Direct and indirect effects of predators on the dominant invertebrates of two freshwater littoral communities

Summary Two congeneric damselfly species, Enallagma traviatum and E. aspersum, dominate the littoral macroinvertebrates of Bays Mountain Lake and of the adjacent fish-free Ecology Pond, respectively (northeastern Tennessee, USA). Extending previous experimental studies, we test seven hypotheses concerning the role of fish (bluegill sunfish, Lepomis macrochirus) and larvaldragonfly (Anax junius) predation, competitive effects on damselflies, and the interaction between competition and predation, in determining invertebrate dominance in these communities. Three types of experiments were conducted: an enclosure experiment within Ecology Pond, an outdoor replicated tub experiment, and a laboratory behavior experiment. The in-situ enclosure experiment showed that E. traviatum larvae were more susceptible to Anax predation than were E. aspersum larvae; a tendency toward greater vulnerability to fish of E. aspersum compared with E. traviatum was not statistically significant. The outdoor tub experiment confirmed both of these trends with statistically significant results. In the tubs, both predators inhibited feeding of both zygopterans (as indicated by reduced fecal mass), particularly for E. aspersum in the presence of fish. This effect appears to have been primarily indirect, mediated through exploitation of the zooplankton. We also detected competitive effects of E. traviatum on E. aspersum: E. traviatum reduced the emergence and increased the exposure above the substrate of E. aspersum. In the absence of predators, E. traviatum inhibited feeding of E. aspersum via interference. In the laboratory behavior experiment, predators inhibited crawling by E. aspersum. E. aspersum was more exposed than was E. traviatum; it swam and crawled more than did E. traviatum, considerably increasing these movements at night. Over all, E. traviatum consistently appeared to be the more cryptic of the two species, and E. aspersum appeared to be much more active. Our results suggest an explanation for the clear difference in structure between communities like Bays Mountain Lake and Ecology Pond: predaceous fish eliminate large invertebrate predators and shift the community toward cryptic forms at relatively low densities, reflecting the effects of both predation and exploitation competition. In the absence of fish, large invertebrate predators are less able to deplete littoral invertebrates but may favor the more active forms, perhaps because these are better able to avoid invertebrate predators.     

Direct and indirect effects of predation,herbivory and surface rugosity on mussel recruitment

Summary The predatory gastropod Nucella lapillus, commonly preys upon the mussel, Mytilus edulis, and is thought to control the distribution and abundance of mussels on the rocky shores of New England, USA. In this study, done in Maine, USA, not only the presence of Nucella lapillus but also the roughness of the experimental surface and the presence of the herbivorous gastropod, Littorina littorea, were manipulated. Four types of surfaces were used as recruitment substrata for mussels: smooth bare granite, aggregations of the barnacle, Semibalanus balanoides, fiberglass resin castings of smooth bare granite and resin castings of aggregations of S. balanoides. To ensure that caged N. lapillus were not starving, barnacles were provided as alternative prey. Experiments showed no detectable effect of N. lapillus on the recruitment of M. edulis. Mussel recruitment was enhanced by surface rugosity and depressed by the activities of L. littorea. Analysis of covariance, using the number of algal species as the covariate, suggested that L. littorea reduced the number of newlyrecruited mussels by removing algae that provided recruitment sites, but no manipulations were done to test this conjecture. It is likely that previous reports of N. lapillus controlling mussel abundance are attributable to N. lapillus preying upon barnacles, which increase surface rugosity and enhance mussel recruitment. Review of literature on feeding preferences of N. lapillus supports this view. When handling times and prey availability are taken into account, Nucella shows a clear preference for barnacles over mussels.     

The influence of salt and nitrogen on herbivore abundance: direct and indirect effects

We report on the influence of experimentally increased interstitial salinity and plant nitrogen on the abundance of the delphacid planthopper, Prokelisia marginata (Van Duzee) (Homoptera: Delphacidae), which feeds on salt marsh cordgrass, Spartina alterniflora. We also report the effects of these treatments on parasitism of P. marginata eggs by the fairyfly parasitoid, Anagrus sophiae (Hymenoptera: Mymaridae). Soil salinity was significantly elevated following the addition of salt pellets broadcast over the ground and plant foliar nitrogen was significantly increased after the addition of fertilizer. The addition of fertilizer increased P. marginata densities on Spartina but addition of salt did not. Neither treatment significantly affected levels of egg parasitism by A. sophiae. In this system direct effects of plants on their herbivores via changes in plant chemistry appear more important than indirect effects of plants on herbivores via their natural enemies. Received: 1 August 1997 / Accepted: 29 September 1997     

