Trophic and non-trophic pathways mediate apparent competition through post-dispersal seed predation in a Patagonian mixed forest

Post‐dispersal predation can be a major source of seed loss in temperate forests. Little is known, however, about how predator‐mediated indirect interactions such as apparent competition alter survival patterns of canopy tree seeds. Understorey plants may enhance tree seed predation by providing sheltered habitat to granivores (non‐trophic pathway). In addition, occurrence of different tree seeds in mixed patches may lead to short‐term apparent competition between seed types, because of the granivores’ foraging response to changes in food patch quality (trophic pathway). We hypothesised that understorey bamboo cover and mixing of seed species in food patches would both increase tree seed predation in a Nothofagus dombeyi?Austrocedrus chilensis forest in northern Patagonia, Argentina. Seed removal experiments were conducted for three consecutive years (2000–2002) differing in overall granivory rates. Seed patch encounter and seed removal rates were consistently higher for the larger and more nutritious Austrocedrus seeds than for the smaller Nothofagus seeds. Seed removal was greater beneath bamboo than in open areas. This apparent competition pathway was stronger in a low‐predation year (2000) than in high‐predation years (2001–2002), suggesting a shift in microhabitat use by rodents. Patch composition had a significant, though weaker, impact on seed survival across study years, whereas seed density per patch enhanced encounter rates but did not influence seed removal. Removal of the less‐preferred Nothofagus seeds increased in the presence of Austrocedrus seeds, but the reciprocal indirect effect was not observed. However, this non‐reciprocal apparent competition between seed species was only significant in the high‐predation years. Our study shows that granivore‐mediated indirect effects can arise through different interaction pathways, affecting seed survival patterns according to the predator's preference for alternative seed types. Moreover, results indicate that the occurrence and relative strength of trophic vs non‐trophic pathways of apparent competition may change under contrasting predation scenarios.     

Interspecific synchrony of seed rain shapes rodent‐mediated indirect seed–seed interactions of sympatric tree species in a subtropical forest

Animal‐mediated indirect interactions play a significant role in maintaining the biodiversity of plant communities. Less known is whether interspecific synchrony of seed rain can alter the indirect interactions of sympatric tree species. We assessed the seed dispersal success by tracking the fates of 21 600 tagged seeds from six paired sympatric tree species in both monospecific and mixed plots across 4 successive years in a subtropical forest. We found that apparent mutualism was associated with the interspecific synchrony of seed rain both seasonally and yearly, whereas apparent competition or apparent predation was associated with interspecific asynchrony of seed rain either seasonally or yearly. We did not find consistent associations of indirect interactions with seed traits. Our study suggests that the interspecific synchrony of seed rain plays a key role in the formation of animal‐mediated indirect interactions, which, in turn, may alter the seasonal or yearly seed rain schedules of sympatric tree species.     

Apparent competition: an impact of exotic shrub invasion on tree regeneration

Invasion of habitats by exotic shrubs is often associated with a decrease in the abundance of native species, particularly trees. This is typically interpreted as evidence for direct resource competition between the invader and native species. However, this may also reflect indirect impacts of the exotic shrubs through harboring high densities of seed predators––known as apparent competition. Here I present data from separate seed predation experiments conducted with two shrub species exotic to North America; Rosa multiflora, an invader of abandoned agricultural land, and Lonicera maackii, an invader of disturbed or secondary forest habitats. Both experiments showed significantly greater risks of seed predation for tree seeds located under shrub canopies when compared to open microhabitats within the same site. These results indicate the potential importance of indirect impacts of exotic species invasions on native biota in addition to the direct impacts that are typically the focus of research.     

