Trait-mediated Indirect Effects Research Articles

Coupled Oscillators in an Agroecosystem: Integrating Direct and Indirect Effects.

AbstractAgricultural pests are increasingly appreciated as subjects of ecology. One particular case, a pest in coffee production, is analyzed here using the conceptual framework of complex systems, increasingly acknowledged as having an obvious home in the field of ecology, notorious for its complex structures. The particular case analyzed here arguably falls under the control of the complexity of the ecological system rather than of a simple magic bullet of population regulation. The system, which has been under study in southern Mexico for the past quarter century, is analyzed through the lens of neutral oscillations of the classical nondissipative Lotka-Volterra system. Based on three consumer/resource pairs (populations of [1] an ant, [2] a scale insect, [3] a beetle predator of the scale insect, [4] a fungal pathogen of the scale insect, and [5] a fly parasitoid of the ant), this five-dimensional system is well known qualitatively. Coupling all agents through both direct effects and trait-mediated indirect effects, the behavior of the neutral oscillation form of the system reveals a complex set of behaviors, including harmonized invariant sets, chaos, and/or quasiperiodicity. Such behaviors are well-known subjects in the science of complex systems and, it is argued, are ultimately sufficient to effect a degree of regulation on the pest, independent of explicit density-dependent feedback. Control of the system is thus seen as arguably actuated through its complexity, independent of any classic dissipative force.

Predators affect a plant virus through density and trait-mediated indirect effects on vectors

Biological control programs frequently rely on insect predators to control pests that vector plant pathogens in agroecosystems. Predators affect vectors by eating them (consumptive effects) and by inducing antipredator behaviors (non-consumptive effects), and these interactions may affect transmission of vector-borne pathogens. However, it has proven difficult to experimentally tease apart the effects of predators on vector fitness and behavior as they are often correlated. We addressed this problem by assessing how both aphids and an aphid-borne pathogen were affected by variable predation risk. Specifically, we experimentally manipulated ladybeetle predators' mouthparts to isolate consumptive, and non-consumptive, effects of predators on aphid fitness, movement, and virus transmission. We show that although lethal predators decreased aphid vector abundance, they increased pathogen transmission by increasing aphid movement among hosts. Moreover, aphids responded to risk of predation by moving to younger plant tissue that was more susceptible to the pathogen. Aphids also responded to predator risk through compensatory reproduction, which offset direct consumptive effects. Our results support predictions of disease models showing alterations of vector movement due to predators can have greater effects on transmission of pathogens than vector consumption, which should be considered when examining natural enemies' role in pathogen dynamics. Broadly, our study shows isolating direct and indirect predation effects can reveal novel pathways by which predators affect vector-borne pathogens.

A skewed literature: Few studies evaluate the contribution of predation-risk effects to natural field patterns.

A narrative in ecology is that prey modify traits to reduce predation risk, and the trait modification has costs large enough to cause ensuing demographic, trophic and ecosystem consequences, with implications for conservation, management and agriculture. But ecology has a long history of emphasising that quantifying the importance of an ecological process ultimately requires evidence linking a process to unmanipulated field patterns. We suspected that such process‐linked‐to‐pattern (PLP) studies were poorly represented in the predation risk literature, which conflicts with the confidence often given to the importance of risk effects. We reviewed 29 years of the ecological literature which revealed that there are well over 4000 articles on risk effects. Of those, 349 studies examined risk effects on prey fitness measures or abundance (i.e., non‐consumptive effects) of which only 26 were PLP studies, while 275 studies examined effects on other interacting species (i.e., trait‐mediated indirect effects) of which only 35 were PLP studies. PLP studies were narrowly focused taxonomically and included only three that examined unmanipulated patterns of prey abundance. Before concluding a widespread and influential role of predation‐risk effects, more attention must be given to linking the process of risk effects to unmanipulated patterns observed across diverse ecosystems.

A sit-and-wait predator, but not an active-pursuit predator, alters pollinator-mediated selection on floral traits.