Effects of insect damage on photosynthesis,transpiration and SO2 uptake by sycamore

Summary The bilberry (Vaccinium myrtillus L.), is the dominant plant in the field layer of many boreal forests in northern Sweden. It is utilized by several herbivorous insect larvae as food (i.e. Lepidoptera: Geometridae, Tortricidae and Hymenoptera: Symphyta). Total density of insect larvae was 63% lower where birds had access to larvae compared to exclosures. Larvae with a feeding behaviour which exposes them to birds (geometrids and sawflies) showed a pronounced reduction in density when exposed to bird predators. Density of larvae with a concealed feeding behaviour (tortricids) was unaffected by birds. The frequency of larval damage to bilberry annual shoots was significantly higher in areas where larval density was high due to exclusion of birds. I concluded that birds have the potential to heavily modify the interaction between bilberry and insect larvae.     

Interactive effects of episodic hypoxia and cannibalism on juvenile blue crab mortality

We hypothesized that as the spatial extent of hypoxic bottom water increased, (1) adult blue crab predator densities would increase in shallow habitats as they avoided hypoxia, and that (2) juvenile blue crabs, which use shallow unvegetated habitat as a predation refuge from adult conspecifics, would experience increased mortality rates during crowding by cannibalistic adult blue crabs. These hypotheses were tested along a depth gradient of sandy-mud shoreline in the Neuse River Estuary (NRE), North Carolina, USA using a combination of (1) hydrographic measurements to characterize the spatial extent of hypoxia, (2) beach seines to quantify the density of adult blue crab predators in relatively shallow water as a function of 1, and (3) tethering experiments to quantify relative rates of predation on juvenile blue crabs as a function of 1 and 2. During our seven tethering experiments, the NRE study site experienced a range of DO scenarios including normoxia, chronic hypoxia, and hypoxic upwelling. No known predators of juvenile blue crabs, other than adult conspecifics, were collected in any of our shallow-water seines. During the transition from normoxia to chronic hypoxia, blue crab predator densities in shallow refuge habitats increased 4-fold, and relative mortality rates of juvenile blue crabs in shallow habitats increased exponentially with the density of adult conspecifics. Conversely, during hypoxic upwelling events, the density of adult blue crabs in shallow water declined, which may explain why the relative mortality of juvenile crabs did not increase significantly with the increasing spatial extent of hypoxia. Thus, juvenile blue crabs may be relatively safe from adult conspecifics during hypoxic upwelling events, but not during chronic hypoxia. These experimental results highlight the need to consider the effects of dynamic water quality on mobile consumers emigrating from degraded habitats when considering indirect trophic impacts beyond the immediate area of impact.     

Predator-prey interactions in a benthic stream community: a field test of flow-mediated refuges

Ecological theory suggests that the impact of predation can be strongly modified by the existence of regions of the environment in which prey are less accessible to predators, which underscores the need for empirical studies examining the factors influencing the availability and importance of such prey refuges. Our study tested whether benthic microhabitats with high flows provide suspension-feeding larval black flies (Simulium␣vittatum) with a spatial refuge in which the negative impact of predatory flatworms (Dugesia dorotocephala) is reduced. We conducted a short-term field experiment in Chester Creek (southeastern Pennsylvania, United States) to examine how the number of black fly larvae inhabiting tile substrates responded to manipulated variations in flatworm abundance and current speed. The abundance of flatworms declined with increasing current speed, thereby creating the potential for sites with high flows to provide larvae with a refuge from these predators. Multiple regression analysis revealed that the final abundance of larvae exhibited a significant negative relationship to flatworm abundance and a significant positive relationship to current speed. After adjusting for variations in elapsed time and initial larval abundance, flow and predators explained 38% of the variation in the rate of change in larval abundance. The positive correlation between larval abundance and flow had two components: a positive, direct effect of flow on larvae, which arises because these food-limited consumers prefer to reside within sites with faster flows where they can feed at higher rates; and a negative effect of flow on predators, and of predators on larvae, which combine to yield a positive indirect effect of flow on larvae. This indirect effect demonstrates the existence of flow-mediated refuges (i.e., microhabitats in which the impact of predation is reduced due to high flows), although the effect accounts for a small proportion of total variation in larval abundance. A consideration of biomechanical relationships suggests that microhabitats with high flows are likely to create prey refuges in a wide range of freshwater and marine benthic environments. In particular, predators will often experience greater dislodgement forces than prey because of their larger size and because they project farther above the bed where current speeds are faster. Moreover, the ability to resist a given dislodgement force may be greater for many prey, especially those that are sessile or semi- sessile. Received: 31 March 1997 / Accepted: 25 October 1997     