Coexistence of plant species in a biodiversity hotspot is stabilized by competition but not by seed predation

Understanding the mechanisms of species coexistence is a key task for ecology. Recent theory predicts that both competition and predation (which causes apparent competition among prey) can either promote or limit species coexistence. Both mechanisms cause negative interactions between individuals, and each mechanism promotes stable coexistence if it causes negative interactions to be stronger between conspecifics than between heterospecifics. However, the relative importance of competition and predation for coexistence in natural communities is poorly known. Here, we study how competition and apparent competition via pre‐dispersal seed predators affect the long‐term fecundity of Protea shrubs in the fire‐prone Fynbos biome (South Africa). These shrubs store all viable seeds produced since the last fire in fire‐proof cones. Competitive effects on cone number and pre‐dispersal seed predation reduce their fecundity and can thus limit recruitment after the next fire. In 27 communities comprising 49 990 shrubs of 22 Protea species, we measured cone number and per‐cone seed predation rate of 2154 and 1755 focal individuals, respectively. Neighbourhood analyses related these measures to individual‐based community maps. We found that conspecific neighbours had stronger competitive effects on cone number than heterospecific neighbours. In contrast, apparent competition via seed predators was comparable between conspecifics and heterospecifics. This indicates that competition stabilizes coexistence of Protea species, whereas pre‐dispersal seed predation does not. Larger neighbours had stronger competitive effects and neighbours with large seed crops exerted stronger apparent competition. For 97% of the focal plants, competition reduced fecundity more than apparent competition. Our results show that even in communities of closely related and ecologically similar species, intraspecific competition can be stronger than interspecific competition. On the other hand, apparent competition through seed predators need not have such a stabilizing effect. These findings illustrate the potential of ‘community demography’, the demographic study of multiple interacting species, for understanding plant coexistence.     

Land-use and edge effects unbalance seed dispersal and predation interactions under habitat fragmentation

The process of fragmentation can greatly influence plant–animal interactions. To assess the degree to which it affects the balance between two interactions of opposite sign, namely seed dispersal and post-dispersal seed predation, we selected 16 patches of chestnut forest in O Courel and El Bierzo, northwestern Spain. We assessed the effect of fragmentation over two different seed dispersal–predation systems using Helleborus foetidus and Ilex aquifolium as model species. In the first case, field experiments consisted of seed-offering trays with selective exclusion of rodents and ants in a two-way orthogonal design. In the second experiment, we placed experimental branches and trays on the floor to assess seed dispersal and predation. The interactions between several fragment traits and the relative contribution of rodents, ants and birds to seed removal were analyzed by means of generalized linear mixed models. Results show that for H. foetidus, differences in seed dispersal–predation were accounted for by patch shape, which affected mainly the dispersal phase. Major seed dispersal took place in patches with a smaller edge to core ratio and high plant cover (abandoned patches), whilst the latter also showed maximum seed predation. For I. aquifolium, fragmentation effects were significant only for seed predation, which was increased in abandoned patches. This shows that the effects of habitat fragmentation can emerge at different phases depending on specific traits of the interacting animals. It also highlights the importance of traditional land-use practices in species interactions.     

Giving-up densities of foraging gerbils: the effect of interspecific competition on patch use

We studied the effect of a dominant species, Gerbillus pyramidum (Egyptian sand gerbil), on the patch use of its subordinate competitor, G. andersoni allenbyi (Allenby's gerbil), to better understand interspecific competition between the two species. We used manipulated resource patches (seed trays) covered with cages with two adjustable species-specific gates (either opened or closed to the bigger-dominant species, but always opened to the subordinate one). We recorded species tracks around and on the seed trays and giving-up densities (GUDs) of seeds in the trays after each night of foraging. G. a. allenbyi depleted seed patches to a lower level whenever G. pyramidum was given the opportunity to forage on the seed trays (i.e., present on the grid). This result held regardless of whether G. pyramidum was actually present at a particular station. We suggest that competition from G. pyramidum occurs both directly by interference, in which G. a. allenbyi is forced to be active in the late part of the night, and indirectly by exploitation via resource depletion by G. pyramidum in the early part of the night. The results suggest that interspecific competition from G. pyramidum reduces seed availability and the richness of the environment for G. a. allenbyi enough to affect the marginal value of energy for G. a. allenbyi individuals and cause them to experience lower costs of predation and manifest lower GUDs.     

