Friend or Foe? Orb-Weaver Spiders Inhabiting Ant–Acacias Capture Both Herbivorous Insects and Acacia Ant Alates

The orb-weaver spiders Eustala oblonga (Chickering) and Eustala illicita (O. Picard-Cambridge) (Araneae: Araneidae) inhabit the ant-defended acacias Vachellia melanocerus (Beurling) and Vachellia collinsii (Safford) (Fabales: Fabaceae), respectively, in Panama. These spiders do not capture patrolling Pseudomyrmex ants but exploit their plant-protection services to escape predation. What effect the spiders have on the ant-acacia mutualisms is unknown. They may provide an additional layer of plant defense by capturing flying herbivorous insects in their webs. Alternatively, the spiders may disrupt the ant–acacia mutualisms by capturing alate acacia ants during nuptial flights. We evaluated these two hypotheses by sampling insects flying through acacia foliage and by identifying prey remains in webs. The proportions of insects captured on sticky card traps and in webs varied with taxonomic order and ecological role. Herbivorous insects greatly outnumbered other groups captured on sticky cards and were captured in spiders’ webs in both acacia species but made up a minority of prey remains in webs. Instead, insect predators and parasitoids made up the majority of prey remains and were comprised primarily by alate ant mutualists of the host acacias. These results provide indirect support for both hypotheses and suggest that the spiders potentially both benefit and harm their host ant-acacia mutualisms. The net effect of spider exploitation, however, is unclear and is likely based on both the effectiveness of plant protection from herbivory provided by the spiders relative to that provided by acacia ants, as well as the overall proportion of the ant reproductive caste the spiders actually capture.

Mutualistic acacia-ants show that specialized bacteria are not required for the evolution of herbivory

Acacia-ant mutualists in the genus Pseudomyrmex nest obligately in acacia plants and, through stable isotope analysis, we show that they are among the strictest of herbivores, feeding exclusively from their hosts. The diets of herbivorous insects such as these are often enriched by obligate bacterial endosymbionts through nitrogen recycling and even gaseous di-nitrogen fixation. We, therefore, examine the bacterial communities associated with mutualistic acacia-ants, comparing them with related non-mutualists in order to determine whether they host bacterial partners likely to contribute to the enrichment of their diets. However, despite their low trophic position, we find no evidence for bacteria-assisted nutrition in either adults or larvae. These acacia-ants do not host any species- or clade-specific bacteria, though several lineages of acetic acid bacteria present across social insects do differ in abundance between mutualists and non-mutualists, likely in response to the sugar-rich diets of their hosts. In addition, two novel lineages of Actinomycetales inhabit both mutualistic and non-mutualistic Pseudomyrmex and differ in abundance between the juveniles of these groups, potentially serving as defensive symbionts. Metagenomic sequencing of these taxa reveal substantial capacity for the production of defensive chemicals. Overall, we find little evidence for nutrition-associated bacteria in these strictly herbivorous ants, showing that bacteria are not as essential to animal nutrition as is often hypothesized.

The acacia ants revisited: convergent evolution and biogeographic context in an iconic ant/plant mutualism

Phylogenetic and biogeographic analyses can enhance our understanding of multispecies interactions by placing the origin and evolution of such interactions in a temporal and geographical context. We use a phylogenomic approach—ultraconserved element sequence capture—to investigate the evolutionary history of an iconic multispecies mutualism: Neotropical acacia ants ( Pseudomyrmex ferrugineus group) and their associated Vachellia hostplants. In this system, the ants receive shelter and food from the host plant, and they aggressively defend the plant against herbivores and competing plants. We confirm the existence of two separate lineages of obligate acacia ants that convergently occupied Vachellia and evolved plant-protecting behaviour, from timid ancestors inhabiting dead twigs in rainforest. The more diverse of the two clades is inferred to have arisen in the Late Miocene in northern Mesoamerica, and subsequently expanded its range throughout much of Central America. The other lineage is estimated to have originated in southern Mesoamerica about 3 Myr later, apparently piggy-backing on the pre-existing mutualism. Initiation of the Pseudomyrmex / Vachellia interaction involved a shift in the ants from closed to open habitats, into an environment with more intense plant herbivory. Comparative studies of the two lineages of mutualists should provide insight into the essential features binding this mutualism.

A review of the Pseudomyrmex ferrugineus and Pseudomyrmex goeldii species groups: acacia-ants and relatives (Hymenoptera: Formicidae)

The Pseudomyrmex ferrugineus group contains the Mesoamerican acacia-ants, an assemblage of species that inhabit and protect swollen-thorn acacias (Vachellia spp.). Recent phylogenetic studies have confirmed the existence of two generalist (dead twig-inhabiting) species that are embedded within the P. ferrugineus group. They are described here as P. evitus sp. nov. (occurring from Mexico to Costa Rica) and P. feralis sp. nov. (Guatemala). The morphological definition of the P. ferrugineus group is revised to incorporate additional variability in the worker and queen castes. The previous diagnosis of the males, based largely on features of the genitalia, requires little revision. Closely related to the P. ferrugineus group is a clade of five predominantly South American species, here designated and diagnosed as the P. goeldii group. The five species, P. goeldii (Forel), P. laevifrons Ward, P. micans sp. nov., P. obtusus sp. nov., and P. parvulus sp. nov., are characterized and illustrated. P. laevifrons and P. micans are closely related and difficult to distinguish, possibly reflecting incomplete isolation. Keys are provided for the identification of the species in both groups.