Indirect species interactions are ubiquitous in nature, often outnumbering direct species interactions. Yet despite evidence that indirect interactions have strong ecological effects, relatively little is known about whether they can shape adaptive evolution by altering the strength and/or direction of natural selection. We tested whether indirect interactions affect the strength and direction of pollinator-mediated selection on floral traits of the bumble-bee pollinated wildflower Lobelia siphilitica. We estimated the indirect effects of two pollinator predators with contrasting hunting modes: dragonflies (Aeshnidae and Corduliidae) and ambush bugs (Phymata americana, Reduviidae). Because dragonflies are active pursuit predators, we hypothesized that they would strengthen pollinator-mediated selection by weakening plant-pollinator interactions (i.e., a density-mediated indirect effect). In contrast, because ambush bugs are sit-and-wait predators, we hypothesized that they would weaken or reverse the direction of pollinator-mediated selection by altering pollinator foraging behavior (i.e., a trait-mediated indirect effect). Specifically, if ambush bugs hunt from plants with traits that attract pollinators (i.e., prey), then pollinators will spend less time visiting those plants, weakening or reversing the direction of selection on attractive floral traits. We did not find evidence that high dragonfly abundance strengthened selection on floral traits via a density-mediated indirect effect: neither pollen limitation (a proxy for the strength of plant-pollinator interactions) nor directional selection on floral traits of L. siphilitica differed significantly between high- and low-dragonfly abundance treatments. In contrast, we did find evidence that ambush bug presence affected selection on floral traits via a trait-mediated indirect effect: ambush bugs hunted from L. siphilitica plants with larger daily floral displays, reversing the direction of pollinator-mediated selection on daily display size. These results suggest that indirect species interactions have the potential to shape adaptive evolution by altering natural selection.

Environmental stress gradients regulate the relative importance of predator density- and trait-mediated indirect effects in oyster reef communities.

Predators affect community structure by influencing prey density and traits, but the importance of these effects often is difficult to predict. We measured the strength of blue crab predator effects on mud crab prey consumption of juvenile oysters across a flow gradient that inflicts both physical and sensory stress to determine how the relative importance of top predator density‐mediated indirect effects (DMIEs) and trait‐mediated indirect effects (TMIEs) change within systems. Overall, TMIEs dominated in relatively benign flow conditions where blue crab predator cues increased oyster survivorship by reducing mud crab–oyster consumption. Blue crab DMIEs became more important in high sensory stress conditions, which impaired mud crab perception of blue crab chemical cues. At high physical stress, the environment benefitted oyster survival by physically constraining mud crabs. Thus, factors that structure communities may be predicted based on an understanding of how physical and sensory performances change across environmental stress gradients.

A framework and standardized terminology to facilitate the study of predation-risk effects.

The very presence of predators can strongly influence flexible prey traits such as behavior, morphology, life history, and physiology. In a rapidly growing body of literature representing diverse ecological systems, these trait (or "fear") responses have been shown to influence prey fitness components and density, and to have indirect effects on other species. However, this broad and exciting literature is burdened with inconsistent terminology that is likely hindering the development of inclusive frameworks and general advances in ecology. We examine the diverse terminology used in the literature, and discuss pros and cons of the many terms used. Common problems include the same term being used for different processes, and many different terms being used for the same process. To mitigate terminological barriers, we developed a conceptual framework that explicitly distinguishes the multiple predation-risk effects studied. These multiple effects, along with suggested standardized terminology, are risk-induced trait responses (i.e., effects on prey traits), interaction modifications (i.e., effects on prey-other-species interactions), nonconsumptive effects (i.e., effects on the fitness and density of the prey), and trait-mediated indirect effects (i.e., the effects on the fitness and density of other species). We apply the framework to three well studied systems to highlight how it can illuminate commonalities and differences among study systems. By clarifying and elucidating conceptually similar processes, the framework and standardized terminology can facilitate communication of insights and methodologies across systems and foster cross-disciplinary perspectives.

Ecological complexity and contingency: Ants and lizards affect biological control of the coffee leaf miner in Puerto Rico

Complexity and contingency frame much of current thinking in population and community ecology. The coffee pest, Leucoptera coffeella, is particularly problematical in Puerto Rico, but is usually held under control in Mexico. A variety of arboreal ants are effective predators in Mexico, but are limited in an indirect fashion by the common aggressive arboreal ant, Azteca sericeasur. In Puerto Rico this species does not occur, suggesting that the small arboreal ants might be more effective predators there than in Mexico. However, the contingency of large population densities of Anoline lizards is well-known as a major biological control force for the leaf miner. Ants, especially the non-native Wasmannia auropunctata, have a negative effect on the lizards. Surveying ants and coffee leaf miners in 25 coffee farms in Puerto Rico, we investigate the effect of ants, in particular W. auropunctata, on the coffee leaf miner, and find that this ant species has a positive relationship with the miner. In a more detailed spatial study of two farms, surveys of anoline lizards show no significant negative relationship between the lizards and W. auropunctata on a per plant basis. However, we found a significantly lower abundance of lizards on patches dominated by this ant, suggesting that W. auropunctata indirectly protects the coffee leaf miner against this potential lizard predator. Thus, the structural complexity of a trait-mediated indirect effect occurs both in Mexico and Puerto Rico and potentially limits the effectiveness of biological control elements, but the contingencies are distinct in the two sites.

