Reproductive strategy: an essential component in the success of incipient colonies of the invasive Argentine ant

Summary: In the last few years, the proximate causes of invasion success in Argentine ants have attracted a lot of interest from behavioral ecologists. Hee et al. (2000) recently showed that small-sized propagules (i.e. queens with as few as 10 workers) can grow quickly, providing insights into the minimum requirements for the establishment of incipient colonies. Here, I stress two complementary factors of the Argentine ant's reproductive strategy that further help explain its success at establishing new populations: (1) the continuous presence of haploid eggs and the ability to produce male and female sexuals throughout the year, and (2) the replacement of mated queens due to intranidal mating. These attributes are important because they make the presence of queens unnecessary for successful propagule establishment in new areas.     

Genetics and behavior of a colonizing species: the invasive Argentine ant

Baker and Stebbins's 1965 book The Genetics of Colonizing Species aimed to draw together scientists from a variety of disciplines to provide a conceptual framework for the study of species introductions. A goal of their volume was to examine how studies on biological invasions could be used to provide insight into basic research questions as well as to develop practical strategies for control. In this article, we attempt to follow the goals of Baker and Stebbins by reviewing work on the genetics and behavior of a widespread colonizing species, the Argentine ant (Linepithema humile). Specifically, we examine the evolutionary changes that have taken place as a result of this species being introduced into new environments and synthesize recent research on Argentine ants from the perspective of population genetics, recognition systems, and the mechanisms that may underlie their ecological success.     

Landscape mulches and termite nutritional ecology: growth and survival of incipient colonies of Coptotermes formosanus (Isoptera: Rhinotermitidae)

Alate swarms are one of the major visible signs of the expansion of the Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), in an area. Successful establishment of an incipient colony is thought to mainly rely on available food resources and moisture. The large-scale use of tree-based mulches in landscapes may inadvertently contribute to local establishment and growth of C. formosanus colonies. This research investigated the nutritional ecology of incipient colonies of C. formosanus feeding on seven tree-based, weathered, and nonweathered landscape mulches: pine straw, pine bark, cedar wood, water oak, eucalyptus, cypress, and melaleuca. Incipient colonies of C. formosanus feeding on pine straw, either weathered or nonweathered, produced significantly more progeny over the course of 1-yr feeding than colonies feeding on the other mulches tested. Regardless of weathered or not, the incipient colonies feeding on pine straw, eucalyptus, bald cypress, and water oak mulches had significantly greater survival rates after 360 d (53-77%) than colonies feeding on the other mulches tested (0-13%), but colonies feeding on nonweathered water oak had significantly lower survival (8%) than those kept on weathered water oak (58%). Colony fitness values were significantly different between the weathering treatment groups and among the different types of mulches. With regard to colony growth characteristics, three distinct growth patterns were identified: a high number of progeny (>100) with high colony survival rate (>50%), a medium number of progeny (12-50) with high colony survival rate (>50%), and a small number of progeny (0-10) with low colony survival rate (<5%). These findings suggest that different types of mulch substrates could significantly impact the nutritional ecology of the founding pairs and the successful establishment of incipient colonies during the swarming season.     

From introduction to equilibrium: reconstructing the invasive pathways of the Argentine ant in a Mediterranean region

Determining the geographical range of invasive species is an important component of formulating effective management strategies. In the absence of detailed distributional data, species distribution models can provide estimates of an invasion range and increase our understanding of the ecological processes acting at various spatial scales. We used two complementary approaches to evaluate the influence of historical and environmental factors in shaping the distribution of the Argentine ant ( Linepithema humile ), a widespread, highly invasive species native to South America. Occurrence data were combined with environmental data at incremental spatial scales (extent and resolution) to predict the suitable range of the ant invasion using ecological niche models. In addition, we also used a spread model that simulated the jump dispersal of the species to identify the most plausible scenarios of arrival of L. humile in the NE Iberian Peninsula at local scales. Based on the results of both modelling practices, we suggest that L. humile might have reached its maximum geographic range at regional scales in the NE Iberian Peninsula. However, the species does not appear in equilibrium with the environment at small spatial scales, and further expansions are expected along coastal and inland localities of the Costa Brava. Long-distance jumps are ultimately responsible for the spread of the Argentine ant in the area. Overall, our study shows the utility of combining niche based models with spread models to understand the dynamics of species' invasions.     