Geographical and within-population variation in the globeflower–globeflower fly interaction: the costs and benefits of rearing pollinator’s larvae

Interspecific interactions can vary within and among populations and geographical locations, and this variation can influence the nature of the interaction (e.g. mutualistic versus antagonistic) and its evolutionary stability. Globeflowers are exclusively pollinated by flies whose larvae feed only on their seeds. Here we document geographical variability in costs and benefits in globeflowers in sustaining their pollinating flies throughout the range of this arctic-alpine European plant over several years. A total of 1,710 flower heads from 38 populations were analysed for their carpel, egg and seed contents. Individual and population analyses control for the confounding influences of variation in both: (1) population traits, such as fly density and egg distribution among flower heads; and (2) individuals traits, such as carpel and egg numbers per flower head. Despite considerable variation in ecological conditions and pollinator densities across populations, large proportions (range 33–58%) of seeds are released after predation, with a benefit-to-cost ratio of 3, indicating that the mutualism is stable over the whole globeflower geographical range. The stability of the mutualistic interaction relies on density-dependent competition among larvae co-developing in a flower head. This competition is revealed by a sharp decrease in the number of seeds eaten per larva with increasing larval number, and is intensified by non-uniform egg distribution among globeflowers within a population. Carpel number is highly variable across globeflowers (range 10–69), and flies lay more eggs in large flowers. Most plants within a population contribute to the rearing of pollinators, but some pay more than others. Large globeflowers lose more seed to pollinator larvae, but also release more seed than smaller plants. The apparent alignment of interests between fly and plant (positive relationship between numbers of seeds released and destroyed) is shown to hide a conflict of interest found when flower size is controlled for.     

Geographic and within-population variation in the globeflower–globeflower fly interaction: the costs and benefits of rearing pollinators’ larvae

Interspecific interactions can vary within and among populations and geographic locations, and this variation can influence the nature of the interaction (e.g. mutualistic vs. antagonistic) and its evolutionary stability. Globeflowers are exclusively pollinated by flies, whose larvae feed only on their seeds. Here we document geographic variability in costs and benefits in globeflowers in sustaining their pollinating flies throughout the range of this arctic-alpine European plant over several years. A total of 1,710 flower heads from 38 populations were analysed for their carpel, egg and seed contents. Individual and population analyses control for the confounding influences of variation in both: (1) population traits, such as fly density and egg distribution among flower heads; and (2) individuals traits, such as carpel and egg numbers per flower head. Despite considerable variation in ecological conditions and pollinator densities across populations, large proportions (range 33–58%) of seeds were released after predation, with a benefit-to-cost ratio of 3, indicating that the mutualism is stable over the whole globeflower geographical range. The stability of the mutualistic interaction relies on density-dependent competition among larvae co-developing in a flower head. This competition is revealed by a sharp decrease in the number of seeds eaten per larva with increasing larval number, and is intensified by non-uniform egg distribution among globeflowers within a population. Carpel number is highly variable across globeflowers (range 10–69), and flies lay more eggs in large flowers. Most plants within a population contribute to the rearing of pollinators, but the costs are greater for some than for others. Large globeflowers lose more seed to pollinator larvae, but also release more seed than smaller plants. The apparent alignment of interests between fly and plants (positive relationship between numbers of seed released and destroyed) is shown to hide a conflict of interest found when flower size is controlled for.     

The qualitative approach in investigating the role of species interactions on stability of natural communities

Community models with competition and mutualism are qualitatively analyzed using the methodology of loop analysis combined with computer stochastic simulation. The concept of "moving equilibrium" in the growth rate of the species is discussed in 14 "tables of predictions", presented as analytical tools that can help to shed light on controversial ecological issues such as direct versus indirect interaction and positive feedback effects on stability. While the stochastic simulation shows that only little or no difference exists in probability of stability between models with competition and models with mutualism, the related tables of predictions show that the networks among links are able to activate indirect interactions, with both negative and positive effects, between any pair of species. This phenomenon makes it difficult to determine how much stability is related to the direct interactions.     