Introduced marine ecosystem engineer indirectly affects parasitism in native mussel hosts

The alteration of habitat structure by introduced ecosystem engineers imposes direct impacts on native biota but can also exert trait-mediated indirect effects. In this study, we show that the habitat structure provided by invasive Pacific oysters (Crassostrea gigas) can also indirectly affect parasitism in native blue mussels (Mytilus edulis). We conducted a 3-month field experiment, in which uninfected mussels were positioned at the bottom and top of two intertidal oyster reefs in the Wadden Sea. On one reef, we detected a significantly higher prevalence of parasitic copepods (Mytilicola spp.) in mussels positioned on top of oysters than in mussels at the bottom, but no difference in infection intensity. For trematodes (Renicola roscovita), a different pattern was observed, with higher prevalence (one reef) and significantly higher infection intensities (both reefs) in mussels positioned at the bottom of the oyster reef. We suggest that the contrasting pattern results from differences in parasite life cycles. Mytilicola spp. larvae spend 2–3 weeks in the water column before infecting their hosts and, therefore, mussels positioned at the top are exposed to higher numbers of planktonic larvae than mussels at the bottom. In contrast, infective trematode larvae spend less than 12 h in the water column and primarily infect mussels during low tide, which may explain higher prevalence and intensity of R. roscovita in mussels near the bottom of the oyster reef. Our results demonstrate that indirect effects leading to alterations of parasite-host interactions may be a more common but hitherto rarely considered impact of biological invasions.

The legacy of predators: persistence of trait-mediated indirect effects in an intertidal food chain

Trait mediated indirect effects are integral to many multiple-level predator-prey interactions. They arise routinely when, in response to predators, prey decrease their foraging on a basal resource, often due to fear. Less examined is a common assumption about trait-mediated indirect effects: that reductions in prey foraging track the instantaneous presence or absence of predators. In particular, although it is recognized that behavioral, physiological, and morphological changes in prey can persist after a predator departs, whether those changes ultimately affect trophic levels below remains an open question. Here, we tested whether legacy effects of predators lead to trait-mediated indirect effects that persist beyond when predators are present, using a model intertidal system that included a crab predator (Cancer productus), a carnivorous snail prey (Nucella ostrina), and a basal suspension feeder (the mussel, Mytilus californianus). We found that previous conditioning of snails to predator cue instilled a sustained behavioral fear response that depressed foraging by snails for at least two weeks beyond when the predator cue was present. Indeed, snails conditioned previously to predator cue consumed similar numbers of mussels as snails currently subjected to cue. Because such durations are long enough to allow new mobile predators to enter prey detection domains previously vacated by other predators, these findings suggest that neglecting the time course of persistence of trait-mediated indirect effects could appreciably underestimate their strengths. Our study supports the notion that prey use prior experience in addition to their body state to inform their anti-predatory decision making, which results in a persistent trophic cascade.

Parasitism in ecosystem engineer species: A key factor controlling marine ecosystem functioning.

Although parasites represent a substantial part of marine communities' biomass and diversity, their influence on ecosystem functioning, especially via the modification of host behaviour, remains largely unknown. Here, we explored the effects of the bopyrid ectoparasite Gyge branchialis on the engineering activities of the thalassinid crustacean Upogebia pusilla and the cascading effects on intertidal ecosystem processes (e.g. sediment bioturbation) and functions (e.g. nutrient regeneration). Laboratory experiments revealed that the overall activity level of parasitized mud shrimp is reduced by a factor 3.3 due to a decrease in time allocated to burrowing and ventilating activities (by factors 1.9 and 2.9, respectively). Decrease in activity level led to strong reductions of bioturbation rates and biogeochemical fluxes at the sediment-water interface. Given the world-wide distribution of mud shrimp and their key role in biogeochemical processes, parasite-mediated alteration of their engineering behaviour has undoubtedly broad ecological impacts on marine coastal systems functioning. Our results illustrate further the need to consider host-parasite interactions (including trait-mediated indirect effects) when assessing the contribution of species to ecosystem properties, functions and services.

