Azteca ants maintain unique microbiomes across functionally distinct nest chambers.

The microbiome of built structures has considerable influence over an inhabitant's well-being, yet the vast majority of research has focused on human-built structures. Ants are well-known architects, capable of constructing elaborate dwellings, the microbiome of which is underexplored. Here, we explore the bacterial and fungal microbiomes in functionally distinct chambers within and outside the nests of Azteca alfari ants in Cecropia peltata trees. We predicted that A. alfari colonies (1) maintain distinct microbiomes within their nests compared to the surrounding environment, (2) maintain distinct microbiomes among nest chambers used for different functions, and (3) limit both ant and plant pathogens inside their nests. In support of these predictions, we found that internal and external nest sampling locations had distinct microbial communities, and A. alfari maintained lower bacterial richness in their 'nurseries'. While putative animal pathogens were suppressed in chambers that ants actively inhabited, putative plant pathogens were not, which does not support our hypothesis that A. alfari defends its host trees against microbial antagonists. Our results show that ants influence microbial communities inside their nests similar to studies of human homes. Unlike humans, ants limit the bacteria in their nurseries and potentially prevent the build-up of insect-infecting pathogens. These results highlight the importance of documenting how indoor microbiomes differ among species, which might improve our understanding of how to promote indoor health in human dwellings.

Public questions spur the discovery of new bacterial species associated with lignin bioconversion of industrial waste.

A citizen science project found that the greenhouse camel cricket (Diestrammena asynamora) is common in North American homes. Public response was to wonder 'what good are they anyway?' and ecology and evolution guided the search for potential benefit. We predicted that camel crickets and similar household species would likely host bacteria with the ability to degrade recalcitrant carbon compounds. Lignocellulose is particularly relevant as it is difficult to degrade yet is an important feedstock for pulp and paper, chemical and biofuel industries. We screened gut bacteria of greenhouse camel crickets and another household insect, the hide beetle (Dermestes maculatus) for the ability to grow on and degrade lignocellulose components as well as the lignocellulose-derived industrial waste product black liquor. From three greenhouse camel crickets and three hide beetles, 14 bacterial strains were identified that were capable of growth on lignocellulosic components, including lignin. Cedecea lapagei was selected for further study due to growth on most lignocellulose components. The C. lapagei secretome was identified using LC/MS/MS analysis. This work demonstrates a novel source of lignocellulose-degrading bacteria and introduces an effective workflow to identify bacterial enzymes for transforming industrial waste into value-added products. More generally, our research suggests the value of ecologically guided discovery of novel organisms.

Quantifying beetle-macrofungal associations in a temperate biodiversity hot spot.

Beetles (Coleoptera) are often among the most abundant and diverse insects that feed on sporocarps of macrofungi, but little is known regarding their relative specialism or generalism in most communities. We surveyed >9000 sporocarps in montane hardwood forest in the Appalachian Mountains (USA) to characterize associations of mycophagous beetles and macrofungi. We used traditional metrics and network analyses to quantify relationships between sporocarp traits (mass, age, persistence, and toughness) and assemblages of adult beetles, drawing from >50 000 beetles collected over two survey years. Strict-sense specificity was rare in these associations: most beetle species were found on multiple fungal genera, and most fungi hosted multiple beetle species. Sporocarp age and fresh mass were positively associated with beetle diversity in fungi with ephemeral sporocarps (here including 12 genera of Agaricales and Russulales), but sporocarp persistence was not. In Polyporales, beetle diversity was greater in softer sporocarps than in tough or woody sporocarps. The increase of beetle diversity in aging sporocarps could not be attributed to increases in sporocarp mass or sampling point in the growing season, suggesting that age-related changes in chemistry or structure may support increasingly diverse beetle communities. Interaction networks differed as a function of sporocarp age, revealing that community-wide measures of generalism (i.e., network connectance) and evenness (i.e., variance in normalized degree) change as sporocarps mature and senesce. Beetles observed on Agaricales and Russulales with more persistent sporocarps had narrower interaction breadth (i.e., were more host-specific) than those on less persistent sporocarps, and beetles on Polyporales with tougher sporocarps had narrower interaction breadth than those on soft sporocarps. In addition to providing a large-scale evaluation of sporocarp use by adult beetles in this temperate biodiversity hot spot, this study shows that characteristics of food organisms are associated with specialism and generalism in interactions relevant to fungal and forest ecology.

The ecology of insect-yeast relationships and its relevance to human industry.

Many species of yeast are integral to human society. They produce many of our foods, beverages and industrial chemicals, challenge us as pathogens, and provide models for the study of our own biology. However, few species are regularly studied and much of their ecology remains unclear, hindering the development of knowledge that is needed to improve the relationships between humans and yeasts. There is increasing evidence that insects are an essential component of ascomycetous yeast ecology. We propose a 'dispersal-encounter hypothesis' whereby yeasts are dispersed by insects between ephemeral, spatially disparate sugar resources, and insects, in turn, obtain the benefits of an honest signal from yeasts for the sugar resources. We review the relationship between yeasts and insects through three main examples: social wasps, social bees and beetles, with some additional examples from fruit flies. Ultimately, we suggest that over the next decades, consideration of these ecological and evolutionary relationships between insects and yeasts will allow prediction of where new yeast diversity is most likely to be discovered, particularly yeasts with traits of interest to human industry.

Reproduction in Flame Azalea (Rhododendron calendulaceum, Ericaceae): A Rare Case of Insect Wing Pollination.