Influence of conspecific and heterospecific adults on riparian tree species establishment during encroachment of a humid palm savanna

Woody plant encroachment of savanna ecosystems has been related to altered disturbance regimes, mainly fire suppression and herbivore exclusion. In contrast, neighbourhood interactions among resident and colonising woody species have received little attention, despite their likely influence on the pattern and rate of tree establishment. We examined how resident palm trees (Butia yatay) and established adults of two riparian forest tree species (Allophylus edulis and Sebastiania commersoniana) influenced seed arrival and seedling performance of the latter two species in a humid savanna of east-central Argentina. Seed traps and seedlings of both riparian species were placed in herbaceous openings, and beneath palm, conspecific and heterospecific adult trees in two unburned savanna patches, and were monitored for 2 years. Only seeds of the bird-dispersed Allophylus arrived in palm microsites, yet survival of Allophylus seedlings near adult palms was limited by animal damage through trampling and burrowing, a non-trophic mechanism of apparent competition. Seeds of both riparian species dispersed into conspecific microsites, although adult trees selectively reduced growth of conspecific seedlings, a pattern consistent with the “escape hypothesis”. Further, survival of Sebastiania increased in the moister Allophylus microsites, suggesting a one-way facilitative interaction between woody colonisers. Our results indicate that dispersal facilitation by resident savanna trees may be critical to riparian species invasion after fire suppression. Distance-dependent effects of conspecific and heterospecific adult trees could contribute to shape the subsequent dynamics of woody seedling establishment. Overall, we show that indirect interactions can play a prominent role in savanna encroachment by non-resident woody species.     

The foraging behavior of granivorous rodents and short-term apparent competition among seeds

The foraging behavior of a predator species is thought to bethe cause of short-term apparent competition among those preyspecies that share the predator. Short-term apparent competitionis the negative indirect effect that one prey species has onanother prey species via its effects on predator foraging behavior.In theory, the density-dependent foraging behavior of granivorousrodents and their preference for certain seeds are capable of inducing short-term apparent competition among seed species.In this study, I examined the foraging behavior of two heteromyidrodent species (family Heteromyidae), Merriam's kangaroo rats(Dipodomys merriami) and little pocket mice (Perognathus longimembris).In one experiment I tested the preferences of both rodent speciesfor the seeds of eight plant species. Both rodent species exhibiteddistinct but variable preferences for some seeds and avoidanceof others. However, the differences in preference appearedto have only an occasional effect on the strength of the short-term apparent competition detected in a field experiment. In anotherexperiment, I found that captive individuals of both rodentspecies had approximately equal foraging effort (i.e., timespent foraging) in patches that contained a highly preferredseed type (Oryzopsis hymenoides) regardless of seed density and the presence of a less preferred seed type (Astragalus cicer)in the patches. The rodents also harvested a large proportionof O. hymenoides seeds regardless of initial seed density;this precluded a negative indirect effect of A. cicer on O.hymenoides. But there was a negative indirect effect of O.hymenoides on A. cicer caused by rodents having a lower foragingeffort in patches that only contained A. cicer seeds than inpatches that contained A. cicer and O. hymenoides seeds. Theindirect interaction between O. hymenoides and A. cicer thusrepresented a case of short-term apparent competition thatwas non-reciprocal. Most importantly, it was caused by theforaging behavior of the rodents.     

How context dependent are species interactions?

