Chadwick V. Tillberg

Trophic ecology of invasive Argentine ants in their native and introduced ranges

Although the ecological effects of invasions often become obvious soon after introduced species become established, more gradual effects may take years to manifest and can thus require long-term data for quantification. We analyzed an 8-year record of stable isotope data on Argentine ants (Linepithema humile) from southern California to infer how the trophic position of this widespread invasive species changes over time as native ant species are displaced. We couple this longitudinal analysis with a biregional comparison of stable isotope data (δ15N) on ants from Argentina (native range) and California (introduced range) to quantify (i) how the trophic position of L. humile differs between native and introduced populations, and (ii) how relative trophic position as estimated by δ15N values of Argentine ants compare with those of other ants at the same site. Both long-term and biregional comparisons indicate that the Argentine ants relative trophic position is reduced at sites with a longer history of occupation. Over the course of 8 years, the relative trophic position of L. humile remained high at the leading edge of an invasion front but declined, on average, behind the front as native ants disappeared. Relative to native populations, where L. humile is among the most carnivorous of ants, Argentine ants from California occupied lower trophic positions. These results support the hypothesis that Argentine ants shift their diet after establishment as a result of resource depletion and increasing reliance on plant-based resources, especially honeydew-producing Hemiptera. Our results demonstrate the value of long-term and biregional data in uncovering ecological effects of invasions.

Measuring the trophic ecology of ants using stable isotopes

Abstract.Ants are prominent components of most terrestrial arthropod food webs, yet due to their highly variable diet, the role ants play in arthropod communities can be difficult to resolve. Stable isotope analysis is a promising method for determining the dietary history of an organism, and has the potential to advance our understanding of the food web ecology of social insects. However, some unique characteristics of eusocial organisms can complicate the application of this technique to the study of their trophic ecology. Using stable isotopes of N and C, we investigated levels of intraspecific variation both within and among colonies. We also examined the effect of a common preservation technique on δ15N and δ13C values. We discuss the implications of our results on experimental design and sampling methods for studies using stable isotopes to investigate the trophic ecology of social insects.

An experimental study of competition between fire ants and Argentine ants in their native range.

An understanding of why introduced species achieve ecological success in novel environments often requires information about the factors that limit the abundance of these taxa in their native ranges. Although numerous recent studies have evaluated the importance of natural enemies in this context, relatively few have examined how ecological success may result from differences in the magnitude of interference competition between communities in the native and introduced ranges of nonnative species. Here we examine how native-range competitive environments may relate to invasion success for two important invasive species, the red imported fire ant (Solenopsis invicta) and the Argentine ant (Linepithema humile), in a region of native-range sympatry. At two study sites in northern Argentina, we used stable-isotope analysis, a variety of observational approaches, and two different reciprocal removal experiments to test (1) whether S. invicta competes asymmetrically with L. humile (as suggested by the 20th century pattern of replacement in the southeastern United States) and (2) the extent to which these two species achieve behavioral and numerical dominance. Stable-isotope analysis and activity surveys indicated that S. invicta and L. humile are both omnivores and forage during broadly overlapping portions of the diel cycle. Short-term removal experiments at baits revealed no competitive asymmetry between S. invicta and L. humile. Longer-term colony removal experiments illustrated that S. invicta and L. humile experience an approximately equal competitive release upon removal of the other. Our results indicate that neither S. invicta nor L. humile achieves the same degree of behavioral or ecological dominance where they co-occur in native populations as they do in areas where either is common in their introduced range. These results strongly suggest that interspecific competition is an important limiting factor for both S. invicta and L. humile in South America.

Caste Determination in a Polymorphic Social Insect: Nutritional, Social, and Genetic Factors

We examined how dietary, social, and genetic factors affect individual size and caste in the Florida harvester ant Pogonomyrmex badius, which has three discrete female castes. The diet that a larva consumed, as indicated by δ13C, δ15N, and C:N, varied with caste. Both N content and estimated trophic position of dietary input was higher for major than for minor workers and was highest for gynes (reproductive females). The size and resources of a colony affected the size of only minor workers, not that of gynes and major workers. Approximately 19% of patrilines showed a bias in which female caste they produced. There were significant genetic effects on female size, and the average sizes of a major worker and a gyne produced by a patriline were correlated, but neither was correlated with minor worker size. Thus, genetic factors influence both caste and size within caste. We conclude that environmental, social, and genetic variation interact to create morphological and physiological variation among females in P. badius. However, the relative importance of each type of factor affecting caste determination is caste specific.

TEMPORAL AND SPATIAL VARIATION TO ANT OMNIVORY IN PINE FORESTS

To understand omnivore function in food webs, we must know the contributions of resources from different trophic levels and how resource use changes through space and time. We investigated the spatial and temporal dynamics of pine (Pinus ponderosa) food webs that included the omnivorous ant, Formica podzolica, using direct observation and stable isotopes. Formica podzolica is a predator of herbivorous and predatory arthropods, and a mutualist with some aphids. Observations in 2001 of foragers showed that in early summer (June) ants fed upon equal parts non-mutualist herbivores (31% prey biomass), mutualist aphids (27%), and predators (42%); ant trophic position was thus between that of primary and secondary predator (trophic level = 3.4). In late summer (September), ant feeding remained relatively constant upon non-mutualist herbivores (53%) and mutualist aphids (43%), but ant feeding upon predators fell (4%), thus shifting ant trophic position to that of a primary predator (trophic level = 3.0). Feeding ...