Although many angiosperms are serviced by flying pollinators, reports of wings as pollen vectors are rare. Flame azalea (Rhododendron calendulaceum) is visited by diverse insects, yet previous observations suggested that only butterfly wings may transfer pollen to stigmas. We used an experimental approach to determine whether butterfly wings are the primary vehicle of pollination in flame azalea. Over two seasons of observations, only butterflies (Papilio glaucus and Speyeria cybele) contacted both anthers and stigmas, yet because of differences in wing-flapping behavior, P. glaucus transferred pollen most efficiently. In contrast, bee species specialized either on pollen or nectar but did not contact both anthers and stigmas. A field experiment revealed that flowers excluding butterflies experienced almost complete fruit failure, whereas fruit set in open flowers did not differ from those that were hand pollinated. Additionally, butterflies had 56-fold more azalea pollen on their wings than bodies, while azalea stigmas bore both pollen and wing scales. These results suggest that plants with many visitors contacting reproductive organs may still specialize on a single guild of visitors for pollination and that wing-borne pollen transfer is a key mode of flame azalea pollination.

Too big to be noticed: cryptic invasion of Asian camel crickets in North American houses.

Despite the rapid expansion of the built environment, we know little about the biology of species living in human-constructed habitats. Camel crickets (Rhaphidophoridae) are commonly observed in North American houses and include a range of native taxa as well as the Asian Diestrammena asynamora (Adelung), a species occasionally reported from houses though considered to be established only in greenhouses. We launched a continental-scale citizen science campaign to better understand the relative distributions and frequency of native and nonnative camel crickets in human homes across North America. Participants contributed survey data about the presence or absence of camel crickets in homes, as well as photographs and specimens of camel crickets allowing us to identify the major genera and/or species in and around houses. Together, these data offer insight into the geographical distribution of camel crickets as a presence in homes, as well as the relative frequency and distribution of native and nonnative camel crickets encountered in houses. In so doing, we show that the exotic Diestrammena asynamora not only has become a common presence in eastern houses, but is found in these environments far more frequently than native camel crickets. Supplemental pitfall trapping along transects in 10 urban yards in Raleigh, NC revealed that D. asynamora can be extremely abundant locally around some homes, with as many as 52 individuals collected from pitfalls in a single yard over two days of sampling. The number of D. asynamora individuals present in a trap was negatively correlated with the trap's distance from a house, suggesting that these insects may be preferentially associated with houses but also are present outside. In addition, we report the establishment in the northeastern United States of a second exotic species, putatively Diestrammena japanica Blatchley, which was previously undocumented in the literature. Our results offer new insight into the relative frequency and distribution of camel crickets living in human homes, and emphasize the importance of the built environment as habitat for two little-known invading species of Orthoptera.

Diversity, abundance and community network structure in sporocarp-associated beetle communities of the central Appalachian Mountains.

Although arthropods are abundant and diverse in and on macrofungal sporocarps, their associations with fungi seldom have been described at a community level. We examined sporocarp-associated beetle communities in two primary sites in the Appalachian Mountains and foothills, assessing beetle diversity and abundance in relation to study site, sampling season (early vs. late summer), and sporocarp characteristics such as taxonomic position, dry mass and age. From 758 sporocarps representing >180 species we recovered 15404 adult beetles representing 72 species and 15 families, primarily Staphylinidae (> 98% of individuals and of 64% morphospecies). The probability of sporocarp colonization by beetles, beetle abundance and diversity differed among fungal species and were positively associated with sporocarp dry mass. Sporocarp age was positively correlated with beetle diversity and abundance (as measured in a focal species, Megacollybia platyphylla, Tricholomataceae), and its effects were independent of dry mass. Many beetle species were generalists, visiting a wide breadth of fungi in both the Agaricales and Polyporales; however, several beetle taxa showed evidence of specialization on particular fungal hosts. Host association data were used to examine the structure underlying sporocarp-beetle associations. Here we present the first evidence of nested community structure in the sporocarp-beetle interaction network.

Food quality, competition, and parasitism influence feeding preference in a neotropical lepidopteran.

We surveyed Lepidoptera found on 11 species of Inga (Fabaceae:Mimosoideae) co-existing on Barro Colorado Island, Panama, to evaluate factors influencing diet choice. Of the 47 species of caterpillars (747 individuals) recorded, each fed on a distinct set of Inga. In the field, 96% of the individuals were found on young leaves. Growth rates of caterpillars that were fed leaves in the laboratory were 60% higher on young leaves compared to mature leaves. When caterpillars were fed leaves of nonhost Inga, they grew more slowly. These data provide support for a link between preference and performance. However, among hosts on which larvae normally occurred, faster growth rates were not associated with greater host electivity (the proportion of larvae found on each host species in the field, corrected for host abundance). Growth rates on normal hosts were positively correlated with leaf expansion rates of the host, and fast expansion was associated with leaves with higher nutritional content. Detailed studies on a gelechiid leaf roller, the species with the largest diet breadth, allowed us to assess the importance of factors other than growth that could influence diet electivity. This species showed a 1.7-fold difference in growth rate among Inga hosts and faster growth on species with fast-expanding leaves. However, there was no correlation between caterpillar growth rate and abundance on different host species. Instead, abundance of the gelechiid on each Inga species was significantly correlated with the temporal predictability of food (synchrony of leaf flushing) and was negatively correlated with competition (amount of leaf area removed by species other than the gelechiid). Although rates of parasitism were high (23-43%), there were no differences among hosts. Parasitism was also not related to measures of escape, such as growth rates of caterpillars, leaf expansion rates, and synchrony of leaf production. Together, food availability, parasitism, and competition explained 84% of the variation in host preference by the gelechiid. We suggest that these ecological interactions may be particularly important in determining diet choice initially and that preferences may be reinforced by subsequent divergence in host chemistry and/or the herbivore's ability to tolerate the secondary metabolites.