John D. Styrsky

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 EVOLUTION OF OMNIVORY IN HETEROPTERAN INSECTS

Although omnivory is common and widespread across many animal taxa, the evolutionary origin of omnivory, the selective forces that promote or constrain omni- vory, and the morphological, physiological, and behavioral hurdles that animals have to overcome to become omnivores have not been studied. The goal of this paper is to stimulate the development of ideas concerning the evolution of omnivory. We focus on the terrestrial lineages of the insect order Heteroptera and use published life history data and recent phylogenies to test two hypotheses concerning the evolutionary origin of feeding on both plants and prey: (1) that the propensity to feed on seeds and pollen is correlated with the evolution of omnivory, and (2) that broad host range (polyphagy) is correlated with the evolution of omnivory. In order to test these hypotheses, we mapped the plant part consumed and host plant range of insect species in two heteropteran suborders onto their respective phylogenies and used phylogenetically independent contrasts to test for correlations of these traits with omnivory. We found evidence that seed and pollen feeding and broad host ranges are correlated with the evolution of omnivory within both ancestrally herbivorous and ancestrally predaceous lineages of terrestrial heteropterans.

A facultative mutualism between aphids and an invasive ant increases plant reproduction

1. The consequences to plants of ant–aphid mutualisms, particularly those involving invasive ants, are poorly studied. Ant–aphid mutualisms may increase or decrease plant fitness depending on the relative cost of herbivory by ant‐tended aphids versus the relative benefit of increased ant suppression of other (non‐aphid) herbivores.

Why Are Incubation Periods Longer in the Tropics? A Common-Garden Experiment with House Wrens Reveals It Is All in the Egg

Incubation periods of Neotropical birds are often longer than those of related species at temperate latitudes. We conducted a common‐garden experiment to test the hypothesis that longer tropical incubation periods result from longer embryo development times rather than from different patterns of parental incubation behavior. House wrens, one of few species whose geographic range includes tropical equatorial and temperate high latitudes, have incubation periods averaging 1.2 days longer at tropical latitudes. We incubated eggs of house wrens in Illinois and Panama under identical conditions in mechanical incubators. Even after factoring out differences in egg size, tropical house wrens still required 1.33 days longer, on average, to hatch. We conclude that parental attendance patterns do not account for latitudinal differences in incubation period but that some other as yet unmeasured factor intrinsic to the egg or embryo, or both, extends development time in the tropics.

SOURCES OF EGG-SIZE VARIATION IN HOUSE WRENS (TROGLODYTES AEDON): ONTOGENETIC AND ENVIRONMENTAL COMPONENTS

Abstract Evolutionary theory predicts that heritability of fitness-related traits should be low. Egg size in birds is a fitness-related trait, but exhibits high heritability. One possible explanation for the apparent failure of natural selection to exhaust variability is that variation in egg size is mediated by female condition. In this study, we estimated repeatability of egg size within and between successive clutches in a wild, double-brooded population of House Wrens (Troglodytes aedon) in central Illinois, and examined the relationship of egg size with female size and condition. Repeatability of egg volume and mass in individual birds was high within years and between successive years (>0.77), suggesting a substantial heritable component to variation in egg size. However, egg mass was also significantly correlated with female condition. We suggest that the high repeatability values largely reflect permanent but nongenetic (ontogenetic) variation in egg size among females, which is reflected in the positive correlation of egg size with female condition. If variation in egg size is attributable to a combination of nonheritable, ontogenetic variation and variation due to current environmental conditions among females, then selection may not produce an evolutionary response in egg size.

Ant-Hemipteran Mutualisms: Keystone Interactions that Alter Food Web Dynamics and Influence Plant Fitness

Predicting the direct and indirect effects of natural enemies on herbivorous insects in species-rich, highly connected arthropod food webs can be extremely difficult. Community ecologists developed the keystone species concept to help simplify this task. Keystone species are species that have disproportionately large effects on the abundance of many interacting species in a community. Keystone species, however, can be difficult to identify in some communities and the effect of species that seem to play key roles in community dynamics often vary dramatically in both space and time. In some communities, pairwise interactions among species may alter the community-wide effect of a species such that it functions as a keystone species. In this chapter, we term this a ‘keystone interaction’ and explore the possibility that mutualisms involving ants and honeydew-producing Hemipterans may alter the abundance and distribution of many species in a predictable manner via increased ant predation in the presence of Hemipterans. Mutualisms involving ants and honeydew-producing insects are incredibly widespread in terrestrial ecosystems and may alter the structure of entire arthropod communities. We review cases where these mutualisms result in interference of biological control via intraguild predation of important biological control agents as well as cases where ant mutualisms result in enhanced biological control via intensified ant predation of important plant-damaging herbivores. In addition, we report the results of our own work involving the ecological consequences of fire ant-aphid mutualisms. We conclude that ant-Hemiptera mutualisms rarely disrupt biological, but instead these mutualisms often increase the effectiveness of ants as biological control agents via the removal of insect herbivores that are more important pests than the Hemipterans that benefit from ant mutualisms.

Forceps Size Does Not Determine Fighting Success in European Earwigs

Male European earwigs (Forficula auricularia) possess substantially larger forceps than females and use these forceps to batter rivals in intrasexual contests to determine dominance. Although previous investigations have shown that male fighting and mating success increases with forceps size, it is not clear that sexual selection acts directly on forceps size per se; increased forceps size may be a correlated response to selection for some other trait. We experimentally reduced forceps length of males and paired them with unmanipulated males in staged encounters. Although apparent (postmanipulation) forceps length did not affect contest outcomes, original (premanipulation) forceps length did: males with longer original forceps won more contests. These results suggest that weapon size itself does not determine success in contests between male European earwigs. Thus, sexual selection may operate on forceps size in some other context or may act on some other trait that covaries with forceps size.

