Gustavo Q. Romero

A Meta-Analysis of Predation Risk Effects on Pollinator Behaviour

Flower-visiting animals are constantly under predation risk when foraging and hence might be expected to evolve behavioural adaptations to avoid predators. We reviewed the available published and unpublished data to assess the overall effects of predators on pollinator behaviour and to examine sources of variation in these effects. The results of our meta-analysis showed that predation risk significantly decreased flower visitation rates (by 36%) and time spent on flowers (by 51%) by pollinators. The strength of the predator effects depended neither on predator taxa and foraging mode (sit-and-wait or active hunters) nor on pollinator lifestyle (social vs. solitary). However, predator effects differed among pollinator taxa: predator presence reduced flower visitation rates and time spent on flowers by Squamata, Lepidoptera and Hymenoptera, but not by Diptera. Furthermore, larger pollinators showed weaker responses to predation risk, probably because they are more difficult to capture. Presence of live crab spiders on flowers had weaker effects on pollinator behaviour than presence of dead or artificial crab spiders or other objects (e.g. dead bees, spheres), suggesting that predator crypsis may be effective to some extent. These results add to a growing consensus on the importance of considering both predator and pollinator characteristics from a community perspective.

TRAIT‐MEDIATED EFFECTS ON FLOWERS: ARTIFICIAL SPIDERS DECEIVE POLLINATORS AND DECREASE PLANT FITNESS

Although predators can affect foraging behaviors of floral visitors, rarely is it known if these top-down effects of predators may cascade to plant fitness through trait-mediated interactions. In this study we manipulated artificial crab spiders on flowers of Rubus rosifolius to test the effects of predation risk on flower-visiting insects and strength of trait-mediated indirect effects to plant fitness. In addition, we tested which predator traits (e.g., forelimbs, abdomen) are recognized and avoided by pollinators. Total visitation rate was higher for control flowers than for flowers with an artificial crab spider. In addition, flowers with a sphere (simulating a spider abdomen) were more frequently visited than those with forelimbs or the entire spider model. Furthermore, the presence of artificial spiders decreased individual seed set by 42% and fruit biomass by 50%. Our findings indicate that pollinators, mostly bees, recognize and avoid flowers with predation risk; forelimbs seem to be the predator trait recognized and avoided by hymenopterans. Additionally, predator avoidance by pollinators resulted in pollen limitation, thereby affecting some components of plant fitness (fruit biomass and seed number). Because most pollinator species that recognized predation risk visited many other plant species, trait-mediated indirect effects of spiders cascading down to plant fitness may be a common phenomenon in the Atlantic rainforest ecosystem.

Beneficial effects of flower-dwelling predators on their host plant

We examined the effects of the sit-and-wait spider Misumenops argenteus (Thomisidae) on the herbivore assemblage and fitness of the perennial woody shrub Trichogoniopsis adenantha (Asteraceae). Because crab spiders prey on both pollinators and phytophagous insects, they can have potentially negative and positive effects on plants. In a manipulative experiment using paired plants, spiders decreased the density of sucking and some endophagous herbivores on the leaves and capitula and reduced the number of damaged achenes produced by the plants. Damaged capitula had a higher proportion of fertilized achenes in plants with spiders than without spiders, but not undamaged capitula. These results indicate that M. argenteus exerted a double positive effect on seed production in T. adenantha. The effect of M. argenteus on herbivores may be taxon specific and vary among years with different herbivore abundances.

Contrasting cascade effects of carnivores on plant fitness: a meta-analysis.

1. Although carnivores indirectly improve plant fitness by decreasing herbivory, they may also decrease plant reproduction by disrupting plant-pollinator mutualism. The overall magnitude of the resulting net effect of carnivores on plant fitness and the factors responsible for the variations in strength and direction of this effect have not been explored quantitatively to date. 2. We performed a meta-analysis of 67 studies containing 163 estimates of the effects of carnivores on plant fitness and examined the relative importance of several potential sources of variation in carnivore effects. 3. Carnivores significantly increased plant fitness via suppression of herbivores and decreased fitness by consuming pollinators. The overall net effect of carnivores on plant fitness was positive (32% increase), indicating that effects via herbivores were stronger than effects via pollinators. 4. Parasitoids had stronger positive effect on plant fitness than predators. Active hunters increased plant fitness, whereas stationary predators had no significant effect, presumably because they were more prone to disrupt plant-pollinator mutualism. Carnivores with broader habitat domain had negative effects on plant fitness, whereas those with narrow habitat domain had positive effects. 5. Predator effects were positive for plants which offered rewards (e.g. extrafloral nectaries) and negative for plants which lacked any attractors. 6. This study adds new knowledge on the factors that determine the strength of terrestrial trophic cascades and highlights the importance of considering simultaneous contrasting interactions in the same study system.

