Raphael K. Didham

Confounding factors in the detection of species responses to habitat fragmentation

Habitat loss has pervasive and disruptive impacts on biodiversity in habitat remnants. The magnitude of the ecological impacts of habitat loss can be exacerbated by the spatial arrangement – or fragmentation – of remaining habitat. Fragmentation per se is a landscape‐level phenomenon in which species that survive in habitat remnants are confronted with a modified environment of reduced area, increased isolation and novel ecological boundaries. The implications of this for individual organisms are many and varied, because species with differing life history strategies are differentially affected by habitat fragmentation. Here, we review the extensive literature on species responses to habitat fragmentation, and detail the numerous ways in which confounding factors have either masked the detection, or prevented the manifestation, of predicted fragmentation effects.

Insects in fragmented forests: a functional approach

Insects are highly susceptible to the adverse effects of forest fragmentation. It is now beyond any doubt that fragmentation-induced changes in abundance and species richness occur in many insect groups. However, the study of insects in fragmented forests is still in its infancy and lacks real direction. Simple empirical studies are not answering the questions we most want to answer about fragmented systems. Are we in the midst of a mass-extinction crisis? What is the functional significance of the immense insect biodiversity? Does biodiversity loss affect ecosystem functioning? A more focused, functional approach to the study of forest fragmentation is required to move beyond the description of pattern and to determine how changes in insect communities affect ecosystem processes in fragmented forests.

BEETLE SPECIES RESPONSES TO TROPICAL FOREST FRAGMENTATION

The effects of forest fragmentation on beetle species composition were investigated in an experimentally fragmented tropical forest landscape in Central Amazonia. Leaf-litter beetles were sampled at seven distances from the forest edge (0–420 m) along forest edge-to-interior transects in two 100-ha forest fragments and two continuous forest edges, and at an identical series of distances along two deep continuous forest transects. Additional samples were taken at the centers of two 10-ha forest fragments and two 1-ha fragments. This sampling regime allowed discrimination between edge and fragment area effects. Beetle species composition changed significantly and independently with both decreasing distance from forest edge and decreasing fragment area. Edge effects on species composition were mediated by six important environmental variables: air temperature, canopy height, percent ground cover of twigs, litter biomass, litter moisture content, and an air temperature × distance from edge interaction effect, due to the different temperature profiles of edges with differing edge vegetation density. n nPopulation densities of 15 of the 32 most abundant beetle species tested (47%) were significantly affected by forest fragmentation. Species responses were classified empirically into four major categories: (A) edge sensitive, area insensitive; (B) area sensitive, edge insensitive; (C) edge and area sensitive; and (D) edge and area insensitive. Within these categories, trends in density were either positive (deep-forest species), or negative (disturbed-area species), with species showing the full spectrum of responses to fragmentation. The vast majority of species were adversely affected. Estimated species loss rates from forest fragments were: 49.8% of common species from 1-ha fragments, 29.8% from 10-ha fragments, and 13.8% from 100-ha fragments. Declining density was a significant precursor of species loss from forest fragments, but other species that did not show significant population density responses to fragmentation were also absent from some fragments, presumably by chance. n nThe probability of species loss from forest fragments was not correlated with body size or trophic group for the 32 common species, although for the entire beetle assemblage (993 species) proportions of species in different trophic groups changed significantly with fragmentation. Rarity and population variability (in undisturbed forest) were significant predictors of susceptibility to fragmentation. Surprisingly, though, common species were significantly more likely to become locally extinct in small fragments than rarer species. This lends empirical support to models of multispecies coexistence under disturbance that suggest competitively dominant but poorly dispersing species are the first to become extinct due to habitat destruction. Thus, rarer species are predicted to be better dispersers and better at persisting.

