genes and selection at levels above the individual. Here, we demonstrate a genetic basis for community structure, arising from the fitness consequences of genetic interactions among species (i.e., interspecific indirect genetic effects or IIGEs). Using simulated and natural communities of arthropods inhabiting North American cottonwoods (Populus), we show that when species comprising ecological communities are summarized using a multivariate statistical method, nonmetric multidimensional scaling (NMDS), the resulting univariate scores can be analyzed using standard techniques for estimating the heritability of quantitative traits. Our estimates of the broad-sense heritability of arthropod communities on known genotypes of cottonwood trees in common gardens explained 56-63% of the total variation in community phenotype. To justify and help interpret our empirical approach, we modeled synthetic communities in which the number, intensity, and fitness consequences of the genetic interactions among species comprising the community were explicitly known. Results from the model suggest that our empirical estimates of broad-sense community heritability arise from heritable variation in a host tree trait and the fitness consequences of IGEs that extend from tree trait to arthropods. When arthropod traits are heritable, interspecific IGEs cause species interactions to change, and community evolution occurs. Our results have implications for establishing the genetic foundations of communities and ecosystems.     

Wave energy alters biodiversity by shaping intraspecific traits of a habitat-forming species

The role of habitat-forming species in promoting biodiversity is widely acknowledged to vary across environmental gradients according to the extent to which they modify resources and environmental conditions. Population- and individual-level traits of habitat-forming species that influence species interactions may vary across gradients, but the importance of this indirect effect of environmental context is seldom considered. Here, we conducted surveys and field experiments to partition the effects of wave exposure on habitat-provisioning for invertebrates by oysters into direct and indirect effects, arising from morphological variation of the oysters. A survey of nine sites with varying degrees of wave exposure in Port Jackson, Australia revealed a decline in oyster densities and surface area as wave energy increased. Correlated to declining oyster surface area was a decrease in the richness and abundance of associated invertebrates. By contrast, taxon diversity increased with increasing wave energy. Experimental deployments of oysters at high and low wave energy sites confirmed that variations in oyster morphology was a phenotypically plastic response to environmental conditions. Oyster recruitment was also lower at high as compared to low wave energy sites, further contributing to the variation in oyster habitat among sites. A colonisation experiment in which exposed and sheltered morphologies of oysters were deployed under high and low wave energy conditions in a fully orthogonal design found that invertebrate communities were influenced by both the wave energy of sites and by habitat structure. Our study suggests that in some instances the indirect effects of environment on habitat availability, arising from changes in habitat-forming species density and morphology, may be as, or even more, important than the direct effects. Understanding how traits of habitat-forming species respond to environmental conditions, and how intraspecific trait-variation cascades to influence associated communities is critical to predicting when and where positive species interactions will be greatest.     

Nurse species and indirect facilitation through grazing drive plant community functional traits in tropical alpine peatlands

Facilitation among plants mediated by grazers occurs when an unpalatable plant extends its protection against grazing to another plant. This type of indirect facilitation impacts species coexistence and ecosystem functioning in a large array of ecosystems worldwide. It has nonetheless generally been understudied so far in comparison with the role played by direct facilitation among plants. We aimed at providing original data on indirect facilitation at the community scale to determine the extent to which indirect facilitation mediated by grazers can shape plant communities. Such experimental data are expected to contribute to refining the conceptual framework on plant–plant–herbivore interactions in stressful environments. We set up a 2‐year grazing exclusion experiment in tropical alpine peatlands in Bolivia. Those ecosystems depend entirely on a few, structuring cushion‐forming plants (hereafter referred to as “nurse” species), in which associated plant communities develop. Fences have been set over two nurse species with different strategies to cope with grazing (direct vs. indirect defenses), which are expected to lead to different intensities of indirect facilitation for the associated communities. We collected functional traits which are known to vary according to grazing pressure (LDMC, leaf thickness, and maximum height), on both the nurse and their associated plant communities in grazed (and therefore indirect facilitation as well) and ungrazed conditions. We found that the effect of indirectly facilitated on the associated plant communities depended on the functional trait considered. Indirect facilitation decreased the effects of grazing on species relative abundance, mean LDMC, and the convergence of the maximum height distribution of the associated communities, but did not affect mean height or cover. The identity of the nurse species and grazing jointly affected the structure of the associated plant community through indirect facilitation. Our results together with the existing literature suggest that the “grazer–nurse–beneficiary” interaction module can be more complex than expected when evaluated in the field.     

Stability of a diamond-shaped module with multiple interaction types

Indirect interactions among species emerge from the complexity of ecological networks and can strongly affect the response of communities to disturbances. To determine these indirect interactions and understand better community dynamics, ecologists focused on the interactions within small sets of species or modules. Thanks to their analytical tractability, modules bring insights on the mechanisms occurring in complex interaction networks. So far, most studies have considered modules with a single type of interaction although numerous species are involved in mutualistic and antagonistic interactions simultaneously. In this study, we analyse the dynamics of a diamond-shaped module with multiple interaction types: two resource species sharing a mutualist and a consumer. We describe the different types of indirect interaction occurring between the resource species and the conditions for a stable coexistence of all species. We show that the nature of indirect interactions between resource species (i.e. apparent facilitation, competition or antagonism), as well as stable coexistence, depend on the species generalism and asymmetry of interactions, or in other words, on the distribution of interaction strengths among species. We further unveil that a balance between mutualistic and antagonistic interactions at the level of resource species favours stable coexistence, and that species are more likely to coexist stably if there is apparent facilitation between the two resource species rather than apparent competition. Our results echo existing knowledge on the trophic diamond-shaped module, and confirm that our understanding of communities combining different interaction types can gain from module analyses.     

Nestedness patterns and the dual nature of community reassembly in California streams: a multivariate permutation‐based approach

Many factors contribute to the nonrandom processes of extinctions and invasions that are changing the structure of ecological communities worldwide. These factors include the attributes of the species, their abiotic environment, and the interactions and feedbacks between them. The relative importance of these factors has been difficult to quantify. We used nested subset theory and a novel permutation‐based extension of gradient analysis to disentangle the direct and indirect pathways by which these factors affect the metacommunity structure of freshwater fishes inhabiting the streams tributary to the San Francisco Bay. Our analyses provide quantitative measures of how species and stream attributes may influence extinction vulnerability and invasion risk, highlight the need for considering the multiple interacting drivers of community change concurrently, and indicate that the ongoing disassembly and assembly of Bay Area freshwater fish communities are not fully symmetric processes. Fish communities are being taken apart and put back together in only partially analogous trajectories of extinction and invasion for which no single explanatory hypothesis is sufficient. Our study thereby contributes to the forecasting of continued community change and its effects on the functioning of freshwater ecosystems.