BROMELIAD-LIVING SPIDERS IMPROVE HOST PLANT NUTRITION AND GROWTH

Although bromeliads are believed to obtain nutrients from debris deposited by animals in their rosettes, there is little evidence to support this assumption. Using stable isotope methods, we found that the Neotropical jumping spider Psecas chapoda (Salticidae), which lives strictly associated with the terrestrial bromeliad Bromelia balansae, contributed 18% of the total nitrogen of its host plant in a greenhouse experiment. In a one-year field experiment, plants with spiders produced leaves 15% longer than plants from which the spiders were excluded. This is the first study to show nutrient provisioning in a spider-plant system. Because several animal species live strictly associated with bromeliad rosettes, this type of facultative mutualism involving the Bromeliaceae may be more common than previously thought.

NATURAL HISTORY OF MISUMENOPS ARGENTEUS (THOMISIDAE): SEASONALITY AND DIET ON TRICHOGONIOPSIS ADENANTHA (ASTERACEAE)

Abstract Seasonal fluctuations, phenology and diet of Misumenops argenteus (Araneae, Thomisidae) on Trichogoniopsis adenantha (Asteraceae) were investigated in the Serra do Japi, southeastern Brazil, over a 2 year period. This spider population increased at the beginning of the rainy season, reaching a peak in March, and decreased in May, reaching its lowest density in the cold/dry season. In the rainy season (December–May), most of the individuals were in the young or juvenile phase (3rd–6th instars). The spiders reached adulthood between the end of the cold/dry season and the beginning of the hot/rainy season. Analysis of temporal displacement (with up to a 3 month delay) detected a one month delay between the blooming period of T. adenantha and the beginning of the rainy season. The number of arthropods (potential prey of M. argenteus) on the plants increased concomitantly with the increase in the number of reproductive branches. The M. argenteus population also increased numerically 2 months after the rise in arthropod density. These results indicate that the spiders require time to respond to changes in environmental conditions. Of the 595 spiders examined, 76 (12.8%) had prey. Prey items included arthropods belonging to several guilds, but spiders showed a preference for wingless prey or prey that remained on the branches for longer periods of time.

ANTI‐HERBIVORE PROTECTION BY MUTUALISTIC SPIDERS AND THE ROLE OF PLANT GLANDULAR TRICHOMES

Although specific associations between spiders and particular types of plants have been reported for several taxonomic groups, their consequences for spiders and plants are still poorly understood. The most common South American lynx spiders, Peucetia flava and P. rubrolineata, live strictly associated with various plant species that have glandular trichomes. To understand more about these spider-plant relationships, we investigated the influence of the spiders on the fitness of a neotropical glandular shrub (Trichogoniopsis adenantha) and on the arthropod community structure on the plant. We also tested whether glandular hairs provided any benefit to the spiders. Spiders reduced the abundance of several species and guilds of herbivores on the leaves and inflorescences. Consequently, damage to the leaves, capitula, ovaries, corollas, and stigmas caused by leaf-mining and chewing insects, as well as endophagous insects, were strongly reduced in the presence of Peucetia spp. Although the spiders fed on flower visitors, their negative influence on ovary fertilization was only marginally nonsignificant (P = 0.065). Spiders on plants of Trichogoniopsis adenantha that fed on common fruit flies that had died before adhering to the glandular trichomes did not lose body mass. However, those living on plants without stalked glandular trichomes (Melissa officinalis) did not feed on dead flies and lost 13-20% of their biomass. These results indicate that Peucetia spiders are effective plant bodyguards and that when there is limited live prey they may feed on insect carcasses adhered to glandular trichomes. Since several spider species of the genus Peucetia live strictly associated with glandular trichome-bearing plants in neotropical, Neartic, Paleartic, and Afrotropical regions, this type of facultative mutualism involving Peucetia and glandular plants may be common worldwide.

