Micky D. Eubanks

Ecological consequences of interactions between ants and honeydew-producing insects

Interactions between ants and honeydew-producing hemipteran insects are abundant and widespread in arthropod food webs, yet their ecological consequences are very poorly known. Ant–hemipteran interactions have potentially broad ecological effects, because the presence of honeydew-producing hemipterans dramatically alters the abundance and predatory behaviour of ants on plants. We review several studies that investigate the consequences of ant–hemipteran interactions as ‘keystone interactions’ on arthropod communities and their host plants. Ant–hemipteran interactions have mostly negative effects on the local abundance and species richness of several guilds of herbivores and predators. In contrast, out of the 30 studies that document the effects of ant–hemipteran interactions on plants, the majority (73%) shows that plants actually benefit indirectly from these interactions. In these studies, increased predation or harassment of other, more damaging, herbivores by hemipteran-tending ants resulted in decreased plant damage and/or increased plant growth and reproduction. The ecological consequences of mutualistic interactions between honeydew-producing hemipterans and invasive ants relative to native ants have rarely been studied, but they may be of particular importance owing to the greater abundance, aggressiveness and extreme omnivory of invasive ants. We argue that ant–hemipteran interactions are largely overlooked and underappreciated interspecific interactions that have strong and pervasive effects on the communities in which they are embedded.

THE ECOLOGICAL CONSEQUENCES OF VARIATION IN PLANTS AND PREY FOR AN OMNIVOROUS INSECT

We conducted a series of laboratory and field experiments to determine the effects of variation in plant quality and prey species on the survival, dispersal, and population size of a common, omnivorous insect. We also tested the hypothesis that plant feeding allows omnivorous “predators” to survive periods when prey are scarce. In addition, we compared the response of omnivores and strict predators to variation in plants and prey. We found that variation in plant parts (pods and leaves) and prey species (moth eggs and aphids) affected the survival, dispersal, and population size of big-eyed bugs, Geocoris punctipes, in Maryland lima beans. The survival of big-eyed bugs fed moth eggs was high and unaffected by the availability of lima bean pods or leaves as supplemental food. The survival of big-eyed bugs fed aphids, however, was relatively low and dramatically improved by the availability of pods. Big-eyed bugs fed only pods developed normally through the first and second instar, but development was arres...

Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species.

1. In order to understand the relative importance of prey quality and mobility in indirect interactions among alternative prey that are mediated by a shared natural enemy, the nutritional quality of two common prey for a generalist insect predator along with the predators relative preference for these prey was determined.

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.

Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae).

Abstract Previous studies have demonstrated genetic variation for resistance to insect herbivores and host plant quality. The effect of plant mating system, an important determinant of the distribution of genetic variation, on host plant characteristics has received almost no attention. This study used a controlled greenhouse experiment to examine the effect of self‐ and cross‐pollination in Mimulus guttatus (Scrophulariaceae) on resistance to and host plant quality for the xylem‐feeding spittlebug Philaenus spumarius (Homoptera: Cercopidae). Spittlebugs were found to have a negative effect on two important fitness components in M. guttatus, flower production and aboveground biomass. One of two M. guttatus populations examined showed a significant interaction between the pollination and herbivore treatments. In this case, the detrimental effects of herbivores on biomass and flower production were much more pronounced in inbred (self) plants. The presence of spittlebug nymphs increased inbreeding depression by as much as three times. Pollination treatments also had significant effects on important components of herbivore fitness, but these effects were in opposite directions in our two host plant populations. Spittlebug nymphs maturing on self plants emerged as significantly larger adults in one of our host plant populations, indicating that inbreeding increased host plant quality. In our second host plant population, spittlebug nymphs took significantly longer to develop to adulthood on self plants, indicating that inbreeding decreased host plant quality. Taken together these results suggest that the degree of inbreeding in host plant populations can have important and perhaps complex effects on the dynamics of plant‐herbivore interactions and on mating‐system evolution in the host.

Host plants mediate omnivore-herbivore interactions and influence prey suppression.

We conducted laboratory and field experiments to determine the effects of plant quality and prey abundance on the intensity of interactions involving an omnivorous insect, its two herbivorous prey, and their shared host plant. We found that variation in plant quality, prey abundance, and presence of alternative prey altered the functional response of the omnivorous big-eyed bug, Geocoris punctipes (Heteroptera: Geocoridae). The presence of high-quality plant parts (lima bean pods) reduced the number of prey (pea aphids and corn earworm eggs) consumed by big-eyed bugs. The results of our caged, field experiments mirrored those of the functional-response experiment. Populations of pea aphids were larger when caged with big-eyed bugs on bean plants with pods than on plants without pods. Pods, therefore, had an indirect, positive effect on the survivorship of herbivorous insects that feed on lima beans. Because pods reduced the number of prey consumed by big-eyed bugs, and caged prey populations were larger o...

APHIDS ALTER THE COMMUNITY-WIDE IMPACT OF FIRE ANTS

Positive species interactions have the potential to strongly influence the structure and dynamics of ecological communities, yet surprisingly few studies have documented their general importance. We tested the hypothesis that the mutualistic association between fire ants and aphids enhances the impact of fire ants on the herbivorous and predaceous arthropod community of cotton. We found that the presence of aphids attracted foraging fire ants onto cotton plants. This shift from ground to foliar foraging resulted in more frequent interactions between fire ants and arthropods associated with cotton. The survival of herbivores (caterpillars) and predators (ladybird beetles and lacewings) was lower in the presence of fire ants and aphids compared with fire ants alone in greenhouse experiments. Similarly, fire ants and aphids deterred plant bugs from spending time on cotton foliage. Using large-scale field manipulations of fire ants along with naturally occurring aphid populations, we found that the ant–aphid ...