The impacts of extreme and fluctuating temperatures on trait‐mediated indirect aphid–parasitoid interactions

1. Global climate change models predict an increase in the frequency and magnitude of extreme temperature events. These temperature events, heatwaves for example, will impact a wide range of physiological and behavioural processes, particularly in ectotherms, and may therefore influence interactions between species. 2. Anti‐predator responses may be more costly under more severe temperature regimes and therefore trait‐mediated disturbance could lead to high mortality or reduced reproduction under extreme and fluctuating temperature regimes. 3. We examined the impacts of extreme and fluctuating temperatures on trait‐mediated indirect interactions in an aphid–parasitoid community. 4. In treatments that isolated the effects of trait‐mediated disturbance from the effects of foraging parasitoids we found that an increase in both the amplitude and frequency of peak temperatures reduced aphid numbers and provided evidence that the cost of trait‐mediated disturbance could increase under frequent periods of high temperature. Aphid dispersal also increased with more frequent periods of high temperature. 5. In treatments where female wasps were allowed to freely forage (direct + trait‐mediated effects), there was no evidence that extreme and fluctuating temperatures influenced the wasp's foraging ability. Exposure to extreme fluctuating temperatures did not influence the offspring production of exposed wasps or the position of the mummies within the plots.     

Habitat effects on the relative importance of trait- and density-mediated indirect interactions

Classical views of trophic cascades emphasize the primacy of consumptive predator effects on prey populations to the transmission of indirect effects [density-mediated indirect interactions (DMIIs)]. However, trophic cascades can also emerge without changes in the density of interacting species because of non-consumptive predator effects on prey traits such as foraging behaviour [trait-mediated indirect interactions (TMIIs)]. Although ecologists appreciate this point, measurements of the relative importance of each indirect predator effect are rare. Experiments with a three-level, rocky shore food chain containing an invasive predatory crab ( Carcinus maenas ), an intermediate consumer (the snail, Nucella lapillus ) and a basal resource (the barnacle, Semibalanus balanoides ) revealed that the strength of TMIIs is comparable with, or exceeds, that of DMIIs. Moreover, the sign and strength of each indirect predator effect depends on whether it is measured in risky or refuge habitats. Because habitat shifts are often responsible for the emergence of TMIIs, attention to the sign and strength of these interactions in both habitats will improve our understanding of the link between individual behaviour and community dynamics.     

生态系统基于性状调节的物种间接作用:特征、成因及后果

物种之间的间接作用关系是维持生物群落结构以及生态系统功能的关键因素。目前的理论模型和实验性研究均认为,物种间接作用的传递主要是由物种的密度变化所引起。但大量的实验证据表明,生物个体在形态、生理、行为和生活史性状的适应性变化,是物种间形成间接互作关系的另一个重要机制。生态学家把这种基于物种性状调控的种间关系称为性状调节的间接作用。深入了解性状调节的间接作用类型,发生机制和作用途径,有助于阐释自然界中多物种种间关系的复杂性和多样性形成机制。对性状调节的概念和性状的分类进行系统的总结,指出性状可塑性和物种特异性是物种间性状调节关系形成的两个重要机制。与其他类型的种间互作一样,性状调节的种间作用是驱动物种进化的重要力量。此外,分析了性状调节在自然群落中传递的几个重要途径,并强调这些间接作用在影响和调节生态系统功能和过程中的重要作用。最后,就性状调节种间关系的研究对象、研究尺度、以及研究方法等问题提出若干建议,为今后对这一问题的研究提供相关参考。     