IMPROVED FITNESS OF APHID PARASITOIDS RECEIVING RESOURCE SUBSIDIES

The availability of nonhost resource subsidies affects the ability of parasitoids to overcome egg and time limitation and maximize lifetime reproductive success. We combined field and laboratory experiments to examine the effects of floral resource subsidies on the reproductive fitness of aphid parasitoids. Under controlled laboratory conditions, sugar resources significantly increased longevity and potential fecundity (egg load) in the endoparasitoids Aphidius rhopalosiphi and Diaeretiella rapae (Hymenoptera: Aphidiidae). Laboratory microcosm experiments showed that increased potential fecundity translated into significantly higher realized fecundity (i.e., rates of aphid parasitism) by A. rhopalosiphi receiving resource subsidies. Mechanisms of enhanced realized fecundity also operated under natural field conditions. Replicated field experiments on cultivated wheat, with host density controlled by experimental placement of aphids, showed that, in general, proximity to floral resource patches significantly increased rates of parasitism. Parasitism rates declined exponentially with increasing distance from floral patches, reaching zero beyond 14 m. Increased potential fecundity reduces the chances of parasitoids becoming egg-limited, whereas increased longevity reduces the chances of parasitoids becoming time-limited during host oviposition. Although the plasticity of egg load and longevity observed under varying conditions of resource availability is probably more relevant to parasitoid evolution, the individual fitness benefits from ephemeral resource patches are certainly important in the ecological enhancement of biological control agents.

SYNERGISTIC INTERACTIONS BETWEEN EDGE AND AREA EFFECTS IN A HEAVILY FRAGMENTED LANDSCAPE

Both area and edge effects have a strong influence on ecological processes in fragmented landscapes, but there is little understanding of how these two factors might interact to exacerbate local species declines. To test for synergistic interactions between area and edge effects, we sampled a diverse beetle community in a heavily fragmented landscape in New Zealand. More than 35,000 beetles of approximately 900 species were sampled over large gradients in habitat area (10(-2) 10(6) ha) and distance from patch edge (2(0)-2(10) m from the forest edge into both the forest and adjacent matrix). Using a new approach to partition variance following an ordination analysis, we found that a synergistic interaction between habitat area and distance to edge was a more important determinant of patterns in beetle community composition than direct edge or area effects alone. The strength of edge effects in beetle-species composition increased nonlinearly with increasing fragment area. One important consequence of the synergy is that the slopes of species area (SA) curves constructed from habitat islands depend sensitively on the distance from edge at which sampling is conducted. Surprisingly, we found negative SA curves for communities sampled at intermediate distances from habitat edges, caused by differential edge responses of matrix- vs. forest-specialist species in fragments of increasing area. Our data indicate that distance to habitat edge has a consistently greater impact on beetle community composition than habitat area and that variation in the strength of edge effects may underlie many patterns that are superficially related to habitat area.

Non-native plantation forests as alternative habitat for native forest beetles in a heavily modified landscape

The once extensive native forests of New Zealand’s central North Island are heavily fragmented, and the scattered remnants are now surrounded by a matrix of exotic pastoral grasslands and Pinus radiata plantation forests. The importance of these exotic habitats for native biodiversity is poorly understood. This study examines the utilisation of exotic plantation forests by native beetles in a heavily modified landscape. The diversity of selected beetle taxa was compared at multiple distances across edge gradients between each of the six possible combinations of adjacent pastoral, plantation, clearfell and native forest land-use types. Estimated species richness (Michaelis–Menten) was greater in production habitats than native forest; however this was largely due to the absence of exotic species in native forest. Beetle relative abundance was highest in clearfell-harvested areas, mainly due to colonisation by open-habitat, disturbance-adapted species. More importantly, though, of all the non-native habitats sampled, beetle species composition in mature P.xa0radiata was most similar to native forest. Understanding the influence of key environmental factors and stand level management is important for enhancing biodiversity values within the landscape. Native habitat proximity was the most significant environmental correlate of beetle community composition, highlighting the importance of retaining native remnants within plantation landscapes. The proportion of exotic beetles was consistently low in mature plantation stands, however it increased in pasture sites at increasing distances from native forest. These results suggest that exotic plantation forests may provide important alternative habitat for native forest beetles in landscapes with a low proportion of native forest cover.

Environmental and spatial influences upon species composition of a termite assemblage across neotropical forest islands

Patterns of species composition in a neotropical termite assemblage were studied in relation to early effects of forest fragmentation as well as other sources of environmental and spatial heterogeneity. Termite diversity surveys were carried out at three mainland forest sites, and 10 islands of varying size, in an area of lowland tropical forest that had been flooded 4 y earlier, during the creation of the Petit Saut hydroelectric project in French Guiana. The ‘ghost forest’ of dead emergent trees in the flooded zone was also studied for its influence on island termite assemblages. Results suggested that the effects of forest fragmentation upon the total assemblage, and upon soil-feeders in particular, were subordinate to the influence of forest understorey palm density, and the closely associated gradients of soil humus depth and soil pH. Moreover, gradients for these three variables were uncorrelated with forest fragmentation and probably reflected spatial environmental heterogeneity pre-dating inundation events. Nevertheless, factors associated with forest fragmentation appeared to have had a significant effect on changes in termite species composition across the study site, primarily in structuring the wood- and leaf-litter-feeder assemblage. Effects upon the latter were not apparently a result of influx of species from the ghost forest. Purely spatial variation also influenced β-diversity changes in species composition across the site. In conclusion, the effects of forest fragmentation upon termites appear to have been relatively mild compared with other faunal groups, 4 y after flooding. Nevertheless, we predict that the effects of fragmentation on termite assemblages will ultimately be negative. This study also points to the importance of Amazonian understorey palms in structuring a tropical forest termite assemblage.

