Helena Wirta

Complementary molecular information changes our perception of food web structure

Significance Understanding the interaction structure of ecological assemblages is the basis for understanding how they vary in space and time. To reconstruct interactions in the High Arctic, we draw on three sources of information: two based on DNA sequence data and one on the rearing of parasitoids from their hosts. Overall, we show that a combination of all three techniques will not only provide high resolution for describing feeding associations among individual species, but also revamp our view of the overall structure of the target network. Thus, our findings suggest that combining several types of information will fundamentally change our impression of both how local interaction webs are structured, and how biotic interactions are patterned across the globe. How networks of ecological interactions are structured has a major impact on their functioning. However, accurately resolving both the nodes of the webs and the links between them is fraught with difficulties. We ask whether the new resolution conferred by molecular information changes perceptions of network structure. To probe a network of antagonistic interactions in the High Arctic, we use two complementary sources of molecular data: parasitoid DNA sequenced from the tissues of their hosts and host DNA sequenced from the gut of adult parasitoids. The information added by molecular analysis radically changes the properties of interaction structure. Overall, three times as many interaction types were revealed by combining molecular information from parasitoids and hosts with rearing data, versus rearing data alone. At the species level, our results alter the perceived host specificity of parasitoids, the parasitoid load of host species, and the web-wide role of predators with a cryptic lifestyle. As the northernmost network of host–parasitoid interactions quantified, our data point exerts high leverage on global comparisons of food web structure. However, how we view its structure will depend on what information we use: compared with variation among networks quantified at other sites, the properties of our web vary as much or much more depending on the techniques used to reconstruct it. We thus urge ecologists to combine multiple pieces of evidence in assessing the structure of interaction webs, and suggest that current perceptions of interaction structure may be strongly affected by the methods used to construct them.

An old adaptive radiation of forest dung beetles in Madagascar

Adaptive radiations of mammals have contributed to the exceptionally high levels of biodiversity and endemism in Madagascar. Here we examine the evolutionary history of the endemic dung beetle tribe Helictopleurini (Scarabaeidae) and its relationship to the widely distributed Oniticellini and Onthophagini. Helictopleurini species are dependent on mammals for their resources. We date the single origin of the tribe at 37 to 23 MY ago, indicating overseas colonization of Madagascar. The main radiation occurred concurrently with the main radiations of lemurs. The ancestors of Helictopleurini are inferred to have been coprophagous species inhabiting open habitats. Subsequent evolution has involved a shift into forests, changes in resource use to a more generalized diet, and changes in body size. Four species of the extant 65 species have shifted to use the dung of the recently introduced cattle in open habitats, allowing these species to greatly expand their geographical ranges.

Exposing the structure of an Arctic food web.

How food webs are structured has major implications for their stability and dynamics. While poorly studied to date, arctic food webs are commonly assumed to be simple in structure, with few links per species. If this is the case, then different parts of the web may be weakly connected to each other, with populations and species united by only a low number of links. We provide the first highly resolved description of trophic link structure for a large part of a high-arctic food web. For this purpose, we apply a combination of recent techniques to describing the links between three predator guilds (insectivorous birds, spiders, and lepidopteran parasitoids) and their two dominant prey orders (Diptera and Lepidoptera). The resultant web shows a dense link structure and no compartmentalization or modularity across the three predator guilds. Thus, both individual predators and predator guilds tap heavily into the prey community of each other, offering versatile scope for indirect interactions across different parts of the web. The current description of a first but single arctic web may serve as a benchmark toward which to gauge future webs resolved by similar techniques. Targeting an unusual breadth of predator guilds, and relying on techniques with a high resolution, it suggests that species in this web are closely connected. Thus, our findings call for similar explorations of link structure across multiple guilds in both arctic and other webs. From an applied perspective, our description of an arctic web suggests new avenues for understanding how arctic food webs are built and function and of how they respond to current climate change. It suggests that to comprehend the community-level consequences of rapid arctic warming, we should turn from analyses of populations, population pairs, and isolated predator–prey interactions to considering the full set of interacting species.