An orb‐weaver spider exploits an ant–acacia mutualism for enemy‐free space

Exploiters of protection mutualisms are assumed to represent an important threat for the stability of those mutualisms, but empirical evidence for the commonness or relevance of exploiters is limited. Here, I describe results from a manipulative study showing that an orb-weaver spider, Eustala oblonga, inhabits an ant-acacia for protection from predators. This spider is unique in the orb-weaver family in that it associates closely with both a specific host plant and ants. I tested the protective effect of acacia ants on E. oblonga by comparing spider abundance over time on acacias with ants and on acacias from which entire ant colonies were experimentally removed. Both juvenile and adult spider abundance significantly decreased over time on acacias without ants. Concomitantly, the combined abundance of potential spider predators increased over time on acacias without ants. These results suggest that ant protection of the ant-acacia Acacia melanocerus also protects the spiders, thus supporting the hypothesis that E. oblonga exploits the ant–acacia mutualism for enemy-free space. Although E. oblonga takes advantage of the protection services of ants, it likely exacts little to no cost and should not threaten the stability of the ant–acacia mutualism. Indeed, the potential threat of exploiter species to protection mutualisms in general may be limited to species that exploit the material rewards traded in such mutualisms rather than the protection services.

An orb-weaver spider eludes plant-defending acacia ants by hiding in plain sight

Myrmecophily is uncommon in spiders and adaptations that allow spider infiltration of ant colonies are poorly studied. Here, a novel interaction between the orb‐weaver spider, Eustala oblonga Chickering, and the acacia ant, Pseudomyrmex satanicus Wheeler, in central Panama is documented. These spiders occupy webs at night, but spend most of the day crouched directly against the surface of their host acacias (Acacia melanocerus Fabaceae) amidst the plant‐defending ants. Detailed behavioural observations indicated that the spiders generally occupied areas on the acacias patrolled more actively by ants, but were attacked only if the spiders moved, which happened very infrequently. We hypothesized, therefore, that the spiders avoid ant aggression behaviourally by being still and not reacting to encounters by patrolling ants. We tested this hypothesis experimentally by comparing ant responses to moving versus immobilised E. oblonga and moving versus immobilised individuals of another plant‐inhabiting, orb‐weaver spider (Argiope argentata Fabricius) not naturally found on ant‐acacias. Consistent with the hypothesis, ants responded significantly more aggressively to moving spiders of both species than to immobilised spiders. Further, moving E. oblonga utilised a particular method of escape in which they suspended themselves on a dragline until ant activity waned before returning to the plant surface and crouching quietly without further agitating the ants. In contrast, moving A. argentata attempted to outrun the ants, thus, continuing to agitate them until the spiders were killed or dropped to the ground. Our results suggest that E. oblonga may be able to inhabit ant‐defended acacias essentially by hiding in plain sight.

FEMALE CONDITION: A PREDICTOR OF HATCHING SYNCHRONY IN THE HOUSE WREN?

Abstract The degree of hatching synchrony in clutches of passerine birds frequently varies among species and among individuals of the same species. Many hypotheses have been proposed to explain why some eggs hatch several days after others in a clutch. We tested one of these hypotheses, the energetic-constraints hypothesis, which proposes that females in poor physical condition postpone initiating incubation and hatch their clutches synchronously, whereas females in good condition begin incubation early and hatch their clutches asynchronously. We tested the hypothesis using the House Wren (Troglodytes aedon) because recent studies have found little difference in productivity between synchronously and asynchronously hatching clutches in this species, suggesting that the degree of hatching synchrony varies for reasons unrelated to nestling growth and survival. We used logistic regression to test the dependence of the degree of hatching synchrony on each of two measures of female condition. We found no relationship between female condition and degree of hatching synchrony. These results and two other lines of evidence are inconsistent with the energetic-constraints hypothesis as an explanation for variation in degree of hatching synchrony in this House Wren population. ¿Predice la Condición de las Hembras la Sincronía de Eclosión en Troglodytes aedon? Resumen. Con frecuencia, el grado de sincronía en la eclosión de nidadas de aves paserinas varía entre especies y entre individuos de la misma especie. Se han propuesto muchas hipótesis para explicar por qué algunos huevos eclosionan varios días después que otros en una misma nidada. Pusimos a prueba una de esas hipótesis, la de las limitaciones energéticas, que propone que hembras en mala condición física postponen el inicio de la incubación y sus nidadas eclosionan sincrónicamente, mientras que aquellas en buena condición inician la incubación temprano y sus nidadas eclosionan asincrónicamente. Pusimos a prueba la hipótesis usando a Troglodytes aedon, pues estudios recientes en esta especie han encontrado pocas diferencias en productividad entre nidadas de eclosión sincrónica y asincrónica, lo que sugiere que el grado de sincronía en la eclosión varía por motivos no relacionados con el crecimiento y supervivencia de los pichones. Utilizamos regresión logística para evaluar el grado de dependencia de la sincronía de eclosión en dos medidas de condición física de las hembras. No encontramos ninguna relación entre la condición de las hembras y el grado de sincronía en la eclosión. Estos resultados y otras dos líneas de evidencia son inconsistentes con la hipótesis de las limitaciones energéticas como una explicación para la variación en el grado de sincronía de eclosión en esta población de T. aedon.