Experimental studies of exploitative competition in a grazing stream insect

Summary Field and laboratory experiments were conducted to determine whether intraspecific competition for food occurs during the larval stage of the periphyton-grazing caddisfly Glossosoma nigrior (Trichoptera: Glossosomatidae). Larvae were placed in field enclosures at densities less than, equal to, or greater than their natural densities. Most of these individuals began to pupate after 3 weeks, whereupon the mass of each individual was determined. Final mass declined significantly as larval densities increased, whereas neither developmental rate nor mortality/emigration rate was significantly affected by density manipulations. a supplemental experiment comparing the final mass of individuals grown at reduced densities in a laboratory stream with individuals from a natural stream bottom confirmed the results of the more extensive field experiment: reductions in density resulted in significant increases in final mass. Periphyton availability in field enclosures declined according to a negative exponential function as larval densities increased. Over the 25-fold range of larval densities used in these experiments, the final mass of individuals increased linearly with periphyton standing crops. This result suggests that Glossosoma larvae may compete for food even at densities below those employed in this study. Path analysis was used to explore the importance of indirect (i.e., exploitative) and direct (i.e, interference) mechanisms for the observed competitive effects. The analysis indicates that a model based solely on exploitation explains nearly as much of the variance in mass as a model incorporating both interference and exploitation.     

Belowground interactions shift the relative importance of direct and indirect genetic effects

Intraspecific genetic variation can affect decomposition, nutrient cycling, and interactions between plants and their associated belowground communities. However, the effects of genetic variation on ecosystems can also be indirect, meaning that genes in a focal plant may affect ecosystems by altering the phenotype of interacting (i.e., neighboring) individuals. We manipulated genotype identity, species identity, and the possibility of belowground interactions between neighboring Solidago plants. We hypothesized that, because our plants were nitrogen (N) limited, the most important interactions between focal and neighbor plants would occur belowground. More specifically, we hypothesized that the genotypic identity of a plant's neighbor would have a larger effect on belowground biomass than on aboveground biomass, but only when neighboring plants were allowed to interact belowground. We detected species‐ and genotype‐level variation for aboveground biomass and ramet production. We also found that belowground biomass and ramet production depended on the interaction of neighbor genotype identity and the presence or absence of belowground interactions. Additionally, we found that interspecific indirect genetic effects (IIGEs; changes in focal plant traits due to the genotype identity of a heterospecific neighbor) had a greater effect size on belowground biomass than did focal genotype; however, this effect only held in pots that allowed belowground interactions. These results expand the types of natural processes that can be attributed to genotypes by showing that, under certain conditions, a plant's phenotype can be strongly determined by the expression of genes in its neighbor. By showing that IIGEs are dependent upon plants being able to interact belowground, our results also provide a first step for thinking about how genotype‐based, belowground interactions influence the evolutionary outcomes of plant‐neighbor interactions.     

Community organization in streams: the importance of species interactions,physical factors,and chance

Summary Experimental studies were used to examine the mechanisms governing the distribution and abundance of two major patch types in unshaded reaches of Augusta Creek, Michigan (USA). One patch type is dominated by Cladophora glomerata, a macroalga potentially able to monopolize space, whereas the other type is comprised of a low-growing, epilithic microalgal lawn inhabited by several species of sessile grazers (especially the caddisflies Leucotrichia pictipes and Psychomyia flavida). Cladophora patches are absent from mid-channel sites characterized by current velocities ca. 50 cm s^–1; caging experiments indicate that their absence is due to grazing by crayfish (Orconectes propinquus). Cladophora's presence in sites with velocities >50 cm s^–1 apparently results in part because crayfish foraging activity is impaired in high flow regimes. The presence of Cladophora strongly affects various other invertebrates due to its alteration of abiotic and biotic characteristics of the microhabitat. For example, the abundance of sessile grazers (e.g. Leucotrichia and Psychomyia) that inhabit microalgal patches is negatively correlated to the abundance of Cladophora, whereas the abundance of several other invertebrates (e.g. Stenonema mayflies and Taeniopteryx stoneflies) is positively correlated to Cladophora's abundance. Therefore, in some portions of this system, crayfish act as keystone predators because of their ability to regulate the abundance of Cladophora, which in turn has strong positive and negative effects on other components of the community. Cladophora does not always monopolize space at high velocities in the absence of crayfish, however. If sessile grazers arrive at such sites before Cladophora, they can prevent its establishment. Thus, where crayfish are absent, the likelihood that a site will be dominated by either Cladophora patches or sessile grazer — microalgal lawn patches depends on two sets of stochastic processes: (1) those that create bare space (e.g. disturbance and grazer emergence); and (2) those controlling the timing of recruitment by Cladophora or grazers at these bare sites. These priority effects (i.e. the ability of grazers and Cladophora to inhibit each other's establishment) contribute to the marked spatial heterogeneity of these two patch types. Collectively, these results demonstrate how interactions between competition, predation, and physical factors can generate a complex mixture of community patterns.     