Food-web composition affects cross-ecosystem interactions and subsidies

1. Ecosystems may affect each other through trophic interactions that cross ecosystem boundaries as well as via the transfer of subsidies, but these effects can vary depending on the identity of species involved in the interaction. 2. In this study, we manipulated two terrestrial bromeliad-living spider species (Aglaoctenus castaneus, Corinna gr. rubripes) that have variable hunting modes, to test their individual and combined effects on aquatic invertebrate community structure and ecosystem processes (i.e. decomposition rate and nitrogen cycling). We predicted that these terrestrial predators can affect aquatic invertebrates and nutrient dynamics within water-filled bromeliads. 3. Aglaoctenus spiders reduced the richness, abundance and biomass of aquatic insect larvae via consumptive or non-consumptive effects on ovipositing terrestrial adults, but effects of the two spider species in combination were usually the linear average of their monoculture effects. In contrast, invertebrates with entirely aquatic life cycles were unaffected or facilitated by spiders. Spiders did not affect either net detritivore biomass or the flux of detrital nitrogen to the bromeliad. Instead, Corinna spiders contributed allochthonous nitrogen to bromeliads. 4. Our results provide the novel observations that predators in one ecosystem not only directly reduce taxa whose life cycles cross-ecosystem boundaries, but also indirectly facilitate taxa whose life cycles are entirely within the second ecosystem. This compensatory response between cross-ecosystem and within-ecosystem taxa may have led to an attenuation of top-down effects across ecosystem boundaries. In addition, our results add to a growing consensus that species identity is an important determinant of community structure and ecosystem functioning. Thus, the composition of both terrestrial and aquatic food webs may affect the strength of cross-ecosystem interactions.

Ecosystem engineering effects on species diversity across ecosystems: a meta-analysis.

Ecosystem engineering is increasingly recognized as a relevant ecological driver of diversity and community composition. Although engineering impacts on the biota can vary from negative to positive, and from trivial to enormous, patterns and causes of variation in the magnitude of engineering effects across ecosystems and engineer types remain largely unknown. To elucidate the above patterns, we conducted a meta‐analysis of 122 studies which explored effects of animal ecosystem engineers on species richness of other organisms in the community. The analysis revealed that the overall effect of ecosystem engineers on diversity is positive and corresponds to a 25% increase in species richness, indicating that ecosystem engineering is a facilitative process globally. Engineering effects were stronger in the tropics than at higher latitudes, likely because new or modified habitats provided by engineers in the tropics may help minimize competition and predation pressures on resident species. Within aquatic environments, engineering impacts were stronger in marine ecosystems (rocky shores) than in streams. In terrestrial ecosystems, engineers displayed stronger positive effects in arid environments (e.g. deserts). Ecosystem engineers that create new habitats or microhabitats had stronger effects than those that modify habitats or cause bioturbation. Invertebrate engineers and those with lower engineering persistence (<1 year) affected species richness more than vertebrate engineers which persisted for >1 year. Invertebrate species richness was particularly responsive to engineering impacts. This study is the first attempt to build an integrative framework of engineering effects on species diversity; it highlights the importance of considering latitude, habitat, engineering functional group, taxon and persistence of their effects in future theoretical and empirical studies.

Dominant predators mediate the impact of habitat size on trophic structure in bromeliad invertebrate communities

Local habitat size has been shown to influence colonization and extinction processes of species in patchy environments. However, species differ in body size, mobility, and trophic level, and may not respond in the same way to habitat size. Thus far, we have a limited understanding of how habitat size influences the structure of multitrophic communities and to what extent the effects may be generalizable over a broad geographic range. Here, we used water-filled bromeliads of different sizes as a natural model system to examine the effects of habitat size on the trophic structure of their inhabiting invertebrate communities. We collected composition and biomass data from 651 bromeliad communities from eight sites across Central and South America differing in environmental conditions, species pools, and the presence of large-bodied odonate predators. We found that trophic structure in the communities changed dramatically with changes in habitat (bromeliad) size. Detritivore : resource ratios showed a consistent negative relationship with habitat size across sites. In contrast, changes in predator: detritivore (prey) ratios depended on the presence of odonates as dominant predators in the regional pool. At sites without odonates, predator: detritivore biomass ratios decreased with increasing habitat size. At sites with odonates, we found odonates to be more frequently present in large than in small bromeliads, and predator: detritivore biomass ratios increased with increasing habitat size to the point where some trophic pyramids became inverted. Our results show that the distribution of biomass amongst food-web levels depends strongly on habitat size, largely irrespective of geographic differences in environmental conditions or detritivore species compositions. However, the presence of large-bodied predators in the regional species pool may fundamentally alter this relationship between habitat size and trophic structure. We conclude that taking into account the response and multitrophic effects of dominant, mobile species may be critical when predicting changes in community structure along a habitat-size gradient.