Gail A. Langellotto

Responses of invertebrate natural enemies to complex-structured habitats: a meta-analytical synthesis

The structural complexity of habitats has been espoused as an important factor influencing natural-enemy abundance and food-web dynamics in invertebrate-based communities, but a rigorous synthesis of published studies has not heretofore been conducted. We performed a meta-analytical synthesis of the density response of natural enemies (invertebrate predators and parasitoids) to experimental increases and decreases in the structural complexity of their habitats using data from 43 published studies, reporting 62 independent taxa. Studies varied in structural complexity at two spatial scales (habitat and within-plant architecture) and comprised a diverse array of natural-enemy taxa (natural-enemy assemblage at large, the entire spider assemblage, hunting spiders, web-building spiders, mites, hemipterans, coccinellid beetles, carabid beetles, ants, and parasitoids). For all taxa combined, increasing habitat structure resulted in a large and significant increase in natural enemy abundance. Similarly, decreasing habitat structure significantly diminished natural enemy abundance. Separate meta-analyses at two spatial scales (habitat and within-plant architecture) found that increasing habitat complexity resulted in significant increases in abundance. In particular, manipulating levels of detritus at the habitat spatial scale had the strongest effect on natural enemy abundance. In general, most guilds of natural enemies were significantly affected when the structural complexity of the habitat was altered. Seven of nine natural enemy guilds were more abundant under conditions of increased habitat complexity, with hunting spiders and web-building spiders showing the strongest response followed by hemipterans, mites, and parasitoids. Spiders in particular were negatively affected when habitat structure was simplified. The mechanisms underlying the accumulation of natural enemies in complex-structured habitats are poorly known. However, refuge from intraguild predation, more effective prey capture, and access to alternative resources (alternative prey, pollen, or nectar), are possible candidates. Our analysis was unable to confirm that predators aggregate in complex-structured habitats because prey (mostly herbivores) are more abundant there. The results of this meta-analysis support the view that basal resources mediate top-down impacts on herbivores, and provide encouragement that manipulations of habitat complexity can be made in agroecosystems that will enhance the effectiveness of the natural enemy complex for more effective pest suppression.

BOTTOM-UP FORCES MEDIATE NATURAL-ENEMY IMPACT IN A PHYTOPHAGOUS INSECT COMMUNITY

We employed a combination of factorial experiments in the field and labo- ratory to investigate the relative magnitude and degree of interaction of bottom-up factors (two levels each of host-plant nutrition and vegetation complexity) and top-down forces (two levels of wolf-spider predation) on the population growth of Prokelisia planthoppers (P. dolus and P. marginata), the dominant insect herbivores on Spartina cordgrass through- out the intertidal marshes of North America. Treatments were designed to mimic combi- nations of plant characteristics and predator densities that occur naturally across habitats in the field. There were complex interactive effects between plant resources and spider predation on the population growth of planthoppers. The degree that spiders suppressed planthoppers depended on both plant nutrition and vegetation complexity, an interaction that was dem- onstrated both in the field and laboratory. Laboratory results showed that spiders checked planthopper populations most effectively on poor-quality Spartina with an associated matrix of thatch, all characteristics of high-marsh meadow habitats. It was also this combination of plant resources in concert with spiders that promoted the smallest populations of planthop- pers in our field experiment. Planthopper populations were most likely to escape the sup- pressing effects of predation on nutritious plants without thatch, a combination of factors associated with observed planthopper outbreaks in low-marsh habitats in the field. Thus, there is important spatial variation in the relative strength of forces with bottom-up factors dominating under low-marsh conditions and top-down forces increasing in strength at higher elevations on the marsh. Enhancing host-plant biomass and nutrition did not strengthen top-down effects on planthoppers, even though nitrogen-rich plants supported higher densities of wolf spiders and other invertebrate predators in the field. Rather, planthopper populations, particularly those of Prokelisia marginata, escaped predator restraint on high-quality plants, a result we attribute to its mobile life history, enhanced colonizing ability, and rapid growth rate. Thus, our results for Prokelisia planthoppers suggest that the life history strategy of a species is an important mediator of top-down and bottom-up impacts. In laboratory mesocosms, enhancing plant biomass and nutrition resulted in increased spider reproduction, a cascading effect associated with planthopper increases on high- quality plants. Although the adverse effects of spider predation on planthoppers cascaded down and fostered increased plant biomass in laboratory mesocosms, this result did not occur in the field where top-down effects attenuated. We attributed this outcome in part to the intraguild predation of other planthopper predators by wolf spiders. Overall, the general paradigm in this system is for bottom-up forces to dominate, and when predators do exert a significant suppressing effect on planthoppers, their impact is generally legislated by vegetation characteristics.