The net effects of interspecific species interactions on individuals and populations vary in both sign (?, 0, +) and magnitude (strong to weak). Interaction outcomes are context‐dependent when the sign and/or magnitude change as a function of the biotic or abiotic context. While context dependency appears to be common, its distribution in nature is poorly described. Here, we used meta‐analysis to quantify variation in species interaction outcomes (competition, mutualism, or predation) for 247 published articles. Contrary to our expectations, variation in the magnitude of effect sizes did not differ among species interactions, and while mutualism was most likely to change sign across contexts (and predation least likely), mutualism did not strongly differ from competition. Both the magnitude and sign of species interactions varied the most along spatial and abiotic gradients, and least as a function of the presence/absence of a third species. However, the degree of context dependency across these context types was not consistent among mutualism, competition and predation studies. Surprisingly, study location and ecosystem type varied in the degree of context dependency, with laboratory studies showing the highest variation in outcomes. We urge that studying context dependency per se, rather than focusing only on mean outcomes, can provide a general method for describing patterns of variation in nature.     

Prey temporarily escape from predation in the presence of a second prey species

1. Indirect interactions between populations of different prey species mediated by a shared predator population are known to affect prey dynamics. 2. Depending on the temporal and spatial scale, these indirect interactions may result in positive (apparent mutualism), neutral or negative effects (apparent competition) of the prey on each other's densities. Although there is ample evidence for the latter, evidence for apparent mutualism is scarce. 3. The effectiveness of using one species of predator for biological control of more than one pest species depends on the occurrence of such positive or negative effects. 4. We used an experimental system consisting of the two prey species Western flower thrips (Franklineilla occidentalis Pergande) and greenhouse whitefly (Trialeurodes vaporariorum Westwood) and a shared predator, the phytoseiid mite Amblyseius swirskii Athias‐Henriot. We released all three species on the same plant and studied their dynamics and distribution along rows of plants. 5. We expected that the more mobile prey species (thrips) would escape temporarily in the presence of the other prey species (whitefly) by dispersing from plants with the predator. The predator was expected to disperse slower in the presence of two prey species because of the higher availability of food. 6. Evidence was found for slower dispersal of predators and short‐term escape of thrips from predation when whiteflies were present, thus confirming the occurrence of short‐term apparent mutualism. 7. The apparent mutualism resulted in a cascade to the first trophic level: a higher proportion of fruits was damaged by thrips in the presence of whiteflies. 8. We conclude that apparent mutualism can be an important phenomenon in population dynamics, and can significantly affect biological control of pest species that share a natural enemy.     

Water and nitrogen addition differentially impact plant competition in a native rough fescue grassland

We examined how water and nitrogen addition and water–nitrogen interactions affect root and shoot competition intensity and competition–productivity relationships in a native rough fescue grassland in central Alberta, Canada. Water and nitrogen were added in a factorial design to plots and root exclusion tubes and netting were used to isolate root and shoot competition on two focal species (Artemisia frigida and Chenopodium leptophyllum). Both water and nitrogen were limiting to plant growth, and focal plant survival rates increased with nitrogen but not water addition. Relative allocation to root biomass increased with water addition. Competition was almost entirely belowground, with focal plants larger when released from root but not shoot competition. There were no significant relationships between productivity and root, shoot, or total competition intensity, likely because in this system shoot biomass was too low to cause strong shoot competition and root biomass was above the levels at which root competition saturates. Water addition had few effects on the intensity of root competition suggesting that root competition intensity is invariant along soil moisture gradients. Contrary to general expectation, the strength of root competition increased with nitrogen addition demonstrating that the relationship between root competition intensity and nitrogen is more complex than a simple monotonic decline as nitrogen increases. Finally, there were few interactions between nitrogen and water affecting competition. Together these results indicate that the mechanisms of competition for water and nitrogen likely differ.     

Are introduced rats (<Emphasis Type="Italic">Rattus rattus</Emphasis>) both seed predators and dispersers in Hawaii?