Disruption of Cotton Aphid (Homoptera: Aphididae)-Natural Enemy Dynamics by Red Imported Fire Ants (Hymenoptera: Formicidae)

Abstract Red imported fire ants, Solenopsis invicta (Buren) (Hymenoptera: Formicidae), are an invasive species found in high densities throughout southeastern agricultural systems. We tested the hypothesis that fire ants tend cotton aphids, Aphis gossypii Glover (Homoptera: Aphididae), and thus release them from predation by lady beetle larvae, Coccinella septempunctata L. and Hippodamia convergens Guerin-Meneville (Coleoptera: Coccinellidae), and green lacewing larvae, Chrysoperla carnea Stephens (Neuroptera: Chrysopidae). Fire ants preferentially foraged on aphid-infested cotton, Gossypium hirsutum L., plants (x̄ = 103 ± 47 ants per plant) compared with plants without aphids (x̄ = 5 ± 3 ants per plant). In caged greenhouse experiments, fire ants reduced survival of lady beetle larvae by 92.9% and green lacewing larvae by 83.3%. Furthermore, strong mortality imposed on aphid predators by fire ants affected aphid survival. With the addition of fire ants to aphid-predator treatments, aphid survival approximately doubled. In a field experiment, predator larvae were more abundant in cotton plots with experimentally suppressed densities of fire ants (0.62 ± 0.11 lady beetle larvae per sample; 0.06 ± 0.02 lacewing larvae per sample) than in plots with high fire ant densities (0.23 ± 0.06 lady beetle larvae per sample; 0.01 ± 0.01 lacewing larvae per sample). Conversely, cotton aphids were more abundant in high fire ant density field plots (x̄ = 6.83 ± 0.03 aphids per leaf) than in low fire ant density plots (x̄ = 4.04 ± 0.03 aphids per leaf). These data suggest that red imported fire ants enhance cotton aphid survival and density in the field through predator interference.

A Multiyear, Large-Scale Comparison of Arthropod Populations on Commercially Managed Bt and Non-Bt Cotton Fields

Abstract Field studies were conducted in 2000–2002 to compare foliage-dwelling arthropod populations on Bacillus thuringiensis Berliner (Bt) (Bollgard) cotton and non-Bt (conventional) cotton season-long in South Carolina, Georgia, northern Alabama, and southern Alabama. For each of these four regions, three or four paired fields were sampled weekly in each of the 3 yr. Each pair of fields consisted of a Bt and a non-Bt cotton field, both at least 5 ha in size. The dominant arthropod taxa collected included target pests (heliothine moths and Spodoptera spp.), nontarget pests (stink bugs and plant bugs), and generalist natural enemies [Geocoris spp., Orius spp., Solenopsis invicta (Buren), ladybeetles, and spiders]. Where target pests were present, particularly Helicoverpa zea (Boddie), their numbers were consistently significantly lower in the Bt cotton fields. Natural enemy populations generally were not significantly different between the Bt and the non-Bt cotton fields (50% of all comparisons) and, where significant differences were present, natural enemy abundance usually was higher in the Bt than the non-Bt cotton fields. These differences were correlated with lower insecticide use on the Bt than the non-Bt cotton fields, particularly in South Carolina, where target pest pressure was heaviest. When presented with insect eggs or larvae as prey items, the larger natural enemy populations in Bt cotton fields exhibited significantly higher predation rates. These results show that Bt cotton has no significant adverse impacts on the nontarget arthropod populations studied and, compared with insecticide-treated non-Bt cotton, Bt cotton supports higher natural enemy populations with significant positive impacts on biological control.

Intercontinental differences in resource use reveal the importance of mutualisms in fire ant invasions

Mutualisms play key roles in the functioning of ecosystems. However, reciprocally beneficial interactions that involve introduced species also can enhance invasion success and in doing so compromise ecosystem integrity. For example, the growth and competitive ability of introduced plant species can increase when fungal or microbial associates provide limiting nutrients. Mutualisms also may aid animal invasions, but how such systems may promote invasion success has received relatively little attention. Here we examine how access to food-for-protection mutualisms involving the red imported fire ant (Solenopsis invicta) aids the success of this prominent invader. Intense interspecific competition in its native Argentina constrained the ability of S. invicta to benefit from honeydew-producing Hemiptera (and other accessible sources of carbohydrates), whereas S. invicta dominated these resources in its introduced range in the United States. Consistent with this strong pattern, nitrogen isotopic data revealed that fire ants from populations in the United States occupy a lower trophic position than fire ants from Argentina. Laboratory and field experiments demonstrated that honeydew elevated colony growth, a crucial determinant of competitive performance, even when insect prey were not limiting. Carbohydrates, obtained largely through mutualistic partnerships with other organisms, thus represent critical resources that may aid the success of this widespread invasive species. These results illustrate the potential for mutualistic interactions to play a fundamental role in the establishment and spread of animal invasions.