Estimating competition in metacommunities: accounting for biases caused by dispersal

Understanding how the strengths of species interactions are distributed among species is critical for developing predictive models of natural food webs as well as for developing management and conservation strategies. Recently a number of ecologists have attempted to clarify the concepts of “strong-” and “weak-interactors” in a community, and to derive techniques for quantifying interaction strengths in the field, using metrics that are consistent, comparable, and of relevance to theoreticians. In this paper, we examine potential biases in different empirical approaches to quantifying variation in interaction strengths within and among natural communities. Using both simulated and published data, we explore the behavior of four commonly used or recently proposed empirical measures of the strength of consumer–prey interactions. The type of index used, the experimental protocol, and the underlying model of predator–prey interaction all strongly influence one’s perception of both (1) the distribution of interaction strengths among species (e.g., presence of “keystone” species), and (2) the specific identity of the interactions that appear to be most important. Raw treatment differences tend to emphasize effects on very abundant prey, while the three proportional indices tend to emphasize effects on extremely rare prey. Two of the proportional indices are inherently asymmetric about zero, and they inflate positive or negative effects, respectively. When predators exhibit a saturating functional response, the three proportional measures of per capita effect are biased toward a skewed distribution of interaction strengths dominated by effects on the rarest prey. Predator interference causes the per capita measures to emphasize the effects of rare predators. Estimates of per capita effects are also problematic when (1) the per capita effects are back-calculated from experiments designed to measure collective effects (e.g., predator exclusions), and (2) the collective effect of a predator is constant across a wide range of predator densities, as may be common for keystone predators. Finally, since all of the indices show time-dependent behavior, they are differentially suited for different experimental protocols (e.g., short-term vs. long-term results, or community initially near vs. far from equilibrium). All the indices explored here have the potential to provide useful, complementary information about ecological impacts of species in natural communities. In this analysis, we attempt to clarify what each index actually measures and the conditions under which each is most revealing.

Understanding how the strengths of species interactions are distributed among species is critical for developing predictive models of natural food webs as well as for developing management and conservation strategies. Recently a number of ecologists have attempted to clarify the concepts of strong- and weak-interactors in a community, and to derive techniques for quantifying interaction strengths in the field, using metrics that are consistent, comparable, and of relevance to theoreticians. In this paper, we examine potential biases in different empirical approaches to quantifying variation in interaction strengths within and among natural communities. Using both simulated and published data, we explore the behavior of four commonly used or recently proposed empirical measures of the strength of consumer-prey interactions. The type of index used, the experimental protocol, and the underlying model of predator- prey interaction all strongly influence one's perception of both (1) the distribution of in- teraction strengths among species (e.g., presence of species), and (2) the specific identity of the interactions that appear to be most important. Raw treatment differences tend to emphasize effects on very abundant prey, while the three proportional indices tend to emphasize effects on extremely rare prey. Two of the proportional indices are inherently asymmetric about zero, and they inflate positive or negative effects, respectively. When predators exhibit a saturating functional response, the three proportional measures of per capita effect are biased toward a skewed distribution of interaction strengths dominated by effects on the rarest prey. Predator interference causes the per capita measures to emphasize the effects of rare predators. Estimates of per capita effects are also problematic when (1) the per capita effects are back-calculated from experiments designed to measure collective effects (e.g., predator exclusions), and (2) the collective effect of a predator is constant across a wide range of predator densities, as may be common for keystone predators. Finally, since all of the indices show time-dependent behavior, they are differentially suited for different experimental protocols (e.g., short-term vs. long-term results, or community ini- tially near vs. far from equilibrium). All the indices explored here have the potential to provide useful, complementary information about ecological impacts of species in natural communities. In this analysis, we attempt to clarify what each index actually measures and the conditions under which each is most revealing.

Bacteriocins are bacteriocidal toxins released by almost all bacteria. They are thought to have a narrow range of killing, but as bacteriocin-mediated interactions have been rarely studied at biologically relevant scales, whether this narrow range of action falls mostly within or mostly between coexisting species in natural communities is an open question with important ecological and evolutionary implications. In a previous study, we systematically sampled Xenorhabdus bacteria along a hillside and found evidence for genotypic variability and bacteriocin-mediated interactions within Xenorhabdus bovienii and X. koppenhoeferi colonies that were collected only a few meters apart. In contrast, colonies that were isolated from the same soil sample were always genetically similar and showed no inhibitions. Here, we conducted pairwise growth-inhibition assays within and between seven X. bovienii and five X. koppenhoeferi colonies that were isolated from different soil samples; all seven X. bovienii colonies and at least three of the X. koppenhoeferi have been distinguished as distinct genotypes based on coarse-grain genomic markers. We found signatures for both conspecific and heterospecific bacteriocin inhibitions in this natural community of Xenorhabdus bacteria, but intraspecific inhibitions were significantly more common than interspecific inhibitions. These results suggest that bacteriocins have a major role in intraspecific competition in nature, but also suggest that bacterocins are important in mediating interspecific interactions among coexisting species in natural communities.