Herbivore-induced indirect interaction webs on terrestrial plants: the importance of non-trophic, indirect, and facilitative interactions

One of the most important issues in ecology is understanding the causal mechanisms that shape the structure of ecological communities through trophic interactions. The focus on direct, trophic interactions in much of the research to date means that the potential significance of non-trophic, indirect, and facilitative interactions has been largely ignored in traditional food webs. There is a growing appreciation of the community consequences of such non-trophic effects, and the need to start including them in food web research. This review highlights how non-trophic, indirect, and facilitative interactions play an important role in organizing the structure of plant-centered arthropod communities. I argue that herbivore-induced plant responses, insect ecosystem engineers, and mutualisms involving ant–honeydew-producing insects all generate interaction linkages among insect herbivores, thereby producing complex indirect interaction webs on terrestrial plants. These interactions are all very common and widespread on terrestrial plants, in fact they are almost ubiquitous, but these interactions have rarely been included in traditional food webs. Finally, I will emphasize that because the important community consequences of these non-trophic and indirect interactions have been largely unexplored, it is critical that indirect interaction webs should be the focus of future research.     

Direct and indirect effects of predation on mosquitofish behavior and survival

Predation can have strong direct and indirect effects on the behavior of prey. We investigated whether predation by chain pickerel (Esox niger) caused adult eastern mosquitofish (Gambusia holbrooki) to alter their habitat use and whether pickerel predation influenced survival of adult and neonate mosquitofish. The number of adult mosquitofish using the riskier of three habitats was lowest when two predators occupied the risky habitat, intermediate in the treatment with one predator, and highest when no predators occurred there. More mosquitofish neonates survived high predation treatments than treatments lacking pickerel. We conclude that pickerel predation causes adult mosquitofish to shift to refuge habitats. The pattern of neonate survival suggests that adult habitat use may create a refuge from cannibalism for neonate mosquitofish, resulting in higher neonate survival in treatments with more pickerel. Hence, pickerel predation has a direct effect on adult mosquitofish behavior and a strong indirect effect on neonate survival. Both interspecific and intraspecific predation can effect prey populations and can interact to produce important indirect effects.     

Possible indirect interactions between transient and resident killer whales: implications for the evolution of foraging specializations in the genus Orcinus

Summary Two distinct forms of killer whale (Orcinus orca) occur off the coast of British Columbia, Alaska and Washington State. These have different diets, and may be reproductively isolated. Because the primary food of transient whales (pinnipeds) is a potential competitor for the primary food of resident whales (salmon), or for the smaller fishes on which salmon feed, there should be an indirect interaction between the two forms of killer whale. We use simple mathematical models to show that this interaction will be either of a plus-minus type, or a plus-plus type (indirect mutualism), depending on whether or not pinnipeds and residents are on the same trophic level. In the case of the plus-minus interaction, increasing the population density or improving the environmental conditions of transients will increase the population density of residents, while increasing resident populations will reduce the equilibrium population size of transients. In the case of the plus-plus interaction, increasing the population density or improving the environmental conditions of transients will increase the population density of residents, while increasing resident populations will reduce the equilibrium population size of transients. In the case of the plus-plus interaction, increasing the population density or improving the environmental conditions of transients will increase the population density of residents, and vice versa. Such effects may not be currently manifest due to reduced populations at most levels in the food web. Regardless, considering such indirect interactions may be important for the management of many of the species involved, and can also provide a valuable framework for examining the evolution of the two forms of killer whales. Frequency-dependent indirect interactions, acting in concert with density-dependence within populations and disruptive selection on prey-type specific foraging characteristics, may have favoured reproductive isolation of the two forms of killer whales. We suggest that these two forms of whale are in the process of speciating, i.e., the two forms are incipient species.     

