Crisanto Gómez

Relative roles of climatic suitability and anthropogenic influence in determining the pattern of spread in a global invader

Because invasive species threaten the integrity of natural ecosystems, a major goal in ecology is to develop predictive models to determine which species may become widespread and where they may invade. Indeed, considerable progress has been made in understanding the factors that influence the local pattern of spread for specific invaders and the factors that are correlated with the number of introduced species that have become established in a given region. However, few studies have examined the relative importance of multiple drivers of invasion success for widespread species at global scales. Here, we use a dataset of >5,000 presence/absence records to examine the interplay between climatic suitability, biotic resistance by native taxa, human-aided dispersal, and human modification of habitats, in shaping the distribution of one of the worlds most notorious invasive species, the Argentine ant (Linepithema humile). Climatic suitability and the extent of human modification of habitats are primarily responsible for the distribution of this global invader. However, we also found some evidence for biotic resistance by native communities. Somewhat surprisingly, and despite the often cited importance of propagule pressure as a crucial driver of invasions, metrics of the magnitude of international traded commodities among countries were not related to global distribution patterns. Together, our analyses on the global-scale distribution of this invasive species provide strong evidence for the interplay of biotic and abiotic determinants of spread and also highlight the challenges of limiting the spread and subsequent impact of highly invasive species.

Structure of ground-foraging ant assemblages in relation to land-use change in the northwestern Mediterranean region

The abandonment by humans of marginal and less productive zones signifies an important change in land use in North Mediterranean agroecosystems. Human perturbations have led to a highly diversified landscape, with a mosaic made up of patches of land at different stages of succession, from cultivated fields to closed forest. Our aim here is to characterize ant assemblages and their functional groups in response to these land-use changes. This progressive abandonment results in an initial increase in ant richness and abundance, which can reach high levels if the succession proceeds as far as woodland. In terms of the ant functional groups, this land-use change implies: (1) the appearance of Subordinate Camponotini; (2) an increase in Generalized Myrmicinae, Cryptics and Cold-climate specialists in terms of ant species richness, overall abundance and, for Generalized Myrmicinae and Cryptics, an increase in abundance percentage; (3) a decrease in percentage abundance of Opportunists; (4) a progressive decrease in species richness as well as overall and percentage abundance of Hot-climate Specialists throughout the transformation from crops to woodlands; and (5) an initial increase of Dominant Dolichoderinae followed by a decrease in ant species richness, overall abundance and percentage abundance. Using the ant functional group approach for the clearly separate stages of the regeneration process is a promising method for comparing responses of ant communities to human land use.

Can the Argentine ant (Linepithema humile Mayr) replace native ants in myrmecochory

We analyse the influence of the Argentine ant ( Linepithema humileMayr) on the seed dispersal process of the myrmecochorous plants Euphorbia characias, E. biumbellata, Genista linifolia, G. triflora, G. monspessulana and Sarothamnus arboreus. The observations were made in two study plots of Mediterranean cork-oak secondary forest (invaded and non-invaded by L. humile). The presence of L. humile implies the displacement of all native ant species that disperse seeds. Seed transports in the non-invaded zone were carried out by eight ant species. In the invaded zone, L. humile workers removed and transported seeds to the nest. In vertebrate exclusion trials, we observed the same level of seed removal in the invaded and non-invaded zones. Two findings could explain this result. Although mean time to seed localization was higher for native ants (431.7 s) than that for L. humile (150.5 s), the mean proportion of seeds transported after being detected was higher (50.1%) in non-invaded than in invaded (16.8%) zones. The proportion of seeds removed and transported into an ant nest after an ant-seed interaction had dramatically reduced from non-invaded (41.9%) to invaded (7.4%) zones. The levels of seed dispersal by ants found prior to invasion are unlikely to be maintained in invaded zones. However, total replacement of seed dispersal function is possible if contact iteration finally offers similar levels or quantities of seeds reaching the nests. The results obtained confirm that the Argentine ant invasion may affect myrmecochory dramatically in the Mediterranean biome.

Seed dispersal curve of a Mediterranean myrmecochore: Influence of ant size and the distance to nests

Euphorbia characias is a Mediterranean spurge with a diplochorous dispersal system: after a ballistic dispersal that scatters the seeds, some ant species find and retrieve the seeds to their nest (myrmecochorous dispersal). The seed dispersal curve generated by ants in an abandoned field was described and partitioned according to ant size and to the distance to nest entrance from where seeds fell after ballistic dispersal. Both variables (ant size, distance to nest) affected dispersal distance. The seed dispersal curve showed a peak at short distance (median = 1 m) and a tail extending to 9.4 m. The peak and the tail are explained differently. Short distances are usually generated by small ants (Pheidole pallidula and Tapinoma nigerrimum; 0.56 ± 0.41 m [n = 48]) both from the nearest or farther nest entrances. The tail of the curve is generated disproportionately by big ants (Aphaenogaster senilis and Messor barbarus; 2.09 ± 1.71 m [n = 61]) from farther nests. Seeds have a much greater probability (P = 0.734) of being transported to nests which are not the nearest. This effect is largely due to transportation by big ants.