Establishing a community‐wide DNA barcode library as a new tool for arctic research

DNA sequences offer powerful tools for describing the members and interactions of natural communities. In this study, we establish the to‐date most comprehensive library of DNA barcodes for a terrestrial site, including all known macroscopic animals and vascular plants of an intensively studied area of the High Arctic, the Zackenberg Valley in Northeast Greenland. To demonstrate its utility, we apply the library to identify nearly 20 000 arthropod individuals from two Malaise traps, each operated for two summers. Drawing on this material, we estimate the coverage of previous morphology‐based species inventories, derive a snapshot of faunal turnover in space and time and describe the abundance and phenology of species in the rapidly changing arctic environment. Overall, 403 terrestrial animal and 160 vascular plant species were recorded by morphology‐based techniques. DNA barcodes (CO1) offered high resolution in discriminating among the local animal taxa, with 92% of morphologically distinguishable taxa assigned to unique Barcode Index Numbers (BINs) and 93% to monophyletic clusters. For vascular plants, resolution was lower, with 54% of species forming monophyletic clusters based on barcode regions rbcLa and ITS2. Malaise catches revealed 122 BINs not detected by previous sampling and DNA barcoding. The insect community was dominated by a few highly abundant taxa. Even closely related taxa differed in phenology, emphasizing the need for species‐level resolution when describing ongoing shifts in arctic communities and ecosystems. The DNA barcode library now established for Zackenberg offers new scope for such explorations, and for the detailed dissection of interspecific interactions throughout the community.

Three parallel radiations of Canthonini dung beetles in Madagascar.

Madagascar has an exceptionally large fauna of more than 250 species of endemic dung beetles. Based on molecular phylogenies, the species descend from eight independent overseas colonisations, of which four have given rise to big radiations. Here, we analyse the tribe Canthonini with three parallel radiations following the respective colonisations at 64-44 Mya (Arachnodes-Epilissus, 101 species), 30-19 Mya (Epactoides, 37 species), and 24-15 Mya (Apotolamprus-Nanos, 61 species). All three radiations have taken place in forests, but there are also substantial differences between them. The oldest radiation exhibits the greatest ecological diversification, including monophyletic groups of primate and cattle dung specialists and multiple shifts to arboreal foraging. Analysis of pairs of sister species suggests allopatric speciation in the oldest and the youngest, apparently non-adaptive, radiations, whereas in Epactoides closely related species have diverged ecologically and have largely overlapping geographical ranges, suggestive of adaptive radiation in parapatry or regional sympatry.

Indirect interactions in the High Arctic

Indirect interactions as mediated by higher and lower trophic levels have been advanced as key forces structuring herbivorous arthropod communities around the globe. Here, we present a first quantification of the interaction structure of a herbivore-centered food web from the High Arctic. Targeting the Lepidoptera of Northeast Greenland, we introduce generalized overlap indices as a novel tool for comparing different types of indirect interactions. First, we quantify the scope for top-down-up interactions as the probability that a herbivore attacking plant species i itself fed as a larva on species j. Second, we gauge this herbivore overlap against the potential for bottom-up-down interactions, quantified as the probability that a parasitoid attacking herbivore species i itself developed as a larva on species j. Third, we assess the impact of interactions with other food web modules, by extending the core web around the key herbivore Sympistis nigrita to other predator guilds (birds and spiders). We find the host specificity of both herbivores and parasitoids to be variable, with broad generalists occurring in both trophic layers. Indirect links through shared resources and through shared natural enemies both emerge as forces with a potential for shaping the herbivore community. The structure of the host-parasitoid submodule of the food web suggests scope for classic apparent competition. Yet, based on predation experiments, we estimate that birds kill as many (8%) larvae of S. nigrita as do parasitoids (8%), and that spiders kill many more (38%). Interactions between these predator guilds may result in further complexities. Our results caution against broad generalizations from studies of limited food web modules, and show the potential for interactions within and between guilds of extended webs. They also add a data point from the northernmost insect communities on Earth, and describe the baseline structure of a food web facing imminent climate change.