Ecological boundaries: a search for synthesis

Abstract The workshop on Structure and Function of Boundaries in Ecological Mosaics was held at the Institute of Ecosystem Studies, Millbrook, New York, USA, from 17 to 19 October 2000.

An experimental assessment of biodiversity and species turnover in terrestrial vs canopy leaf litter.

Forest canopies support diverse assemblages of free-living mites. Recent studies suggest mite species complementarity between canopy and terrestrial soils is as high as 80–90%. However, confounding variation in habitat quality and resource patchiness between ground and canopy has not been controlled in previous comparative studies. We used experimental litter bags with standardized microhabitat structure and resource quality to contrast the colonization dynamics of 129 mite species utilizing needle accumulations on the ground vs in the canopy of Abies amabilis trees in a temperate montane forest in Canada. Mite abundance and species richness per litter bag were five to eight times greater on the ground than in the canopy, and composition differed markedly at family-, genus-, and species-level. Seventy-seven species (57%) were restricted to either ground or canopy litter bags, but many of these species were rare (n<5 individuals). Of 49 ‘common’ species, 30.6% were entirely restricted to one habitat, which is considerably lower than most published estimates. In total, 87.5% of canopy specialists had rare vagrants on the ground, whereas only 51.9% of ground specialists had rare vagrants in the canopy. Canonical correspondence analysis of mite community structure showed high species turnover through time and a high degree of specialization for early-, mid-, and late-successional stages of litter decomposition, in both ground and canopy mites. In addition, distinct assemblages of ground-specialist mites dominated each elevation (800, 1000, and 1200xa0m), whereas few canopy-specialist mites had defined elevational preferences. This suggests that canopy mites may have greater tolerance for wide variation in environmental conditions than soil mites. The degree of species turnover between adjacent mountains also differed markedly, with 46.5% turnover of ground species, but 63.4% turnover of canopy species between the two montane areas. While ground and canopy assemblages are similar in total biodiversity, it appears that local mite richness (alpha diversity) is higher on the ground, whereas species turnover between sites (beta diversity) is higher in the canopy.

Rapid recovery of an insect–plant interaction following habitat loss and experimental wetland restoration

This study examined the impact of wetland habitat loss and isolation on an insect–plant interaction, and the subsequent rate of recovery of the interaction following experimental habitat restoration. We compared herbivore colonisation rates and herbivory damage by ‘Batrachedra’ sp. (Lepidoptera: Coleophoridae) on experimentally placed potted Sporadanthus ferrugineus (Restionaceae) plants at increasing distances (up to 800xa0m) from an intact habitat (the source population). These tests showed that even a moderate degree of isolation (i.e. greater than 400xa0m) from the intact wetland habitat caused an almost complete collapse of the insect–plant interaction, at least in the short term. The number of eggs and larvae of colonising ‘Batrachedra’ sp., as well as average larval size and the proportion of S. ferrugineus stems damaged, all decreased logarithmically with increasing distance from the intact habitat, presumably due to dispersal limitation of the herbivore. Subsequently, to test whether the interaction can recover following habitat restoration, we surveyed herbivore colonisation rates and herbivory damage on naturally regenerated S. ferrugineus plants on experimentally restored ‘islands’ at increasing distances (up to 800xa0m) from an intact habitat. The rate of recovery of the interaction was surprisingly rapid (i.e. between 196 and 308xa0weeks). The degree of difference in the density of eggs and larvae, and in the proportion of stems damaged with increasing isolation from the intact wetland, gradually diminished over 196xa0weeks. After 308xa0weeks there was no significant difference in the insect–plant interaction between the intact wetland sites and any of the experimentally restored sites up to 800xa0m away. These results suggest that some insect–plant interactions can recover rapidly from habitat loss with restoration management.