Bee Richness and Abundance in New York City Urban Gardens

Abstract We describe the richness, abundance, and ecological characteristics of bees in community gardens located in heavily developed neighborhoods of the Bronx and East Harlem, NY. In total, 1,145 individual bees, representing 54 species (13% of the recorded New York State bee fauna) were collected over 4 yr. The nesting habits of these species include bees that nest in cavities (33% of species), hives (11% of species), pith (1.9% of species), wood (1.9% of species), or soft/rotting wood (7.4% of species) substrates. Soil-nesting individuals were relatively rare (25% of individuals), perhaps due to a lack of proper soils for nesting sites. Parasitic species were scarce (5.6% of species, 2.6% of individuals), most likely because of an absence or rarity of host species. Overall, exotic species were abundant and constituted 27% of the total individuals collected and 19% of the identified species. We compare these results to several bee faunal surveys in New Jersey and New York State, including newly reported species lists for Central Park and Prospect Park in New York City. Relative to other studies, bee richness of the urban gardens is reduced and composition is biased toward exotic and cavity-nesting species. Nevertheless, despite their small size and location within highly urbanized areas, urban community gardens harbor a diverse assemblage of bees that may provide pollination services and opportunities for ecological exposure and education.

Feeding-induced changes in plant quality mediate interspecific competition between sap-feeding herbivores.

Feeding-induced plant resistance is a well-documented phenomenon for leaf- chewing insects. Furthermore, feeding-induced resistance provides the mechanistic basis for many cases of delayed interspecific competition, whereby previous feeding by one species diminishes the performance of other herbivores which attack the same plant later in the season. This phenomenon, however, has been very poorly investigated for sap-feeding insects. The results we present here for salt marsh-inhabiting planthoppers ( Prokelisia dolus and P. marginata) provide one of the few known examples of delayed, plant-mediated interspecific competition between two sap-feeding insects. Three lines of experimental evidence from the laboratory, field cages, and open field plots provide support for the detrimental effects of previous feeding by one planthopper species on the subsequent survival and performance of the other. Laboratory experiments showed that prior feeding on cordgrass by one congener resulted in reduced performance of the other in the following generation. However, the effect was asymmetric. Prior feeding by P. dolus resulted in prolonged development and reduced body size (a correlate of fecundity) in P. marginata, whereas only development was protracted in P. dolus when plants were previously exposed to P. marginata. Consequently, P. dolus appears to be the superior competitor in the context of delayed, plant-mediated interactions. The negative effects of previous feeding by P. dolus on the development time, body size, and survival of P. marginata obtained in the laboratory were confirmed both in cages and on cage-free islets of cordgrass in the field. Feeding-induced reductions in host-plant quality by P. dolus may provide additional impetus for P. marginata to migrate from shared habitats on the high marsh to nutritionally superior plants in the low marsh rarely occupied by P. dolus. The mechanism underlying the delayed competitive effects between Prokelisia plan- thoppers is most likely diminished plant nutrition, because feeding by P. dolus significantly reduces the concentration of essential amino acids in cordgrass. The asymmetry of plant- mediated competition between the Prokelisia species may be due to the ability of P. dolus to better tolerate feeding-depleted levels of plant nitrogen via compensatory feeding. Even though these two planthoppers do not suffer significant fitness reductions during contemporaneous interactions, they compete severely in the context of feeding-induced plant resistance which is expressed later in the season. This result, coupled with the fact that most studies of interspecific interaction between herbivorous insects are contempo- raneous, indicates that interspecific competition may be profoundly underestimated as a structuring force in phytophagous insect communities.

