Roger Kitching

Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding

To manage and conserve biodiversity, one must know what is being lost, where, and why, as well as which remedies are likely to be most effective. Metabarcoding technology can characterise the species compositions of mass samples of eukaryotes or of environmental DNA. Here, we validate metabarcoding by testing it against three high-quality standard data sets that were collected in Malaysia (tropical), China (subtropical) and the United Kingdom (temperate) and that comprised 55,813 arthropod and bird specimens identified to species level with the expenditure of 2,505 person-hours of taxonomic expertise. The metabarcode and standard data sets exhibit statistically correlated alpha- and beta-diversities, and the two data sets produce similar policy conclusions for two conservation applications: restoration ecology and systematic conservation planning. Compared with standard biodiversity data sets, metabarcoded samples are taxonomically more comprehensive, many times quicker to produce, less reliant on taxonomic expertise and auditable by third parties, which is essential for dispute resolution.

Food webs: Reconciling the structure and function of biodiversity

The global biodiversity crisis concerns not only unprecedented loss of species within communities, but also related consequences for ecosystem function. Community ecology focuses on patterns of species richness and community composition, whereas ecosystem ecology focuses on fluxes of energy and materials. Food webs provide a quantitative framework to combine these approaches and unify the study of biodiversity and ecosystem function. We summarise the progression of food-web ecology and the challenges in using the food-web approach. We identify five areas of research where these advances can continue, and be applied to global challenges. Finally, we describe what data are needed in the next generation of food-web studies to reconcile the structure and function of biodiversity.

Arthropod diversity in a tropical forest

Assessing Creepy Crawlies Arthropods are the most diverse group of terrestrial animal species, yet estimates of the total number of arthropod species have varied widely, especially for tropical forests. Basset et al. (p. 1481, see the cover) now provide more reliable estimates of total arthropod species richness in a tropical rainforest in Panama. Intensive sampling of a half hectare of forest yielded just over 6000 arthropod species. Scaling up this result to the whole forest suggests that the total species diversity lies between 17,000 and 40,000 species. Total arthropod species richness in a tropical rainforest can be best predicted by plant diversity. Most eukaryotic organisms are arthropods. Yet, their diversity in rich terrestrial ecosystems is still unknown. Here we produce tangible estimates of the total species richness of arthropods in a tropical rainforest. Using a comprehensive range of structured protocols, we sampled the phylogenetic breadth of arthropod taxa from the soil to the forest canopy in the San Lorenzo forest, Panama. We collected 6144 arthropod species from 0.48 hectare and extrapolated total species richness to larger areas on the basis of competing models. The whole 6000-hectare forest reserve most likely sustains 25,000 arthropod species. Notably, just 1 hectare of rainforest yields >60% of the arthropod biodiversity held in the wider landscape. Models based on plant diversity fitted the accumulated species richness of both herbivore and nonherbivore taxa exceptionally well. This lends credence to global estimates of arthropod biodiversity developed from plant models.

The costs and benefits of cooperation between the Australian lycaenid butterfly, Jalmenus evagoras, and its attendant ants

SummaryThe larvae and pupae of the Australian lycaenid butterfly, Jalmenus evagoras associate mutualistically with ants in the genus Iridomyrmex. Four ant exclusion experiments in three field sites demonstrated that predation and parasitism of J. evagoras are so intense that individuals deprived of their attendant ants are unlikely to survive. Larvae and pupae of J. evagoras aggregate, and the mean number of attendant ants per individual increases with larval age and decreases with group size. Field observations showed that young larvae could gain more attendant ants per individual by joining the average size group of about 4 larvae than by foraging alone. Aggregation behaviour is influenced by ant attendance: young larvae and pupating fifth instars aggregated significantly more often on plants with ants than on plants where ants had been excluded. In return for tending and protecting the larvae, ants were rewarded by food secretions that can amount to as much as 409 mg dry biomass from a single host plant containing 62 larvae and pupae of J. evagoras over a 24 h period. Larval development in the laboratory lasted approximately a month, and larvae that were tended by ants developed almost 5 days faster than larvae that were not tended. However, tended individuals, particularly females, pupated at a significantly lower weight than their untended counterparts, and the adults that eclosed from these pupae were also lighter and smaller. On average, pupae that were tended by ants lost 25% more weight than untended pupae, and in contrast with larvae, they took longer to eclose than pupae that were not tended. These experimental results are discussed in terms of costs and benefits of association for both partners, and of aggregation for the lycaenids.

Species number, species abundance and body length of arboreal arthropods associated with an Australian rainforest tree

Abstract. 1 The species number, the abundance per species and the body length of arthropods foraging within the crowns of an over‐storey rainforest tree from Australia, Argyrodendron actinophyllum (Sterculiaceae), were investigated by interception trap sampling and restricted canopy fogging. Emphasis was placed upon the interpretation of trap data. Arthropods were trapped continuously day and night, over a 2‐year period and the final analyses examined the attributes of 759 species which represented 20,500 individuals. 2 The proportion of‘rare’species (Le. collected once) intercepted was high (35.7%), although lower than in other similar rainforest surveys. Neither the α log‐series nor the log‐normal distribution could be fitted to the relationship between number of species and number of individuals, since the number of rare species was much higher than predicted and the mode of the distribution could not be identified. The proportion of rare species was higher in fogging collections (452%) than in trap collections. 3 The data are compared with a study of Bornean arboreal beetles, obtained by fogging trees during a single sampling event. Several patterns were common to both data sets. However, the three‐dimensional plot of the variables describing the structure of the arthropod community showed a notably rougher surface than in the case of Bornean beetles. 4 Although several factors may complicate the interpretation of the three‐dimensional plots, long‐term and continuous sampling may alter our perception of complex arthropod communities. This methodology is imperative for a proper understanding of arthropod community structure in rain forests.