Modeling the effects of trait-mediated dispersal on coexistence of mutualists.

Even though mutualistic interactions are ubiquitous in nature, we are still far from making good predictions about the fate of mutualistic communities under threats such as habitat fragmentation and climate change. Fragmentation often causes declines in abundance of a species due to increased susceptibility to edge effects between remnant habitat patches and lower quality "matrix" surrounding these focal patches. It has been argued that ecological communities are replete with trait-mediated indirect effects, and that these effects may sometimes contribute more to the dynamics of a population than direct density-mediated effects, e.g., lowering an organism's fitness through competitive interactions. Although some studies have focused on trait-mediated behavior such as trait-mediated dispersal, in which an organism changes its dispersal patterns due to the presence of another species, they have been mostly limited to predator-prey systems-little is known regarding their effect on other interaction systems such as mutualism. Here, we explore consequences of fragmentation and trait-mediated dispersal on coexistence of a system of two mutualists by employing a model built upon the reaction diffusion framework. To distinguish between trait-mediated dispersal and density-mediated effects, we isolate effects of trait-mediated dispersal on the mutualistic system by excluding any direct density-mediated effects in the model. Our results demonstrate that fragmentation and trait-mediated dispersal can have important impacts on coexistence of mutualists. Specifically, one species can be better able to invade and persist than the other and be crucial to the success of the other species in the patch. Matrix quality degradation can also bring about a complete reversal of the role of which species is supporting the other's persistence in the patch, even as the patch size remains constant. As most mutualistic relationships are identified based on density-mediated effects, such an effect may be easily overlooked.

Parasite-induced vulnerability to predation in larval anurans.

Within communities, pathogens and parasites have the potential to indirectly influence predator-prey interactions. For instance, prey that exhibit pathology or altered traits (e.g. behavioral shifts) following infection could be more prone to predation, which is known as parasite-induced vulnerability to predation (PIVP). PIVP has been frequently documented for pathogens with trophic transmission, because predators are often critical in the pathogen's life cycle. However, for pathogens without trophic transmission, PIVP can lead to a healthy herds effect, thereby reducing transmission in the system. In this study, we explored whether the pathogen ranavirus (family Iridoviridae) enhances vulnerability of 4 species of larval amphibians (spring peepers Pseudacris crucifer, gray treefrogs Hyla versicolor, American toads Anaxyrus americanus, and northern leopard frogs Lithobates pipiens) to 2 common tadpole predators (larval green darners Anax junius [hereinafter Anax] and adult water bugs Belostoma flumineum [hereinafter Belostoma]). For each anuran species, we conducted short-term microcosm experiments to assess predation rates on individuals that were or were not exposed to virus. For 3 of the 4 species, we found that exposure to ranavirus decreased survival rates with Anax between 2- and 9-fold. However, we did not see the same trend with Belostoma, which indicates that predator identity is important in this interaction. More specifically, the higher efficiency of Anax in capturing and consuming prey, relative to Belostoma, may allow Anax to capitalize on trait changes induced by virus exposure and enhance the PIVP effect. Our results indicate that trait-mediated indirect effects could play a role in creating healthy herds in amphibian communities.

Indirect effects in a planktonic disease system

Indirect effects, both density- and trait-mediated, have been known to act in tandem with direct effects in the interactions of numerous species. They have been shown to affect populations embedded in competitive and mutualistic networks alike. In this work, we introduce a four-dimensional system of ordinary differential equations and investigate the interplay between direct density-effects and density- and trait-mediated indirect effects that take place in a yeast parasite–zooplankton host–incompetent competitor system embedded in a food web which also includes resources and predators. Among our main findings is the demonstration that indirect effects cause qualitative and quantitative changes almost indistinguishable from direct effects and the corroboration through our analysis of the fact that the effects of direct and indirect mechanisms cannot be disentangled. Our results underpin the conclusions of past studies calling for comprehensive models that incorporate both direct and indirect effects to better describe field data.