Habitat Persistence Underlies Intraspecific Variation in the Dispersal Strategies of Planthoppers

Dispersal is considered a vital life history characteristic for insects exploiting temporary habitats, and life history theorists have often hypothesized an inverse relationship between dispersal capability and habitat persistence. Most often, this hypothesis has been tested using interspecific comparisons of dispersal capability and qualitative estimates of habitat persistence. Consequently, most assessments have failed to control for possible phylogenetic nonindependence and they also lack quantitative rigor. We capitalized on existing intraspecific variation in the dispersal capability of Prokelisia planthoppers to examine the relationship between habitat persistence and dispersal, thereby minimizing possible phylogenetic effects. Two congeneric species (Prokelisia marginata and P. dolus) occur in the intertidal marshes of North America, where they feed exclusively on cordgrasses (Spartina). Because these planthoppers exhibit wing dimorphism, flight- capable adults (macropters with fully developed wings) are easily differentiated from flight- less adults (brachypters with reduced wings). Thus, dispersal capability can be readily estimated by the percentage of macropters in a population. At a regional spatial scale, we found a highly significant negative relationship between dispersal capability (percent macroptery) and habitat persistence. In this system, habitat persistence is influenced by a combination of marsh elevation, winter severity, and tidal range, which interact to determine the ability of planthoppers to endure through winter in their primary habitat for development. P. marginata develops primarily in low-marsh hab- itats during summer, habitats that can be subjected to pronounced winter disturbance due to ice scouring and/or extensive tidal inundation. Levels of winter disturbance of the low marsh are extreme along the Atlantic coast, intermediate along the Pacific, and low along the Gulf. Both the failure of P. marginata populations to remain through winter in this habitat, and the dispersal ability of these populations (92%, 29%, and 17% macroptery, respectively), are correlated with levels of disturbance. Thus, in regions where winter disturbance is high, levels of dispersal are correspondingly high to allow for recolonization of extirpated habitats from overwintering sites on the high marsh. Unlike P. marginata, P. dolus develops primarily in high-marsh habitats, which are much less disturbed on all coasts during winter. Consequently, this species remains year-round in its primary habitat for development, and most populations exhibit relatively low levels of macroptery (<10%). When raised under common garden conditions, many more macropters of both species were produced from Atlantic compared to Gulf populations. Thus the proportion of ma- cropters produced from the populations used in this experiment paralleled the incidence of macroptery measured in the field, providing evidence that the geographic variation in dispersal capability in both species has in part a genetic basis. The results of this study provide strong intraspecific evidence for an inverse relationship between the dispersal capability of insects and the persistence of their habitats.

The Bee Fauna of Residential Gardens in a Suburb of New York City (Hymenoptera: Apoidea)

Abstract As suburban landscapes expand, it is critical to understand their capacity to support wildlife. Pollinators, specifically bees (Hymenoptera: Apoidea: Anthophila), are to some degree compatible with urbanization and may be able to exist in suburbs in diverse assemblages. We surveyed 21 residential gardens for bees in Westchester County, a suburban area immediately north of New York City. From a sample of 1,675 individuals, we documented 110 species, of which 95% were native, 50% were solitary, and 93% were polylectic. In terms of abundance of specimens, eusocial (50% of specimens), native (97%), and polylectic (98%) bees were dominant. Contrary to our expectation, based on previous bee surveys in urban landscapes, the bee community documented was not depauperate in either soil-nesting or parasitic species (65 and 19% of species, respectively), nor was it enriched in exotic species (6% of species). Instead, the assemblage resembled the richer bee fauna documented at a 1,520-ha research preserve (forest) located in the same region, although certain specialist (oligolectic) and/or forest-associated species were absent. These results suggest that suburban landscapes in eastern North America have the potential to host relatively diverse and intact bee communities.