Integrating physiology, population dynamics and climate to make multi-scale predictions for the spread of an invasive insect: the Argentine ant at Haleakala National Park, Hawaii

Mechanistic models for predicting species’ distribution patterns present particular advantages and challenges relative to models developed from statistical correlations between distribution and climate. They can be especially useful for predicting the range of invasive species whose distribution has not yet reached equilibrium. Here, we illustrate how a physiological model of development for the invasive Argentine ant can be connected to differences in micro‐site suitability, population dynamics and climatic gradients; processes operating at quite different spatial scales. Our study is located in the subalpine shrubland of Haleakala National Park, Hawaii, where the spread of Argentine ants Linepithema humile has been documented for the past twenty‐five years. We report four main results. First, at a microsite level, the accumulation of degree‐days recorded in potential ant nest sites under bare ground or rocks was significantly greater than under a groundcover of grassy vegetation. Second, annual degree‐days measured where population boundaries have not expanded (456–521 degree‐days), were just above the developmental requirements identified from earlier laboratory studies (445 degree‐days above 15.9°C). Third, rates of population expansion showed a strong linear relationship with annual degree‐days. Finally, an empirical relationship between soil degree‐days and climate variables mapped at a broader scale predicts the potential for future range expansion of Argentine ants at Haleakala, particularly to the west of the lower colony and the east of the upper colony. Variation in the availability of suitable microsites, driven by changes in vegetation cover and ultimately climate, provide a hierarchical understanding of the distribution of Argentine ants close to their cold‐wet limit of climatic tolerances. We conclude that the integration of physiology, population dynamics and climate mapping holds much promise for making more robust predictions about the potential spread of invasive species.     

Native predator eats invasive toxic prey: evidence for increased incidence of consumption rather than aversion-learning

Contemporary adaptation of native prey species to invasive predators has been relatively well documented, but that of native predators to invasive prey has received less attention. Because the level of impact an invasive species will have on its predators versus its prey will determine changes in community trophic structure, it is important to understand how native predators respond to novel prey. Here we examine the response of native fence lizards to the invasion of red imported fire ants, a novel toxic prey. Examining invaded and uninvaded lizard populations, we tested whether or not aversion-learning occurs in juvenile fence lizards over successive feedings (within lifetime), how previous fire ant exposure may affect avoidance behavior (over generations), and whether population differences are consistent when prey choice exists. We also examine rates of phenotypic divergence in traits associated with the native species as both predator and prey. Aversion-learning did not occur in either population. Instead, the incidence of fire ant consumption increased over both successive feedings and generations. Lizards from the fire ant invaded population had a higher propensity to eat fire ants than fire ant-naïve lizards, even when given a choice between prey items. We found greater phenotypic divergence in traits associated with the native species as predator on, versus as prey to, fire ants. Although the strategy of eating these novel toxic prey can impose survival costs in the short term, over the longer-term, eating fire ants may cost little or even benefit survivors.     

The feeding ecology of the pit-making ant lion larva,Myrmeleon bore: Feeding rate and species composition of prey in a habitat

The prey species composition and feeding rate of the pit-making ant lion larva,Myrmeleon bore Tjeder, which inhabits open sandy areas, were examined. Not less than 30 prey species, most of which were ants, were collected during a research period of 1.5 years. First instar larvae most often (81.1%) captured ants. Although 3rd instar larvae captured larger-sized prey than individuals of any other instar, they also captured small prey. The feeding rate of 3rd instar larvae was estimated by using the frequency of observed predation (FOP; (no. of ant lions handling a prey)/(total no. of pits observed)), the prey-handling time and the rhythm of daily foraging activity. FOP ofM. bore larvae was constant on the whole from spring to autumn. It was estimated that each captured 1.25 prey per day on average during this period. This estimate, however, was the feeding rate for days on which there was no rain. Assuming that the larvae cannot capture prey due to pit destruction when there is more than 10 mm of rainfall per day, the figure was reduced to 1.03 prey/day. The estimated feeding rate was evaluated with reference to larval foraging behavior.     

Genetic and behavioural evidence for a city-wide supercolony of the invasive Argentine ant Linepithema humile (Mayr) (Hymenoptera: Formicidae) in southeastern Australia

The success of invasive ants is frequently attributed to genetic and behavioural shifts in colony structure during or after introduction. The Argentine ant ( Linepithema humile ), a global invader, differs in colony genetic structure and behaviour between native populations in South America and introduced populations in Europe, Japan, New Zealand and North America. However, little is known about its colony structure in Australia. We investigated the genetic structure and behaviour of L. humile across Melbourne, Victoria by quantifying variation at four microsatellite loci and assaying intraspecific aggression at neighbourhood (30–200 m), fine (1–3.3 km) and regional (5–82 km) spatial scales. Hierarchical analyses across these scales revealed that most genetic variation occurred among workers within nests (∼98%). However, although low genetic differentiation occurred among workers between nests at the fine and regional scales (∼2%), negligible differentiation was detected among workers from neighbouring nests. Spatial genetic autocorrelation analysis confirmed that neighbouring nests were genetically more similar to each other. Lack of aggression within and across these scales supported the view that L. humile is unicolonial and forms a large supercolony across Melbourne. Comparisons of genetic structure of L. humile among single nests sampled from Adelaide, Brisbane, Hobart and Perth with Melbourne showed no greater levels of genetic differentiation or dissimilar spatial structure, suggesting an Australia-wide supercolony.     