Culture experiments showed that 10 rotifer species differed greatly in their susceptibilities to mechanical interference from Daphnia pulex. Direct observations and videographic analyses of rotifers entrained in Daphnia's inhalant feeding current provided some mechanistic explanations for these differences in susceptibility. In general, well—protected species either: (1) were too large to enter Daphnia's branchial chamber (Conochilus unicornis), (2) regularly escaped from Daphnia's inhalent current (Polyarthra remata), or (3) were rejected from Daphnia's branchial chamber after very short residence times (<2 s) (Asplanchna priodonta, Keratella crassa, K. testudo, Synchaeta pectinata). Highly susceptible species were rejected from Daphnia's branchial chamber only after relatively long residence times (6—15 s) and were either small in size (Keratella cochlearis, Synchaeta ablonga) or delicate (Ascomorpha ecaudis). Species with the longest residence times probably are those that are least likely to irritate Daphnia's branchial chamber and hence the most likely to be eaten or manipulated and damaged before being detected and rejected. In natural zooplankton communities, Daphnia interference has the potential to impose high morality rates on susceptible rotifer species and, therefore, to shift the species structure of rotifer assemblages in favor of resistant species. The ability of Daphnia to suppress most rotifer species in natural communities probably is often due to the combined effects of interference and exploitative competition. Large rotifer species least susceptible to Daphnia interference should be the most susceptible to declining food availability.

In population ecology, there has been a fundamental controversy about the relative importance of competition-driven (density-dependent) population regulation vs. abiotic influences such as temperature and precipitation. The same issue arises at the community level; are population sizes driven primarily by changes in the abundances of cooccurring competitors (i.e., compensatory dynamics), or do most species have a common response to environmental factors? Competitive interactions have had a central place in ecological theory, dating back to Gleason, Volterra, Hutchison and MacArthur, and, more recently, Hubbell's influential unified neutral theory of biodiversity and biogeography. If competitive interactions are important in driving year-to-year fluctuations in abundance, then changes in the abundance of one species should generally be accompanied by compensatory changes in the abundances of others. Thus, one necessary consequence of strong compensatory forces is that, on average, species within communities will covary negatively. Here we use measures of community covariance to assess the prevalence of negative covariance in 41 natural communities comprising different taxa at a range of spatial scales. We found that species in natural communities tended to covary positively rather than negatively, the opposite of what would be expected if compensatory dynamics were important. These findings suggest that abiotic factors such as temperature and precipitation are more important than competitive interactions in driving year-to-year fluctuations in species abundance within communities.

Studies of systemic endophyte in grasses have skyrocketed in the past two decades. However, the vast majority of these studies still occur in agroecosystems. We show that ecological and evolutionary concepts derived from these systems may be misleading because they fail to incorporate the enormous variability found in endophyte-host grass interactions in wild grass populations. This variability stems from 1) genetic differences in host plants and endophytes, 2) environmental factors such as light and soil nutrients and moisture, and 3) the tangled web of interacting species in natural communities, such as conspecific and interspecific plants, multiple generalist and specialist herbivore species, and the third trophic level, predators and parasites. Studies of natural populations and communities continue to lag far behind those involving agronomic grass systems. However, we argue that additional studies of infected wild grass populations and communities are essential to advance ecological and evolutionary concepts of endophytegrass interactions. Keywords: endophytes, herbivore resistance, grasses, natural populations and communities, natural enemies, Neotyphodium, pathogens, plant defenses, variability

Animal pollinators mediate reproduction of many plant species. Foraging theory suggests that animal pollinators exhibit preferences for common plant species in natural communities (positive frequency-dependent foraging) and temporary single-species specialization (flower constancy) during foraging bouts. Positive frequency dependence may favor common plant species; flower constancy may enhance conspecific pollen transfer particularly in rare plant species. Previous experimental studies suggest that avian pollinators are unlikely to exhibit these behaviors. We studied foraging behavior of Cape Sugarbirds (Promerops cafer), the main avian pollinator of many Protea species, using focal-plant and focal-bird sampling, assisted by high-resolution maps of the spatiotemporal distribution of Protea individuals and their flowering status. We found that Sugarbird's visitation preference increased with species' relative floral abundance, and that individual Sugarbirds tended to visit single species in sequence. Flower constancy during foraging bouts was significantly higher than expected from random plant-animal encounters at the scale of pollinator movements. Positive frequency dependence may favor the reproduction of abundant plant species while flower constancy may be particularly important for rare plant species. This first simultaneous study of both behaviors in a natural plant-pollinator system shows that bird pollinators exhibit both types of behavior and, in this way, possibly influence plant community structure.