Interactions between a hunting spider and a web‐builder: consequences of intraguild predation and cannibalism for prey suppression

Abstract.  1. Antagonistic interactions among invertebrate predators such as intraguild predation and cannibalism have the potential to dampen top‐down impacts on shared prey at lower trophic levels. Two abundant spider predators, the large wolf spider Pardosa littoralis and the small sheet‐web builder Grammonota trivitatta co‐occur on the salt marshes of eastern North America where they both attack planthoppers (Prokelisia spp.), the dominant herbivores on the marsh. Experiments both in the laboratory and field were used to assess the incidence of intraguild predation and cannibalism in these spiders and elucidate how such antagonistic interactions influence planthopper suppression.

A trade-off between flight capability and reproduction in males of a wing-dimorphic insect.

The widespread occurrence of dispersal polymorphisms among insects is consistent with the hypothesis that fitness costs are associated with flight capability. Al- though trade-offs between flight capability and reproduction are well documented in the females of many wing-polymorphic insect species, the relationship between dispersal ca- pability and reproductive success in males is poorly established. Here we examine the potential cost of flight capability in males of the salt-marsh-inhabiting planthopper Pro- kelisia dolus (Hemiptera: Delphacidae). This species exhibits a dispersal polymorphism with both flightless adults (brachypters) and migratory adults (macropters) occurring in populations. In a competitive setting in the laboratory, brachypterous males exhibited a threefold mating advantage over macropterous males; they obtained 77% of the matings with bra- chypterous females. This mating advantage resulted, in part, from brachypterous males aggressively displacing rival macropters during courtship. There was also a nonsignificant tendency for brachypterous males to arrive before macropterous males to court a calling female. Neither female rejection behavior nor male body size appeared to contribute to the mating advantage of brachypterous males. When macropterous females were contested, the mating advantage of the male wing forms changed and macropterous males obtained the majority of matings. Thus, there was evidence for assortative mating based on wing form. When placed with ten brachypterous females, brachypterous males sired twice as many offspring as did macropterous males. This advantage was due to brachypters siring more offspring per female and not from inseminating more females; hence differences in sperm load between the male wing forms are implicated in the siring advantage of brachypters. There was, however, no tendency for brachypterous males to survive longer than their macropterous counterparts; thus, differences in longevity did not contribute to enhanced siring ability. Overall, these results provide support for a trade-off between dispersal ca- pability and reproductive success in males.

Refuge from cannibalism in complex‐structured habitats: implications for the accumulation of invertebrate predators

Abstract 1. Like many invertebrate predators, the wolf spider Pardosa littoralis Banks (Araneae: Lycosidae) accumulates in complex‐structured habitats replete with leaf litter (thatch). Here we test the hypothesis that P. littoralis accumulates in complex habitats to gain refuge from cannibalism.

BENEFITS OF DISPERSAL IN PATCHY ENVIRONMENTS: MATE LOCATION BY MALES OF A WING‐DIMORPHIC INSECT

Dispersal dimorphisms, in which both flight-capable and flightless adults occur in the same species, are commonplace in insects. Such dimorphisms are seen as reflecting a balance between the benefits and costs of flight and wing reduction or loss. In heterogeneous habitats, theory predicts that fitness trade-offs can favor the evolution of a dispersal dimorphism in which both flight-capable and flightless morphs are retained in the same population. Despite the wealth of theory, however, there has never been an explicit field assessment of how habitat heterogeneity directly influences the reproductive success of the flight-capable and flightless wing forms of an insect species. The objective of this research was to investigate how variation in habitat heterogeneity (vegetation structure) and female density influence mate location and thus the potential for reproductive success by the male wing forms of a salt marsh inhabiting insect, the planthopper Prokelisia dolus. By placing unmated females in the field at different densities and in sparse and contiguous vegetation, we were able to compare the ability of male wing forms to locate stationary mates. Our data show that both vegetation structure and female density differentially influenced the ability of the male wing forms to locate mates. Flight-capable males located females and acquired matings far more frequently in sparse vegetation, whereas flightless males discovered females more often in contiguous vegetation. Flight-capable males located females more effectively at low female densities, whereas flightless males discovered females more efficiently at higher female densities. Thus, natural variation in vegetation structure and female density are two important factors which combine to influence the mating success of each male wing form. We conclude that habitat heterogeneity in concert with the known reproductive penalties imposed by flight capability (reduced siring ability) interact to favor the persistence of the dispersal polymorphism in males of this planthopper species.