Towards a synthesis of frameworks in nutritional ecology: interacting effects of protein,carbohydrate and phosphorus on field cricket fitness

Phosphorus has been identified as an important determinant of nutrition-related biological variation. The macronutrients protein (P) and carbohydrates (C), both alone and interactively, are known to affect animal performance. No study, however, has investigated the importance of phosphorus relative to dietary protein or carbohydrates, or the interactive effects of phosphorus with these macronutrients, on fitness-related traits in animals. We used a nutritional geometry framework to address this question in adult field crickets (Gryllus veletis). Our results showed that lifespan, weight gain, acoustic mate signalling and egg production were maximized on diets with different P : C ratios, that phosphorus did not positively affect any of these fitness traits, and that males and females had different optimal macronutrient intake ratios for reproductive performance. When given a choice, crickets selected diets that maximized both lifespan and reproductive performance by preferentially eating diets with low P : C ratios, and females selected diets with a higher P : C ratio than males. Conversely, phosphorus intake was not regulated. Overall, our findings highlight the importance of disentangling the influences of different nutrients, and of quantifying both their individual and interactive effects, on animal fitness traits, so as to gain a more integrative understanding of their nutritional ecology.     

Widespread evidence for incipient ecological speciation: a meta‐analysis of isolation‐by‐ecology

Ecologically mediated selection has increasingly become recognised as an important driver of speciation. The correlation between neutral genetic differentiation and environmental or phenotypic divergence among populations, to which we collectively refer to as isolation‐by‐ecology (IBE), is an indicator of ecological speciation. In a meta‐analysis framework, we determined the strength and commonality of IBE in nature. On the basis of 106 studies, we calculated a mean effect size of IBE with and without controlling for spatial autocorrelation among populations. Effect sizes were 0.34 (95% CI 0.24–0.42) and 0.26 (95% CI 0.13–0.37), respectively, indicating that an average of 5% of the neutral genetic differentiation among populations was explained purely by ecological contrast. Importantly, spatial autocorrelation reduced IBE correlations for environmental variables, but not for phenotypes. Through simulation, we showed how the influence of isolation‐by‐distance and spatial autocorrelation of ecological variables can result in false positives or underestimated correlations if not accounted for in the IBE model. Collectively, this meta‐analysis showed that ecologically induced genetic divergence is pervasive across time‐scales and taxa, and largely independent of the choice of molecular marker. We discuss the importance of these results in the context of adaptation and ecological speciation and suggest future research avenues.     

Scale-area curves: a tool for understanding the ecology and distribution of invasive tree species

Scale-area curves are increasingly used in ecology to predict population trajectories, based on the assumption that observed patterns are indicative of population dynamics. However, for introduced species, scale-area curves might be strongly influenced by introduction history. We examined the spatial structure of an invasive tree species (Acacia elata; Fabaceae) introduced to South Africa as an ornamental plant and compared our findings with previous work done on a species introduced for dune stabilization (A. longifolia). A fractal sampling method was used to map the occupancy of A. elata at twelve spatial scales for ten quarter-degree grid cells throughout South Africa. Based on the fractal dimension (D _ij ) calculated at different spatial scales we found that populations were more contiguous at plot (2.5–25 m) and regional scales (2.5–25 km) than at local and landscape scales (0.025–2.5 km). We argue that the lack of contiguous A. elata populations over 250 m to 2.5 km is not indicative of a low risk, but the result of the spatial structure of available land in suburban environments. When working with introduced species, scale-area curves representing fragmented populations at the edge of invasions should not be considered to indicate a lack of invasive spread/threat. Rather they can be used to identify “missing links” in the invasive introduction-naturalization-invasion continuum, but only if the life-history traits, introduction history, and area suitable for invasion are well understood and are used in interpreting the results. We suggest that their greatest value will lie in their use as a method for long-term monitoring of introduced species.     