Foraging Activity and Dietary Spectrum of the Argentine Ant (Hymenoptera: Formicidae) in Invaded Natural Areas of the Northeast Iberian Peninsula

Abstract We analyzed the foraging activity and the dietary spectrum of the Argentine ant (Linepithema humile Mayr) and select native ants on cork oaks from Mediterranean open cork oak (Quercus suber) secondary forests. The study areas included invaded and noninvaded zones in close proximity. The Argentine ant’s daily foraging activity was correlated to the abiotic factors studied, whereas the seasonal foraging activity was related not only to the variations in the average air temperature, but also to the trophic needs of the colony. Argentine ant workers focused their attention on protein foods during the queens’ oviposition periods and during the larvae development phase, and on carbohydrate foods, such as honeydew, when males and workers were hatching. There were no significant differences over the entire year in the quantity of liquid food collected by the Argentine ant workers in comparison with the native ants studied. The solid diet of the Argentine ant on cork oaks is composed of insects, most of which are aphids. Our results have clear applications for control methods based on toxic baits in the invaded natural ecosystems of the Iberian Peninsula.

Ant behaviour and seed morphology: a missing link of myrmecochory

Seed dispersal by ants (myrmecochory) is mediated by the presence of a lipid-rich appendage (elaiosome) on the seed that induces a variety of ants to collect the diaspores. When seeds mature or fall onto the ground, these ant species transport them to their nest. After eating the elaiosome, the seed is discarded in nest galleries or outside, in the midden or farther away, where seeds can potentially germinate. The final location of seeds with their elaiosomes removed was evaluated to assess the importance of possible handles (structures that ants can grasp to carry) in transporting ants during re-dispersal experiments of seeds from nests of six species of ants. The results indicate that seeds remained within the nest because the ants were not able to transport them out of the nest. As a consequence of the elaiosome being removed, small ant species could not take Euphorbia characias seeds out of their nests. Only large ant species could remove E. characias seeds from their nests. Attaching an artificial handle to E. characias seeds allowed small ant species to redistribute the seeds from their nests. On the other hand, Rhamnus alaternus seeds that have a natural handle after the elaiosome removal were removed from the nests by both groups of ant species. If a seed has an element that acts as a handle, it will eventually get taken out of the nest. The ants’ size and their mandible gap can determine the outcome of the interaction (i.e. the pattern of the final seed shadow) and as a consequence, could influence the events that take place after the dispersal process.

Effect of temperature on the development and survival of the Argentine ant, Linepithema humile.

Abstract The influence of temperature on the developmental times and survival of insects can largely determine their distribution. For invasive species, like the Argentine ant, Linepithema humile Mayr (Hymenoptera: Formicidae), these data are essential for predicting their potential range based on mechanistic models. In the case of this species, such data are too scarce and incomplete to make accurate predictions based on its physiological needs. This research provides comprehensive new data about brood survival and developmental times at a wide range of temperatures under laboratory conditions. Temperature affected both the complete brood development from egg to adult worker and each of the immature stages separately. The higher the temperature, the shorter the development times. Brood survival from egg to adult was low, with the maximum survival rate being only 16% at 26° C. Temperature also affected survival of each of the immature stages differently: eggs were negatively affected by high temperatures, while larvae were negatively affected by low temperatures, and the survival of pupae was apparently independent of environmental temperature. At 32° C no eggs survived, while at 18° C less than 2% of the eggs hatched into larva. The data from the present study are essential for developing prediction models about the distribution range of this tramp species based on its physiological needs in relation to temperature.

Comparative transcriptomics reveals the conserved building blocks involved in parallel evolution of diverse phenotypic traits in ants.