Salt marshes: biological controls of food webs in a diminishing environment

Determining the strengths of interactions among species in natural communities presents a major challenge to ecology. Using an approach combining experimental perturbations and path analysis, I examined the mechanisms by which birds directly and indirectly affected other members of an intertidal community, evaluated alternative causal hypotheses, and predicted whether interactions among the unmanipulated species would be strong or weak. Comparing treatments with t tests indicated that excluding bird predators with cages caused increases in Pollicipes polymerus, and declines in Nucella spp., Mytilus californianus, and Semibalanus cariosus. However, these conclusions provided no insight into the underlying mechanisms causing the differences. Path analysis permitted insight into the causal mechanisms by making a variety of predictions about the strength of direct interactions: (a) Bird predation negatively affects Pollicipes, but not Nucella, Leptasterias, or Mytilus; (b) Pollicipes reduces Semibalanus and Mytilus abundance because of space competition; (c) Mytilus reduces Semibalanus cover through competition for space; and (d) as prey species, Semibalanus and Pollicipes enhance Nucella density, but Nucella predation does not have important effects on Semibalanus of Pollicipes. Based on the estimated strength of direct interactions, the importance of indirect effects among species could also be predicted. In experiments manipulating Nucella, Pollicipes, Semibalanus, and birds independently of one another, I tested 11 of the interactions predicted by the path analysis; all were supported. Path analysis in conjunction with limited experiments may provide an efficient means to predict important direct and indirect interactions among unmanipulated species within ecological communities.

Rich ecosystems harbour thousands of species interacting in tangled networks encompassing predation, mutualism and competition. Such widespread biodiversity is puzzling, because in ecological models it is exceedingly improbable for large communities to stably coexist. One aspect rarely considered in these models, however, is that coexisting species in natural communities are a selected portion of a much larger pool, which has been pruned by population dynamics. Here we compute the distribution of the number of species that can coexist when we start from a pool of species interacting randomly, and show that even in this case we can observe rich, stable communities. Interestingly, our results show that, once stability conditions are met, network structure has very little influence on the level of biodiversity attained. Our results identify the main drivers responsible for widespread coexistence in natural communities, providing a baseline for determining which structural aspects of empirical communities promote or hinder coexistence.

Within natural communities, different taxa display different dynamics in time. Why this is the case we do not fully know. This thwarts our ability to predict changes in community structure, which is important for both the conservation of rare species in natural communities and for the prediction of pest outbreaks in agriculture. Species sharing phylogeny, natural enemies and/or life-history traits have been hypothesized to share similar temporal dynamics. We operationalized these concepts into testing whether feeding guild, voltinism, similarity in parasitoid community and/or phylogenetic relatedness explained similarities in temporal dynamics among herbivorous community members. Focusing on two similar datasets from different geographical regions (Finland and Japan), we used asymmetric eigenvector maps as temporal variables to characterize species- and community-level dynamics of specialist insect herbivores on oak (Quercus). We then assessed whether feeding guild, voltinism, similarity in parasitoid community and/or phylogenetic relatedness explained similarities in temporal dynamics among taxa. Species-specific temporal dynamics varied widely, ranging from directional decline or increase to more complex patterns. Phylogeny was a clear predictor of similarity in temporal dynamics at the Finnish site, whereas for the Japanese site, the data were uninformative regarding a phylogenetic imprint. Voltinism, feeding guild and parasitoid overlap explained little variation at either location. Despite the rapid temporal dynamics observed at the level of individual species, these changes did not translate into any consistent temporal changes at the community level in either Finland or Japan. Overall, our findings offer no direct support for the notion that species sharing natural enemies and/or life-history traits would be characterized by similar temporal dynamics, but reveal a strong imprint of phylogenetic relatedness. As this phylogenetic signal cannot be attributed to guild, voltinism or parasitoids, it will likely derive from shared microhabitat, microclimate, anatomy, physiology or behaviour. This has important implications for predicting insect outbreaks and for informing insect conservation. We hope that future studies will assess the generality of our findings across plant-feeding insect communities and beyond, and establish the more precise mechanism(s) underlying the phylogenetic imprint.

