Do asynchronies in extinction debt affect the structure of trophic networks? A case study of antagonistic butterfly larvae–plant networks

Habitat loss and fragmentation affect species richness in fragmented habitats and can lead to immediate or time‐delayed species extinctions. Asynchronies in extinction and extinction debt between interacting species may have severe effects on ecological networks. However, these effects remain largely unknown. We evaluated the effects of habitat patch and landscape changes on antagonistic butterfly larvae–plant trophic networks in Mediterranean grasslands in which previous studies had shown the existence of extinction debt in plants but not in butterflies. We sampled current species richness of habitat‐specialist and generalist butterflies and vascular plants in 26 grasslands. We assessed the direct effects of historical and current patch and landscape characteristics on species richness and on butterfly larvae–plant trophic network metrics and robustness. Although positive species‐ and interactions–area relationships were found in all networks, structure and robustness was only affected by patch and landscape changes in networks involving the subset of butterfly specialists. Larger patches had more species (butterflies and host plants) and interactions but also more compartments, which decreased network connectance but increased network stability. Moreover, most likely due to the rescue effect, patch connectivity increased host‐plant species (but not butterfly) richness and total links, and network robustness in specialist networks. On the other hand, patch area loss decreased robustness in specialist butterfly larvae–plant networks and made them more prone to collapse against host plant extinctions. Finally, in all butterfly larvae–plant networks we also detected a past patch and landscape effect on network asymmetry, which indicates that there were different extinction rates and extinction debts for butterflies and host plants. We conclude that asynchronies in extinction and extinction debt in butterfly–plant networks provoked by patch and landscape changes caused changes in species richness and network links in all networks, as well as changes in network structure and robustness in specialist networks.     

Habitat isolation affects plant–herbivore–enemy interactions on cherry trees

Understanding the interactions between herbivores and natural enemies in fragmented landscapes is essential for conservation biological control. Studies including multiple enemies affecting multiple herbivores, plant damage and growth are needed. Here, we separated independent effects of (1) isolation of cherry trees from woody habitat and (2) the amount of woody habitat in the surrounding landscape (500 m buffers) on interactions between different groups of herbivores with their natural enemies and resulting changes in the growth of young cherry trees. Most predatory arthropods declined with habitat isolation, except some aphid predators (ladybeetles and hoverflies). Herbivores either increased with isolation (herbivorous beetles) or showed no significant response (aphids). In contrast, the amount of woody habitat in the landscape was not relevant for herbivore–enemy interactions at the investigated scale. Plant growth was affected by bottom-up (nutrient availability) and top-down (aphid density) forces but did not change significantly with habitat amount or isolation. We conclude that herbivores can be released from natural enemies at isolated sites, in accordance with the hypothesis that habitat connectivity improves pest control. However, each herbivore group responded differently to the landscape context and had contrasting effects on the same host plant, demonstrating the difficulty to predict landscape effects on plant growth.     

Metapopulation extinction in fragmented landscapes: using bacteria and protozoa communities as model ecosystems

Extinction is notoriously difficult to study because of the long timescales involved and the difficulty in ascertaining that extinction has actually occurred. The effect of habitat subdivision, or fragmentation, on extinction risk is even harder to study, as it requires copious replication of habitat patches on large spatial scales and control of area effects between treatments. I used simple small-scale communities of bacteria and protozoa to study extinction in response to habitat loss and habitat fragmentation. I studied several different community configurations, each with three trophic levels. Unlike most metapopulation studies (experimental as well as theoretical), which have tended to deal with inherently unstable species interactions, I deliberately used community configurations that were persistent in large stock cultures. I recorded the time to extinction of the top predator in single habitat patches of different sizes and in fragmented systems with different degrees of subdivision but the same amount of available habitat. Habitat loss reduced the time to extinction of isolated populations. Fragmented systems went extinct sooner than corresponding unfragmented (continuous) systems of the same overall size. Unfragmented populations persisted longer than fragmented systems (metapopulations) with or without dispersal corridors between subpopulations. In fact, fragmented systems where the fragments were linked by dispersal corridors went extinctly significantly sooner than those where subpopulations were completely isolated from each other. If these results extend to more "natural" systems, it suggests a need for caution in management programs that emphasize widespread establishment of wildlife corridors in fragmented landscapes.     