Invasive rodents are among the most ubiquitous and problematic species introduced to islands; more than 80% of the world’s island groups have been invaded. Introduced rats (black rat, Rattus rattus; Norway rat, R. norvegicus; Pacific rat, R. exulans) are well known as seed predators but are often overlooked as potential seed dispersers despite their common habit of transporting fruits and seeds prior to consumption. The relative likelihood of seed predation and dispersal by the black rat, which is the most common rat in Hawaiian forest, was tested with field and laboratory experiments. In the field, fruits of eight native and four non-native common woody plant species were arranged individually on the forest floor in four treatments that excluded vertebrates of different sizes. Eleven species had a portion (3–100%) of their fruits removed from vertebrate-accessible treatments, and automated cameras photographed only black rats removing fruit. In the laboratory, black rats were offered fruits of all 12 species to assess consumption and seed fate. Seeds of two species (non-native Clidemia hirta and native Kadua affinis) passed intact through the digestive tracts of rats. Most of the remaining larger-seeded species had their seeds chewed and destroyed, but for several of these, some partly damaged or undamaged seeds survived rat exposure. The combined field and laboratory findings indicate that many interactions between black rats and seeds of native and non-native plants may result in dispersal. Rats are likely to be affecting plant communities through both seed predation and dispersal.     

The role of indirect interactions in structuring tropical insect communities

Apparent competition is a form of indirect interaction among species that can potentially structure biological communities. In insect communities, parasitoid-mediated apparent competition has been proposed as a particularly important structuring force. We argue that short-term apparent competition may be less important in structuring insect communities in tropical regions, compared with temperate regions. This prediction arises because, compared with temperate insects, tropical insects that share natural enemies are more likely to be isolated in both space and time.     

Introduced galliforms as seed predators and dispersers in Hawaiian forests

In altered communities, novel species’ interactions may critically impact ecosystem functioning. One key ecosystem process, seed dispersal, often requires mutualistic interactions between frugivores and fruiting plants, and functional traits, such as seed width, may affect interaction outcomes. Forests of the Hawaiian Islands have experienced high species turnover, and introduced galliforms, the largest of the extant avian frugivores, consume fruit from both native and non-native plants. We investigated the roles of two galliform species as seed dispersers and seed predators in Hawaiian forests. Using captive Kalij Pheasants (Lophura leucomelanos) and Erckel’s Francolins (Pternistis erckelii), we measured the probability of seed survival during gut passage and seed germination following gut passage. We also examined which seeds are being dispersed in forests on the islands of O’ahu and Hawai’i. We found that galliforms are major seed predators for both native and non-native plants, with less than 5% of seeds surviving gut passage for all plants tested and in both bird species. Gut passage by Kalij Pheasants significantly reduced the probability of seeds germinating, especially for the native plants. Further, larger-seeded plants were both less likely to survive gut passage and to germinate. In the wild, galliforms dispersed native and non-native seeds at similar rates. Overall, our results suggest the introduced galliforms are a double-edged sword in conservation efforts; they may help reduce the spread of non-native plants, but they also destroy the seeds of some native plants. Broadly, we show mutualism breakdown may occur following high species turnover, and that functional traits can be useful for predicting outcomes from novel species’ interactions.

     

Comparing methods of weed seed exposure to predators

Several methods of seed exposure are used in seed predation studies, but how these methods influence the results remains poorly studied. In this article, two commonly used methods of seed exposure – seed cards and plasticine trays – were compared in the field and in the laboratory using three species of weed seeds. In the field, cards or trays with seeds were exposed either with or without cages to keep vertebrates out and either with or without impermeable roofs to provide protection from the weather. The overall seed retrieval from the control stands varied significantly between the methods of seed exposure, roof treatment and the species of seeds, and the scatter in the seed retrieval increased or decreased monotonically with the temperature or precipitation for some species of seeds. This indicates that the controls were more or less relevant depending on the weather conditions and species. The seed removal from cards varied between the species of seeds. The effect of exclosure cages indicated that invertebrates were the dominant seed predators of Capsella bursa‐pastoris, while in Poa annua and Stellaria media both vertebrates and invertebrates were important. Higher seed removal from plasticine trays compared to seed cards was found for all three species of seeds, and placing roofs over the seeds affected seed removal in C. bursa‐pastoris and P. annua. In the laboratory, seed consumption varied with the method of exposure in 10 out of 12 combinations of seed species and predator (two species of carabids and two species of isopods). The overall tendency was the opposite of the field observations: seed consumption was higher for seeds on filter paper and cards compared to seeds on tin trays. We conclude that seed cards are more convenient for short term studies in the field, while tin trays are useful in laboratory multi‐choice experiments. To measure the realistic consumption of invertebrate predators in the laboratory, filter paper seems to be the best option as it does not present an obstacle to predators eating the seed. Using roofs introduced further bias regarding the estimates of seed removal in the field and thus should be avoided.     