Consensual predictions of potential distributional areas for invasive species: a case study of Argentine ants in the Iberian Peninsula

Invasive species are known to influence the structure and function of invaded ecological communities, and preventive measures appear to be the most efficient means of controlling these effects. However, management of biological invasions requires use of adequate tools to understand and predict invasion patterns in recently introduced areas. The present study: (1) estimates the potential geographic distribution and ecological requirements of the Argentine ant (Linepithema humile Mayr), one of the most conspicuous invasive species throughout the world, in the Iberian Peninsula using ecological niche modeling, and (2) provides new insights into the process of selection of consensual areas among predictions from several modeling methodologies. Ecological niche models were developed using 5 modeling techniques: generalized linear models (GLM), generalized additive models (GAM), generalized boosted models (GBM), Genetic Algorithm for Rule-Set Prediction (GARP), and Maximum Entropy (Maxent). Models for the eastern and western portions of the Iberian Peninsula were built using subsets of occurrence and environmental data to investigate the potential for ecological niche differences between the invading populations. Our results indicate geographic differences between predictions of different approaches, and the utility of ensemble predictions in identifying areas of uncertainty regarding the species’ invasive potential. More generally, our models predict coastal areas and major river corridors as highly suitable for Argentine ants, and indicate that western and eastern Iberian Peninsula populations occupy similar environmental conditions.

Carrying capacity models should not use fixed prey density thresholds: a plea for using more tools of behavioural ecology

Earlier studies have developed models of carrying capacity to predict the number of animals a certain area can support. These models assume that resources are not renewed after consumption ('standing stock' models), and that the initial number of prey and the rate of prey consumption determine the time a population of foragers can live in an area. Within such areas, foragers give up feeding at a sub-site or patch when intake rates no longer cover energy expenditure. To improve the success rate of the models' predictions, we here change the existing rate-maximising models into fitness-maximising models, and include dynamics in the availability of patches. These new (conceptual) models show that the approaches used so far may over- as well as underestimate carrying capacity. We review empirical studies that have aimed to estimate carrying capacity, and discuss how concepts have been confused. We make explicit suggestions on how to proceed in predicting carrying capacities in future studies.     

Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue

Starch is made up of amylose (linear alpha-1,4-polyglucans) and amylopectin (alpha-1,6-branched polyglucans). Amylopectin has a distinct fine structure called multiple cluster structure and is synthesized by multiple subunits or isoforms of four classes of enzymes: ADPglucose pyrophosphorylase, soluble starch synthase (SS), starch branching enzyme (BE), and starch debranching enzyme (DBE). In the present paper, based on analyses of mutants and transgenic lines of rice in which each enzyme activity is affected, the contribution of the individual isoform to the fine structure of amylopectin in rice endosperm is evaluated, and a new model referred to as the "two-step branching and improper branch clearing model" is proposed to explain how amylopectin is synthesized. The model emphasizes that two sets of reactions, alpha-1,6-branch formation and the subsequent alpha-1,4-chain elongation, are catalyzed by distinct BE and SS isoforms, respectively, are fundamental to the construction of the cluster structure. The model also assesses the role of DBE, namely isoamylase or in addition pullulanase, to remove unnecessary alpha-1,6-glucosidic linkages that are occasionally formed at improper positions apart from two densely branched regions of the cluster.     

Molecular systematics and ecology of invasive Kangaroo Paws in South Africa: management implications for a horticulturally important genus

Most legislation pertaining to non-native organisms is implicitly focussed at the individual species level. However, in some cases interspecific hybrids can be more invasive than any of the parent species. This is problematic for policy makers, and for horticulturists developing or trading in new ornamental cultivars. We explore these issues in the context of the need to manage naturalized populations of Kangaroo Paws (Anigozanthos species) in South Africa. Self-sustaining, dense populations of naturalized Kangaroo Paws occur at several localities and are highly attractive to local nectar-feeding birds. The populations show high levels of seed set with or without bird pollination. Given the known propensity of Kangaroo Paws to hybridise in their native range in Australia, and confusion about the species identity of naturalized populations in South Africa, it was essential to resolve some key taxonomic issues in the group. We constructed the first molecular phylogeny for all species of the Kangaroo Paw group (genera Anigozanthos and Macropidia; family Haemodoraceae). As previously determined by taxonomists working on herbarium specimens, naturalized populations were identified as A. flavidus. In addition, we also identified a second species, A. rufus. Relative genome size estimates for Anigozanthos species indicated that small inter-specific differences in genome sizes are positively correlated to hybrid fitness. Anigozanthos flavidus and A. rufus have relatively ‘compatible’ genomes and may produce fertile hybrids under field conditions. However, for species whose genome size differ more than ~30%, there is little inter-specific compatibility and consequently a very low risk of producing fertile hybrids. In conclusion, we recommend that trade in Kangaroo Paws in South Africa should be temporarily restricted and that particular cultivars should first be subjected to a careful risk assessment.     