Friend or foe? A behavioral and stable isotopic investigation of an ant–plant symbiosis

In ant–plant symbioses, the behavior of ant inhabitants affects the nature of the interaction, ranging from mutualism to parasitism. Mutualistic species confer a benefit to the plant, while parasites reap the benefits of the interaction without reciprocating, potentially resulting in a negative impact on the host plant. Using the ant–plant symbiosis between Cordia alliodora and its ant inhabitants as a model system, I examine the costs and benefits of habitation by the four most common ant inhabitants at La Selva Biological Station, Costa Rica. Costs are measured by counting coccoids associated with each ant species. Benefits include patrolling behavior, effectiveness at locating resources, and recruitment response. I also compare the diets of the four ant species using stable isotope analysis of nitrogen (N) and carbon (C). Ants varied in their rates of association with coccoids, performance of beneficial behaviors, and diet. These differences in cost, benefit, and diet among the ant species suggest differences in the nature of the symbiotic relationship between C. alliodora and its ants. Two of the ant species behave in a mutualistic manner, while the other two ant species appear to be parasites of the mutualism. I determined that the mutualistic ants feed at a higher trophic level than the parasitic ants. Behavioral and dietary evidence indicate the protective role of the mutualists, and suggest that the parasitic ants do not protect the plant by consuming herbivores.

Contrasting effects of an invasive ant on a native and an invasive plant

When invasive species establish in new environments, they may disrupt existing or create new interactions with resident species. Understanding of the functioning of invaded ecosystems will benefit from careful investigation of resulting species-level interactions. We manipulated ant visitation to compare how invasive ant mutualisms affect two common plants, one native and one invasive, on a sub-tropical Indian Ocean island. Technomyrmex albipes, an introduced species, was the most common and abundant ant visitor to the plants. T. albipes were attracted to extrafloral nectaries on the invasive tree (Leucaenaleucocephala) and deterred the plant’s primary herbivore, the Leucaena psyllid (Heteropsylla cubana). Ant exclusion from L. leucocephala resulted in decreased plant growth and seed production by 22% and 35%, respectively. In contrast, on the native shrub (Scaevola taccada), T. albipes frequently tended sap-sucking hemipterans, and ant exclusion resulted in 30% and 23% increases in growth and fruit production, respectively. Stable isotope analysis confirmed the more predacious and herbivorous diets of T. albipes on the invasive and native plants, respectively. Thus the ants’ interactions protect the invasive plant from its main herbivore while also exacerbating the effects of herbivores on the native plant. Ultimately, the negative effects on the native plant and positive effects on the invasive plant may work in concert to facilitate invasion by the invasive plant. Our findings underscore the importance of investigating facilitative interactions in a community context and the multiple and diverse interactions shaping novel ecosystems.

Nutritional asymmetries are related to division of labor in a queenless ant.

Eusocial species exhibit pronounced division of labor, most notably between reproductive and non-reproductive castes, but also within non-reproductive castes via morphological specialization and temporal polyethism. For species with distinct worker and queen castes, age-related differences in behavior among workers (e.g. within-nest tasks versus foraging) appear to result from physiological changes such as decreased lipid content. However, we know little about how labor is divided among individuals in species that lack a distinct queen caste. In this study, we investigated how fat storage varied among individuals in a species of ant (Dinoponera australis) that lacks a distinct queen caste and in which all individuals are morphologically similar and capable of reproduction (totipotent at birth). We distinguish between two hypotheses, 1) all individuals are physiologically similar, consistent with the possibility that any non-reproductive may eventually become reproductive, and 2) non-reproductive individuals vary in stored fat, similar to highly eusocial species, where depletion is associated with foraging and non-reproductives have lower lipid stores than reproducing individuals. Our data support the latter hypothesis. Location in the nest, the probability of foraging, and foraging effort, were all associated with decreased fat storage.

Abiotic mediation of a mutualism drives herbivore abundance.

Species abundance is typically determined by the abiotic environment, but the extent to which such effects occur through the mediation of biotic interactions, including mutualisms, is unknown. We explored how light environment (open meadow vs. shaded understory) mediates the abundance and ant tending of the aphid Aphis helianthi feeding on the herb Ligusticum porteri. Yearly surveys consistently found aphids to be more than 17-fold more abundant on open meadow plants than on shaded understory plants. Manipulations demonstrated that this abundance pattern was not due to the direct effects of light environment on aphid performance, or indirectly through host plant quality or the effects of predators. Instead, open meadows had higher ant abundance and per capita rates of aphid tending and, accordingly, ants increased aphid population growth in meadow but not understory environments. The abiotic environment thus drives the abundance of this herbivore exclusively through the mediation of a protection mutualism.

Stable isotope and elemental analysis in ants.

Over the past 20 yr, the use of stable isotopes to infer feeding ecology and the examination of how energetic and elemental exchanges are affected by and affect life (ecological stoichiometry) have gained momentum. The ecological diversity of ants makes them interesting models to explore dietary ecology and their role in food webs. Moreover, their ecological dominance in most habitats facilitates sampling. The protocol described here will produce samples adequate for submission to most labs that specialize in high-throughput analysis of stable isotopes; one should check with any particular lab for specific submission instructions. Note, however, that this protocol is designed specifically for the quantification of the natural abundance of stable isotopes; it does not cover the preparation of trace samples.