Trait-mediated indirect effects in a natural tidepool system

We demonstrate an apparent trait-mediated indirect interaction (TMII) of predators on primary producers in a natural community by altering prey behavior over short and long time scales. Small predatory sea stars (Leptasterias spp.) caused herbivorous snails (Tegula funebralis) added to rocky intertidal tidepools to quickly flee into refuge microhabitats outside tidepools within days, and this was associated with a 58% increase in microalgal growth after 2 weeks. Similarly, removing sea stars caused snails to increase use of tidepools for 1–10 months. After adding sea stars to tidepools, snails quickly fled and then consistently increased use of refuges outside tidepools for 10 months. This was associated with average increases of 59% for microalgal growth over 1 month and 254% for macroalgal growth over 8 months inside tidepools. In 63 unmanipulated tidepools, densities of sea stars and snails were negatively correlated. High densities of snails were associated with unpalatable algal species and bare rock, while high densities of sea stars were associated with palatable algal species, suggesting that this apparent TMII may have community-level impacts. Though multiple lines of evidence suggest TMIIs were likely operating in this system, it was not possible to experimentally partition the relative contributions of TMIIs and density-mediated indirect interactions (DMIIs), so further caging experiments are necessary to distinguish their relative strengths. Overall, we suggest that predators can benefit primary producers by changing prey behavior even when predators and prey are unrestrained by cages or mesocosms, embedded in complex communities, and observed over multiple time scales.

Bottom-up trait-mediated indirect effects decrease pathogen transmission in a tritrophic system.

A plant's induction of secondary defenses helps to decrease herbivore damage by changing resource quality. While these chemical or physical defenses may directly decrease herbivory, they can also have indirect consequences. In a tritrophic system consisting of a plant, an insect herbivore, and an insect pathogen, plant based trait-mediated indirect effects (TMIEs) can alter host-pathogen interactions and, thereby, indirectly affect disease transmission. In a series of field experiments, individual soybean plants (Glycine max) were sprayed with either a jasmonic acid (JA) solution to trigger induction of plant defenses or a similar control compound. Fall armyworm (Spodoptera frugiperda) larvae along with varying amounts of a lethal baculovirus were placed on the plants to measure transmission. Induction of plant defenses decreased viral transmission due to increased population heterogeneity arising from changes in individual susceptibility. The change in susceptibility via TMIEs was driven by a decrease in feeding rates and an increase viral dose needed to infect larvae. While the induction against herbivore attack may decrease herbivory, it can also decrease the efficacy of the herbivore's pathogen potentially to the plant's detriment. While TMIEs have been well-recognized for being driven by top-down forces, bottom-up interactions can dictate community dynamics and, here, epizootic severity.

Contrasting indirect effects of an ant host on prey–predator interactions of symbiotic arthropods

Indirect interactions occur when a species affects another species by altering the density (density-mediated interactions) or influencing traits (trait-mediated interactions) of a third species. We studied variation in these two types of indirect interactions in a network of red wood ants and symbiotic arthropods living in their nests. We tested whether the ant workers indirectly affected survival of a symbiotic prey species (Cyphoderus albinus) by changing the density and/or traits of three symbiotic predators, i.e., Mastigusa arietina, Thyreosthenius biovatus and Stenus aterrimus, provoking, respectively, low, medium and high ant aggression. An ant nest is highly heterogeneous in ant worker density and the number of aggressive interactions towards symbionts increases with worker density. We, therefore, hypothesized that varying ant density could indirectly impact prey-predator interactions of the associated symbiont community. Ants caused trait-mediated indirect effects in all three prey-predator interactions, by affecting the prey capture rate of the symbiotic predators at different worker densities. Prey capture rate of the highly and moderately aggressed spider predators M. arietina and T. biovatus decreased with ant density, whereas the prey capture rate of the weakly aggressed beetle predator S. aterrimus increased. Ants also induced density-mediated indirect interactions as high worker densities decreased the survival rate of the two predatory spider species. These results demonstrate for the first time that a host can indirectly mediate the trophic interactions between associated symbionts. In addition, we show that a single host can induce opposing indirect effects depending on its degree of aggression towards the symbionts.

Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction.

Species often interact indirectly with each other via their traits. There is increasing appreciation of trait‐mediated indirect effects linking multiple interactions. Flowers interact with both pollinators and floral herbivores, and the flower‐pollinator interaction may be modified by indirect effects of floral herbivores (i.e., florivores) on flower traits such as flower size attracting pollinators. To explore whether flower size affects the flower‐pollinator interaction, we used Eurya japonica flowers. We examined whether artificial florivory decreased fruit and seed production, and also whether flower size affected florivory and the number of floral visitors. The petal removal treatment (i.e., artificial florivory) showed approximately 50% reduction in both fruit and seed set in natural pollination but not in artificial pollination. Furthermore, flower size increased the number of floral visitors, although it did not affect the frequency of florivory. Our results demonstrate that petal removal indirectly decreased 75% of female reproductive output via decreased flower visits by pollinators and that flower size mediated indirect interactions between florivory and floral visitors.