Dermatan is a better substrate for 4-O-sulfation than chondroitin: implications in the generation of 4-O-sulfated, L-iduronate-rich galactosaminoglycans

The biosynthesis of dermatan sulfate is a complex process that involves, inter alia, formation of L-iduronic acid residues by C5-epimerization of D-glucuronic acid residues already incorporated into the growing polymer. It has been shown previously that this reaction is promoted by the presence of the sulfate donor 3'-phosphoadenosine-5'-phosphosulfate. In the present investigation, the role of sulfation in the biosynthesis of L-iduronic acid-rich galactosaminoglycans was examined more closely by a study of the substrate specificities and kinetic properties of the sulfotransferases involved in dermatan sulfate biosynthesis. Comparison of the acceptor reactivities of oligosaccharides from chondroitin and dermatan, in an in vitro system containing microsomes from cultured human skin fibroblasts and 3'-phosphoadenosine-5'-phosphosulfate, showed that Km values for the dermatan fragments were substantially lower than those for their chondroitin counterparts. Calculation of Vmax values likewise showed that dermatan was the better substrate. Whereas dermatan incorporated [35S]sulfate exclusively at the C4 position of N-acetylgalactosamine residues, approximately equal amounts of radioactivity were found at the C4 and C6 positions in the labelled chondroitin. Under standard assay conditions, the 4-O-sulfation of dermatan proceeded about six times faster than the 4-O-sulfation of chondroitin. On the basis of these results, we propose that L-iduronic acids, formed in the course of the biosynthesis of dermatan sulfates, enhance sulfation of their adjacent N-acetylgalactosamine residues, and will thereby be locked in the L-ido configuration.     

Evidence for a quiet revolution: seasonal variation in colonies of the specialist tansy aphid, Macrosiphoniella tanacetaria (Kaltenbach) (Hemiptera: Aphididae) studied using microsatellite markers

In cyclical parthenogens, clonal diversity is expected to decrease due to selection and drift during the asexual phase per number of asexual generations. The decrease in diversity may be counteracted by immigration of new genotypes. We analysed temporal variation in clonal diversity in colonies of the monophagous tansy aphid, Macrosiphoniella tanacetaria (Kaltenbach), sampled four times over the course of a growing season. In a related field study, we recorded aphid colony sizes and the occurrence of winged dispersers throughout the season. The number of colonies increased from April, when asexual stem mothers hatched from the sexually produced eggs, to the end of June. The proportion of colonies with winged individuals also increased over this period. After a severe reduction in colony sizes in late summer, a second expansion phase occurred in October when sexuals were produced. At the season's end, the only winged forms were males. A linked genetic study showed that the number of microsatellite multilocus genotypes and genetic variability assessed at three polymorphic loci per colony decreased from June to October. Overall, the relatedness of wingless to winged individuals within colonies was lower than average relatedness among wingless individuals, suggesting that winged forms mainly originated in different colonies. The results demonstrate that patterns of genetic diversity within colonies can be explained by the antagonistic forces of clonal selection, migration and genetic drift (largely due to midsummer population bottlenecks). We further suggest that the males emigrate over comparatively longer distances than winged asexual females.     

Integral projection models perform better for small demographic data sets than matrix population models: a case study of two perennial herbs

1. Matrix population models are widely used to describe population dynamics, conduct population viability analyses and derive management recommendations for plant populations. For endangered or invasive species, management decisions are often based on small demographic data sets. Hence, there is a need for population models which accurately assess population performance from such small data sets.
2. We used demographic data on two perennial herbs with different life histories to compare the accuracy and precision of the traditional matrix population model and the recently developed integral projection model (IPM) in relation to the amount of data.
3. For large data sets both matrix models and IPMs produced identical estimates of population growth rate (λ). However, for small data sets containing fewer than 300 individuals, IPMs often produced smaller bias and variance for λ than matrix models despite different matrix structures and sampling techniques used to construct the matrix population models.
4. Synthesis and applications . Our results suggest that the smaller bias and variance of λ estimates make IPMs preferable to matrix population models for small demographic data sets with a few hundred individuals. These results are likely to be applicable to a wide range of herbaceous, perennial plant species where demographic fate can be modelled as a function of a continuous state variable such as size. We recommend the use of IPMs to assess population performance and management strategies particularly for endangered or invasive perennial herbs where little demographic data are available.