Resource shifts in Malagasy dung beetles: contrasting processes revealed by dissimilar spatial genetic patterns

The endemic dung beetle subtribe Helictopleurina has 65 species mostly in wet forests in eastern Madagascar. There are no extant native ungulates in Madagascar, but three Helictopleurus species have shifted to the introduced cattle dung in open habitats in the past 1500 years. Helictopleurus neoamplicollis and Helictopleurus marsyas exhibit very limited cytochrome oxidase subunit 1 haplotype diversity and a single haplotype is present across Madagascar, suggesting that these species shifted to cattle dung in a small region followed by rapid range expansion. In contrast, patterns of molecular diversity in Helictopleurus quadripunctatus indicate a gradual diet shift across most of southern Madagascar, consistent with somewhat broader diet in this species. The three cattle dung-using Helictopleurus species have significantly greater geographical ranges than the forest-dwelling species, apparently because the shift to the currently very abundant new resource relaxed interspecific competition that hinders range expansion in the forest species. Ecology Letters (2008) 11: 1208–1215

Origin and Diversification of Dung Beetles in Madagascar

Madagascar has a rich fauna of dung beetles (Scarabaeinae and Aphodiinae) with almost 300 species described to date. Like most other taxa in Madagascar, dung beetles exhibit an exceptionally high level of endemism (96% of the species). Here, we review the current knowledge of the origin and diversification of Malagasy dung beetles. Based on molecular phylogenies, the extant dung beetles originate from eight colonizations, of which four have given rise to extensive radiations. These radiations have occurred in wet forests, while the few extant species in the less successful radiations occur in open and semi-open habitats. We discuss the likely mechanisms of speciation and the ecological characteristics of the extant communities, emphasizing the role of adaptation along environmental gradients and allopatric speciation in generating the exceptionally high beta diversity in Malagasy dung beetles. Phylogeographic analyses of selected species reveal complex patterns with evidence for genetic introgression between old taxa. The introduction of cattle to Madagascar 1500 years ago created a new abundant resource, onto which a few species have shifted and thereby been able to greatly expand their geographical ranges.

Evolution of the Canthonini Longitarsi (Scarabaeidae) in Madagascar

Dung beetle species belonging to the worldwide tribe Canthonini (Scarabaeidae) and occurring in Madagascar are all endemic to that island. The Malagasy Canthonini form three lineages, one of which is the group Longitarsi that includes five genera. The phylogenetic relationships of Malagasy Canthonini are not fully resolved and only few species of Longitarsi have been included in previous studies. Here we infer the phylogenetic relationships within the Longitarsi group using molecular data and together with morphological examination revise the systematics of the group. The five genera of the Longitarsi group form one monophyletic clade and thus we suggest the synonymization of the younger genera Sikorantus, Phacosomoides, Madaphacosoma and Aleiantus; with the oldest genus belonging to this clade Epactoides. We describe two new species: Epactoides jounii sp. n and Epactoides mangabeensis sp. n. Most of the species of Longitarsi inhabit the eastern rainforests, with very low local species diversity and highly restricted geographical ranges. In the group Longitarsi four species are wingless. The loss of wings has evolved at least twice, at high altitude along the mountain range.

Structure of local communities of endemic dung beetles in Madagascar

The wet tropical forests in Madagascar have endemic dung beetles that have radiated for tens of millions of years using a limited range of resources produced by the species-poor mammalian fauna. Beetles were trapped in two wet-forest localities over 4 years (6407 trap nights, 18,869 individuals). More limited data for six other local communities were used to check the generality of the results. Local communities are relatively species poor (around 30 species) in comparison with wet-forest-inhabiting dung beetle communities elsewhere in the tropics (typically 50 or more species). The species belong to only two tribes, Canthonini and Helictopleurina (Oniticellini), which have evolved, exceptionally for dung beetle tribes, completely nocturnal versus diurnal diel activities, respectively. Patterns in the elevational occurrence, body size and resource use suggest that interspecific competition restricts the numbers of locally coexisting species exploiting the limited range of resources that are available. On the other hand, regional turnover in the species composition is exceptionally high due to a large number of species with small geographical ranges, yielding a very large total fauna of dung beetles in Madagascar (>250 species). Apart from exceptionally low local (alpha) diversity and high beta diversity, the Malagasy dung beetle communities are ecologically distinctive from comparable communities in other tropical regions in having high numerical dominance of the most abundant species, small average body size and low degree of resource specialization.