Discriminatory power of different arthropod data sets for the biological monitoring of anthropogenic disturbance in tropical forests

Arthropods were monitored by local parataxonomists at 12 sites of increasing anthropogenic disturbance (old and young secondary forests, savanna and cultivated gardens) at Gamba, Gabon. We report on the discriminatory power of different data sets with regard to the classification of sites along the disturbance gradient, using preliminary data accounting for 13 surveys and 142425 arthropods collected by Malaise, pitfall and yellow-pan traps. We compared the performance of different data sets. These were based upon ordinal, familial and guild composition, or upon 22 target taxa sorted to morphospecies and either considered in toto or grouped within different functional guilds. Finally we evaluated ‘predictor sets’ made up of a few families or other target taxa, selected on the basis of their indicator value index. Although the discriminatory power of data sets based on ordinal categories and guilds was low, that of target taxa belonging to chewers, parasitoids and predators was much higher. The data sets that best discriminated among sites of differing degrees of disturbance were the restricted sets of indicator families and target taxa. This validates the concept of predictor sets for species-rich tropical systems. Including or excluding rare taxa in the analyses did not alter these conclusions. We conclude that calibration studies similar to ours are needed elsewhere in the tropics and that this strategy will allow to devise a representative and efficient biotic index for the biological monitoring of terrestrial arthropod assemblages in the tropics.

The use of ants and other soil and litter arthropods as bio-indicators of the impacts of rainforest clearing and subsequent land use

The present study investigated the impacts of rainforest clearance, and associated subsequent land␣use for pasture, on assemblages of soil and litter arthropods in eastern subtropical Australia. We assessed the utility of soil and litter arthropods as potential bio-indicators of cleared and forested habitats. Arthropods were sampled from 24 sites (12 sites each in rainforest and pasture) using two methods (extraction from litter, pitfall traps). Responses of taxa were analysed at various levels of taxonomic resolution, including ‘coarse’ arthropods (all arthropods sorted to Order/Class), ant genera and ant species. Multivariate analyses of arthropod composition indicated that an increase in the level of taxonomic resolution did not provide a commensurate increase in the sensitivity of assemblage response. Indicator values (IndVals), computed for each taxon, showed that a number of arthropod taxa may have potential as bio-indicators of habitat change. However the use of many of these, especially many ant species found in our study, may be unreliable because even after extensive numbers of sites were sampled, most species showed patchy distributions. To overcome this problem, we generated ‘composite indices’, by combining information from sets of indicator taxa. The utility of these composite indices is discussed.

Logging cuts the functional importance of invertebrates in tropical rainforest

Invertebrates are dominant species in primary tropical rainforests, where their abundance and diversity contributes to the functioning and resilience of these globally important ecosystems. However, more than one-third of tropical forests have been logged, with dramatic impacts on rainforest biodiversity that may disrupt key ecosystem processes. We find that the contribution of invertebrates to three ecosystem processes operating at three trophic levels (litter decomposition, seed predation and removal, and invertebrate predation) is reduced by up to one-half following logging. These changes are associated with decreased abundance of key functional groups of termites, ants, beetles and earthworms, and an increase in the abundance of small mammals, amphibians and insectivorous birds in logged relative to primary forest. Our results suggest that ecosystem processes themselves have considerable resilience to logging, but the consistent decline of invertebrate functional importance is indicative of a human-induced shift in how these ecological processes operate in tropical rainforests.

Temporal and spatial variation of mortality in field populations of Danaus plexippus L. and D. chrysippus L. Larvae (Lepidoptera: Nymphalidae)

SummaryMortality estimates for the immature stages of two butterfly species, Danaus plexippus and D. chrysippus, were obtained by observing the survival of egg cohorts on different sized patches of food plants (Asclepias spp.), over a one-year period. Losses were variable (0–100%) but usually high (90% and over) throughout the year for both species. Most of the losses in both species occurred in the early stages. The mortality by the third instar accounts for 86–100% of the total losses by instar V. Accordingly both species fall into Prices (1975) type A survivorship category. The size of patches of host plants affected losses. The trend was for increasing losses with increasing patch size. A full life-budget is presented for D. plexippus and implications of the observed mortality levels for competition between the two butterfly species is discussed.

The Myrmecophilous organs of the larvae of some British Lycaenidae (Lepidoptera): a comparative study

Scanning electron microscope studies have been made of larvae of eight of the fifteen resident British lycaenids (including Maculinea arion). A full suite of myrmecophilous organs comprising Newcomers organs, tentacular organs and pore cupolas, has been identified in Lysandra coridon, L. bellargus and Polyommatus icarus. M. arion possesses Newcomers organs and pore cupolas. Quercusia quercus has pore cupolas and what may be the rudiments of tentacular organs. Strymonidia pruni and Hamearis lucina have only pore cupolas. No myrmecophilous organs were identified on larvae of Cupido minimus, but poor quality material suggests this may be artifactual. The ultrastructure of the myrmecophilous organs or their supposed homologues is described in detail. The results presented are compared with those of earlier authors for the other seven resident species of British lycaenids. The functions, homologies and possible evolutionary origins of the myrmecophilous organs are discussed.