Time-lagged effect of predators on tadpole behaviour and parasite infection.

Prey should adjust their defences against natural enemies to match their current level of risk and balance other needs. This is particularly important when optimal defences represent trade-offs, as is the case with many predator-induced trait-mediated indirect effects (TMIEs) that are antagonistic to those promoting host resistance to parasites and pathogens. However, trade-offs may depend on whether different natural enemies are present simultaneously or represent temporally discrete threats. We found that larval amphibians (Anaxyrus americanus) previously exposed to predator cues did not engage in anti-parasite behaviours (activity increases) in response to a current risk of infection by a pathogenic trematode parasite compared to controls, resulting in higher infection intensities. This suggests that the memory of the likely more lethal threat (predation) had greater influence, maladaptively dampening tadpole activity. Incorporating complexity inherent in natural systems, including spatial and temporal overlap, is necessary to better understand natural enemy ecology and how TMIEs relate to infectious diseases.

Parasites alter freshwater communities in mesocosms by modifying invasive crayfish behavior.

Parasites can alter communities by reducing densities of keystone hosts, but few studies have examined how trait-mediated indirect effects of parasites can alter ecological communities. We test how trematode parasites (Microphallus spp.) that affect invasive crayfish (Orconectes rusticus) behavior alter how crayfish impact lake littoral communities. O. rusticus drive community composition in north temperate lakes, and predatory fish can reduce crayfish activity and feeding. In laboratory studies, Microphallus parasites also alter O. rusticus behavior: infected O. rusticus eat fewer macroinvertebrates and are bolder near predatory fish than uninfected individuals. We used a 2 x 2 factorial experiment to test how predatory fish and parasites affect O. rusticus impacts in large mesocosms over 4 weeks. We predicted (1) that when predators were absent, infected crayfish would have lower impacts than uninfected crayfish on macrophytes and macroinvertebrates (as well as reduced growth and higher mortality). However, (2) when predators were present but unable to consume crayfish, infected crayfish would have greater impacts (as well as greater growth and lower mortality) than uninfected crayfish because of increased boldness. Because of its effect on crayfish feeding behavior, we also predicted (3) that infection would alter macrophyte and macroinvertebrate community composition. In contrast to our first hypothesis, we found that infected and uninfected crayfish had similar impacts on lower trophic levels when predators were absent. Across all treatments, infected crayfish were more likely to be outside shelters and had greater growth than uninfected crayfish, suggesting that the reduced feeding observed in short-term experiments does not occur over longer timescales. However, in support of the second hypothesis, when predatory fish were present, infected crayfish ate more macroinvertebrates than did uninfected crayfish, likely due to increased boldness. We also observed a trend for greater macrophyte consumption associated with infection and a trend indicating infection might alter macroinvertebrate community composition. Our results suggest that parasites can alter aquatic communities in mesocosms merely by modifying host behavior.

Nectar robbing impacts pollinator behavior but not plant reproduction

Trait‐mediated indirect effects (TMIEs) refer to interactions in which the effect of one species on another is mediated by the behavior of a third species. A mechanistic approach that identifies the direction and impact of TMIEs can shed light on why different net outcomes are observed in the same general phenomena across systems. Nectar robbing has variable net effects through TMIEs on animal‐pollinated plants across systems, but the mechanistic steps underlying this range of outcomes are often unclear. To address this knowledge gap, we assessed linkages between nectar robbing, pollinator behavior and plant reproductive success in the Andean tree, Oreocallis grandiflora. We found that robbing in this system led to lower nectar volumes, higher nectar sucrose concentration, and higher nectar viscosity, which together negatively impact nectar quality. This drop in nectar quality was associated with decreased visitation rates by hummingbirds, which might be expected to impact plant reproduction negatively by pollen limitation. However, it was also associated with increased diversity (Shannon's) and evenness in the pollinator community due to reduced visitation by a territorial hummingbird, which might be expected to impact reproduction positively via enhanced genetic diversity of pollen as non‐territorial pollinators forage over greater areas. We measured seed set and mass to distinguish the relative intensity of these two possible outcomes, but found no detectable effect. We tentatively conclude that these two consequences of TMIEs may have balanced each other out to yield a neutral net effect of nectar robbing on plant reproduction, though other explanations are also possible. This study highlights ways in which ecologically important TMIEs may act in opposing directions to mask important ecological forces, and underscores the continued need for detailed study of the mechanisms through which TMIEs operate.