Background Reproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes. Queen and worker phenotypes play major roles in the evolution of eusocial insects. Their behavior, morphology and physiology underpin many ecologically relevant colony-level traits, which evolved in parallel in multiple species. Results Using queen and worker transcriptomic data from 16 ant species we tested the hypothesis that conserved sets of genes are involved in ant reproductive division of labor. We further hypothesized that such sets of genes should also be involved in the parallel evolution of other key traits. We applied weighted gene co-expression network analysis, which clusters co-expressed genes into modules, whose expression levels can be summarized by their ‘eigengenes’. Eigengenes of most modules were correlated with phenotypic differentiation between queens and workers. Furthermore, eigengenes of some modules were correlated with repeated evolution of key phenotypes such as complete worker sterility, the number of queens per colony, and even invasiveness. Finally, connectivity and expression levels of genes within the co-expressed network were strongly associated with the strength of selection. Although caste-associated sets of genes evolve faster than non-caste-associated, we found no evidence for queen- or worker-associated co-expressed genes evolving faster than one another. Conclusions These results identify conserved functionally important genomic units that likely serve as building blocks of phenotypic innovation, and allow the remarkable breadth of parallel evolution seen in ants, and possibly other eusocial insects as well. Electronic supplementary material The online version of this article (doi:10.1186/s13059-016-0902-7) contains supplementary material, which is available to authorized users.BackgroundReproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes. Queen and worker phenotypes play major roles in the evolution of eusocial insects. Their behavior, morphology and physiology underpin many ecologically relevant colony-level traits, which evolved in parallel in multiple species.ResultsUsing queen and worker transcriptomic data from 16 ant species we tested the hypothesis that conserved sets of genes are involved in ant reproductive division of labor. We further hypothesized that such sets of genes should also be involved in the parallel evolution of other key traits. We applied weighted gene co-expression network analysis, which clusters co-expressed genes into modules, whose expression levels can be summarized by their ‘eigengenes’. Eigengenes of most modules were correlated with phenotypic differentiation between queens and workers. Furthermore, eigengenes of some modules were correlated with repeated evolution of key phenotypes such as complete worker sterility, the number of queens per colony, and even invasiveness. Finally, connectivity and expression levels of genes within the co-expressed network were strongly associated with the strength of selection. Although caste-associated sets of genes evolve faster than non-caste-associated, we found no evidence for queen- or worker-associated co-expressed genes evolving faster than one another.ConclusionsThese results identify conserved functionally important genomic units that likely serve as building blocks of phenotypic innovation, and allow the remarkable breadth of parallel evolution seen in ants, and possibly other eusocial insects as well.

Soil surface searching and transport of Euphorbia characias seeds by ants

Abstract The intensity of exploring the soil surface by ants was studied for the four species involved in the dispersal and predation of seeds of the West-Mediterranean myrmecochorous plant Euphorbia characias. During the dehiscence period (June) the whole soil surface is sccanned in 43 minutes. Not all ants that find a seed take it to the nest. For the four ant species studied (Pheidole pallidula, Aphaenogaster senilis, Tapinoma nigerrimum, Messor barbarus) the proportion of ants that finally take the seed is 67.6%. In spite of this, the high level of soil surface searching explains the rather short time that seeds remain on the soil before being removed. The presence of an elaiosome is a key element in the outcome of the ant-seed interaction: a seed with elaiosome has a seven-fold increase in probability of being taken to the nest if found by a non-granivorous ant. The predator-avoidance hypothesis for myrmecochory is supported.

Exclusive frugivory and seed dispersal of Rhamnus alaternus in the bird breeding season

We studied avian frugivory and seed dispersal in a dioecious shrub, Rhamnus alaternus, focusing on the quantitative and qualitative components of effectiveness. The study took place at three locations in the northeast of the Iberian Peninsula, and examined bird behaviour, intensity of feeding, and the consequences for seedling emergence. The coincidence between the bird breeding season and fruit ripening of R. alaternus in the absence of other ripe fruit, generates a monospecific interaction. The extant frugivorous species were mainly legitimate seed dispersers and their abundance was low. Sylvia melanocephala and S. undata were the most important at one site whereas S. atricapilla, Erithacus rubecula and Turdus merula predominated at the other two sites. Fruit handling took place directly on the branches. Bird species used microhabitats differently as first post-feeding perch, which usually was a short distance away. The low density of frugivorous birds in all localities, among others factors, resulted in satiation of the disperser community and many mature fruits unconsumed. Both adults and juveniles feed upon the plants and their foraging patterns are similar. Adults of S. melanocephala were observed to feed fruit to nestlings and consequently a second phase of dispersal potentially arises from the transport of fecal sacs. Pulp removal and passage through the digestive tract increased the probability of seedling emergence. This plant-dispersal interaction has important consequences, both positive and negative for the plant. Positively, the fruiting of R. alaternus at a time when other ripe fruits are not available avoids interspecific competition for seed dispersers. In addition, a low density of seed rain may reduce intraspecific competition. Negatively, the low density and small size of the breeding frugivorous bird community limit fruit handling and removal away from the parent plants, while the territorial behaviour of birds at that time of the year reduces the potential distances of seed dispersal.