Alteration of trophic interactions between periphyton and invertebrates in an acidified stream: a stable carbon isotope study

The hypothesis according to which proliferation of periphytic algae under acid conditions results from a release of grazing pressure is tested. Stable carbon isotope analysis is used to investigate the autochthonous/allochthonous balance of invertebrate feeding in streamside artificial channels that were experimentally acidified. We find that the relative contribution of autochthonous food sources (epilithon) to total invertebrate biomass was slightly lower (after 1 mo of acidification) or not altered (after 2 mo) under acidified conditions when compared with a control. Feeding shifts were exhibited by some invertebrate taxa and provided evidence that acidification modifies trophic interactions between attached algae and primary consumers. Cross-treatment calculations showed that reduction of grazing pressure after the first month of acidification was an effect rather than the cause of periphyton proliferation. Our approach using stable carbon isotope analysis and biomass measurements of macroinvertebrates allows the quantification of the trophic base of lotic secondary producer communities under both experimental and natural conditions.     

An experimental evaluation of the direct and indirect effects of endemic seaweeds,barnacles, and invertebrate predators on the abundance of the introduced rocky intertidal barnacle Balanus glandula

The barnacle, Balanus glandula has recently invaded along the Pacific coast of eastern Hokkaido, Japan. To evaluate the direct and indirect effects of endemic seaweeds, barnacles, and invertebrate predators on the abundance of B. glandula on the rocky intertidal coast of eastern Hokkaido, we conducted a field experiment from June 2011 to October 2012 in which we manipulated the presence or absence of these factors. Seaweeds showed no significant effect on the abundance of B. glandula. The endemic barnacle Chthamalus dalli and the invertebrate predator Nucella lima reduced the abundance of B. glandula. However, the simultaneous influence of N. lima and C. dalli was compensative rather than additive, probably due to keystone predation. These findings suggest that competition by the endemic barnacle C. dalli and predation by the invertebrate predator N. lima decreased the abundance of B. glandula, but that N. lima predation on C. dalli weakened the negative influence of C. dalli on B. glandula. The implications of these findings are twofold: the endemic competitor and invertebrate predator may have played important roles in decreasing the abundance of B. glandula in natural habitats, and conservation of endemic invertebrate predators may be crucial to impede the establishment and survival of introduced barnacles in rocky intertidal habitats.     

Competition,predation and flow rate as mediators of direct and indirect effects in a stream food chain

Using semi-natural stream channels, we estimated the effects of competition and predation exerted by juvenile and adult exotic rainbow trout (Oncorhynchus mykiss) on the diel activity pattern of juvenile native Atlantic salmon (Salmo salar), a secondary consumer. We also evaluated the direct and indirect effects of competition, predation and abiotic factors (water depth and velocity) on the growth rate of salmon, the biomass of invertebrate grazers (primary consumers) and the biomass of periphytic algae (primary producers; chlorophyll a). The presence of chemical cues emanating from adult predatory trout reduced the daily activity of juvenile Atlantic salmon. In contrast, competition imposed by juvenile rainbow trout forced Atlantic salmon to be more active during the day, even if adult rainbow trout were also present. We found no effect of either competition or of predatory cues on the growth rate of Atlantic salmon, and no evidence of indirect effects on either the biomass of invertebrates or the biomass of chlorophyll a. In contrast, we demonstrated that this food chain (fish--invertebrate grazers--periphytic algae) was under the control of a critical abiotic factor, the water velocity, and of bottom-up processes. We concluded that the exotic species directly increases the risk of predation of the native Atlantic salmon, but behavioral compensation probably limits the effects on growth rate. The competition and predation imposed by the invaders had no indirect effects on lower trophic levels. Top-down effects may have been mitigated by the dominant influence of water velocity controlling all components of the food chain and by elevated levels of primary production.     

Effects of parasitoid fecundity and host resistance on indirect interactions among hosts sharing a parasitoid

We examine the effects of fecundity‐limited attack rates and resistance of hosts to parasitism on the dynamics of two‐host–one‐parasitoid systems. We focus primarily on the situation where one parasitoid species attacks two host species that differ in their suitability for parasitism. While all eggs allocated to suitable hosts develop into adult parasitoids, some of the eggs allocated to marginal host do not develop. Marginal hosts can therefore act as a sink for parasitoid eggs. Three‐species coexistence is favoured by low levels of parasitoid fecundity and by low levels of suitability of the marginal host. Our model also produces an indirect (+, ?) interaction in which the suitable host can benefit from the presence of the marginal host, but the marginal host suffers from the presence of the suitable host. The mechanism driving the indirect (+, ?) interaction is egg limitation of parasitoids incurred by allocating eggs to marginal hosts.