Intra- and interspecific interactions can be broken down into facilitative and competitive components. The net interaction between two organisms is simply the sum of these counteracting elements. Disentangling the positive and negative components of species interactions is a critical step in advancing our understanding of how the interaction between organisms shift along physical and biotic gradients, and whether component interactions are unique or redundant across species in natural communities. We performed a manipulative field experiment to quantify the positive and negative components of the interactions between a perennial forb, Aster tenuifolius, and three dominant, matrix-forming grasses and rushes in a New England salt marsh. Specifically, we asked whether positive and negative interaction components: (1) are unique or redundant across three matrix-forming grass and rush species (Juncus gerardi, Distichlis spicata, and Spartina patens), and (2) change across Aster life stages (seedling, juvenile, and adult). For adult forbs, the strength of the facilitative component of the matrix-forb interaction was stronger than the competitive component for two of the three matrix species, leading to net positive interactions. There was no statistically significant variation among matrix species in their net or component effects, however, the competitive effect of J. gerardi was negligible, especially compared to that of D. spicata. We found little difference in the effects of J. gerardi on Aster at later life-history stages; interaction component strengths did not differ between juveniles and adults. However, mortality of seedlings in neighbor removal plots was 100%, indicating a particularly strong and critical facilitative effect of matrix species on this forb during the earliest life stages. Overall, our results indicate that matrix forming grasses and rushes have important, yet largely redundant, positive net effects on Aster performance across its life cycle. Studies that untangle various components of interactions and their contingencies are critical to both expanding our basic understanding of community organization, and predicting how natural communities and their component parts will respond to environmental change.

Phenological shifts can alter the relative arrival time of competing species in natural communities, but predicting the consequences for species interactions and community dynamics is a major challenge. Here we show that differences in relative arrival time can lead to predictable priority effects that alter the outcome of competitive interactions. By experimentally manipulating the relative arrival time of two competing tadpole species across a resource gradient, we found that delaying relative arrival of a species reduced the interaction asymmetry between species and could even reverse competitive dominance. However, the strength of these priority effects was contingent on the abundance of the shared resource. Priority effects were generally weak when resources were limited, but increased at higher resource levels. Importantly, this context dependency could be explained by a shift in per capita interaction strength driven by a shift in relative body sizes of competitors. These results shed new light into the mechanisms that drive variation in priority effects and help predict consequences of phenological shifts across different environments.

Attempts to answer the old question of whether high diversity causes high invasion resistance have resulted in an invasion paradox: while large-scale studies often find a positive relationship between diversity and invasibility, small-scale experimental studies often find a negative relationship. Many of the small-scale studies are conducted in artificial communities of even-aged plants. Species in natural communities, however, do not represent one simultaneous cohort and occur at various levels of spatial aggregation at different scales. This study used natural patterns of diversity to assess the relationship between diversity and invasibility within a uniformly managed, semi-natural community. In species-rich grassland, one seed of each of ten species was added to each of 50 contiguous 16 cm(2) quadrats within seven plots (8 × 100 cm). The emergence of these species was recorded in seven control plots, and establishment success was measured in relation to the species diversity of the resident vegetation at two spatial scales, quadrat (64 cm(2)) within plots (800 cm(2)) and between plots within the site (approx. 400 m(2)) over 46 months. Invader success was positively related to resident species diversity and richness over a range of 28-37 species per plot. This relationship emerged 7 months after seed addition and remained over time despite continuous mortality of invaders. Biotic resistance to plant invasion may play only a sub-ordinate role in species-rich, semi-natural grassland. As possible alternative explanations for the positive diversity-invasibility relationship are not clear, it is recommended that future studies elaborate fine-scale environmental heterogeneity in resource supplies or potential resource flows from resident species to seedlings by means of soil biological networks established by arbuscular mycorrhizal fungi.

Despite the progressive accumulation of exotic species in natural communities, little effort has been devoted to elucidating the mechanisms underpinning the coexistence of invaders in environmentally and biologically heterogeneous systems. The exotic seaweeds, Asparagopsis taxiformis and Caulerpa racemosa, exhibit a segregated distribution on Mediterranean rocky reefs. A. taxiformis dominates assemblages in topographically complex habitats, but is virtually absent on homogenous platforms. In contrast, C. racemosa achieves extensive cover in both types of habitat. We assessed whether differences in their distribution were generated by biotic interactions (between invaders and/or between invaders and natives) or by environmental constraints. Three models were proposed to explain seaweed distribution patterns: (1) invaders inhibit one another; (2) native assemblages, differing between complex and simple habitats, prevent the establishment/spread of one invader, but not that of the other; and (3) environmental conditions regulate the establishment/persistence of the seaweeds in different habitats. We removed the dominant invader and resident assemblages in each type of habitat. Moreover, A. taxiformis thalli were transplanted into the habitat dominated by C. racemosa to establish whether its failure to colonize the simple habitat was due to the lack of propagules or post-recruitment mortality. C. racemosa spread in the complex habitat was not influenced by the removal of resident assemblages, but it was slightly enhanced by A. taxiformis removal. Neither C. racemosa removal nor that of resident assemblages promoted A. taxiformis colonization and survival in simple habitats. Our results suggest that heterogeneity in environmental conditions can promote invader coexistence by mitigating the effects of negative biotic interactions. Therefore, the accumulation of introduced species in native communities does not necessarily imply established invaders fostering further invasion.