Biological control of thrips and whiteflies by a shared predator: Two pests are better than one

We studied the capacity of one species of predator to control two major pests of greenhouse crops, Western flower thrips (Frankliniella occidentalis (Pergande)) and the greenhouse whitefly (Trialeurodes vaporariorum (Westwood)). In such a one-predator–two-prey system, indirect interactions can occur between the two pest species, such as apparent competition and apparent mutualism. Whereas apparent competition is desired because it brings pest levels down, apparent mutualism is not, because it does the opposite. Because apparent competition and apparent mutualism occurs at different time scales, it is important to investigate the effects of a shared natural enemy on biological control on a time scale relevant for crop growth. We evaluated the control efficacy of the predatory mites Amblyseius swirskii (Athias-Henriot) and Euseius ovalis (Evans) in cucumber crops in greenhouse compartments with only thrips, only whiteflies or both herbivorous insects together. Each of the two predators controlled thrips, but A. swirskii reduced thrips densities the most. There was no effect of the presence of whiteflies on thrips densities. Whitefly control by each of the two predators in absence of thrips was not sufficient, yet better with E. ovalis. However, whitefly densities in presence of thrips were reduced dramatically, especially by A. swirskii. The densities of predators were up to 15 times higher in presence of both pests than in the single-pest treatments. Laboratory experiments with A. swirskii suggest that this is due to a higher juvenile survival and developmental rate on a mixed diet. Hence, better control may be achieved not only because of apparent competition, but also through a positive effect of mixed diets on predator population growth. This latter phenomenon deserves more attention in experimental and theoretical work on biological control and apparent competition.     

A non‐pollinating moth inflicts higher seed predation than two co‐pollinators in an obligate pollination mutualism

1. Mutualisms are relationships of mutual exploitation, in which interacting species receive a net benefit from their association. In obligate pollination mutualisms (OPMs), female pollinators move pollen between the flowers of a single plant species and oviposit eggs within the female flowers that they visit. 2. Competition between co‐occurring pollinator species is predicted to increase pollinator virulence, i.e. laying more eggs or consuming more seeds per fruit. Plants involved in OPMs frequently host various non‐pollinating seed parasites and parasitoids that may influence the outcome of the mutualism. Quantifying the prevalence of parasites and parasitoids and competition between pollinators is important for understanding the factors that influence OPM evolutionary stability. 3. This study investigated the pollination mutualism occurring between the leaf flower plant, Breynia oblongifolia, and its co‐pollinating Epicephala moths. A third moth, Herpystis, also occurs in B. oblongifolia fruits as a non‐pollinating seed parasite. 4. Breynia oblongifolia fruits were collected to quantify seed predation and compare seed predation costs between the three moth species. Results showed that the larvae of the two pollinator species consume similar numbers of seeds, and that adults deposit similar numbers of eggs per flower. As such, no evidence of increases in virulent behaviours was detected as a result of competition between co‐pollinators. 5. By contrast, the seed parasite Herpystis consumed more seeds than either pollinator species, and fruit crops with a high proportion of Herpystis had significantly lower net seed production. 6. This work adds to the growing understanding of the ecology and dynamics of plant–pollinator mutualisms.