Relative importance of quantity, quality and isolation of patches for butterfly diversity in fragmented urban forests

The majority of forests in urban areas are small and isolated. Improving habitat quality of small forests instead of increasing habitat size and connectivity could be an effective means of conserving the biodiversity of such highly fragmented landscapes. In this study, we investigated the relative importance of habitat quantity, quality and isolation on butterfly assemblages in urban fragmented forests in Tokyo, Japan. We used four habitat geographic parameters: (1) fragment size, (2) shape index, (3) isolation (distance to the mainland), and (4) connectivity; and three habitat quality parameters: (1) herbaceous nectar plant abundance, (2) herbaceous nectar plant diversity, and (3) larval host plant diversity. We surveyed butterfly assemblages along transects in 20 forest fragments that ranged in size from 1 to 122 ha. We used generalized linear models to relate the number of species in a fragment to four habitat geographic parameters and three habitat quality parameters. The averaged models based on AIC_c showed that fragment size had a strong positive effect on butterfly species richness. There was also a positive effect of herbaceous nectar plant abundance on species diversity. These findings suggest that improving the habitat quality of small and isolated forests in highly fragmented landscapes may be capable of maintaining levels of butterfly diversity comparable to those of large fragments.     

Habitat Characteristics of Forest Fragments Determine Specialisation of Plant-Frugivore Networks in a Mosaic Forest Landscape

Plant-frugivore networks play a key role in the regeneration of sub-tropical forest ecosystems. However, information about the impact of habitat characteristics on plant-frugivore networks in fragmented forests is scarce. We investigated the importance of fruit abundance, fruiting plant species richness and canopy cover within habitat fragments for the structure and robustness of plant-frugivore networks in a mosaic forest landscape of South Africa. In total, 53 avian species were involved in fruit removal of 31 fleshy-fruiting plant species. Species specialisation was always higher for plants than for frugivores. Both species and network-level specialisation increased with increasing fruit abundance and decreased with increasing fruiting plant species richness and canopy cover within fragments. Interaction diversity was unaffected by fruit abundance and canopy cover, but increased slightly with increasing fruiting plant species richness. These findings suggest that especially the availability of resources is an important determinant of the structure of plant-frugivore networks in a fragmented forest landscape.     

The tails of two geckos tell the story of dispersal in a fragmented landscape

The fragmentation of habitat is a major cause of biodiversity loss. However, while numerous studies have suggested that reducing the size of populations and isolating them on fragments leads ultimately to the extinction of a species (small isolated populations are extinction prone), the evidence has been rather conjectural. This is because dispersal is so difficult to measure and isolation difficult to confirm. In past studies, evidence that populations become small and isolated on fragments, leading to declines, has relied on spatial patterns of distribution and abundance. Thus, a species not trapped in the matrix in which fragments are embedded might be assumed isolated on fragments, and if low in abundance on fragments compared to continuous habitat is assumed to have declined on fragments due to this isolation. However, without accurately measuring the degree of isolation, it is difficult to distinguish the role of isolation from other important causes of population decline that are correlated with fragment and population size, such as habitat degradation. Developments in molecular techniques and statistical methods now make it possible to measure isolation. Refreshingly, in this issue Hoehn et al. analyse microsatellite DNA with a suite of statistical methods to show convincingly that a declining species of gecko suffers from greater isolation on habitat fragments than a contrasting gecko that is able to disperse between fragments and hence persist in the severely fragmented wheatbelt of Western Australia.     

Seed‐dispersal interactions in fragmented landscapes – a metanetwork approach

Mutualistic interactions repeatedly preserved across fragmented landscapes can scale‐up to form a spatial metanetwork describing the distribution of interactions across patches. We explored the structure of a bird seed‐dispersal (BSD) metanetwork in 16 Neotropical forest fragments to test whether a distinct subset of BSD‐interactions may mediate landscape functional connectivity. The metanetwork is interaction‐rich, modular and poorly connected, showing high beta‐diversity and turnover of species and interactions. Interactions involving large‐sized species were lost in fragments < 10 000 ha, indicating a strong filtering by habitat fragmentation on the functional diversity of BSD‐interactions. Persistent interactions were performed by small‐seeded, fast growing plant species and by generalist, small‐bodied bird species able to cross the fragmented landscape. This reduced subset of interactions forms the metanetwork components persisting to defaunation and fragmentation, and may generate long‐term deficits of carbon storage while delaying forest regeneration at the landscape level.     

Scale-dependent diversity effects of seed dispersal by a wild herbivore in fragmented grasslands

Dispersal limitation between habitat fragments is a known driver of landscape-scale biodiversity loss. In Europe, agricultural intensification during the twentieth century resulted in losses of both grassland habitat and traditional grassland seed dispersal vectors such as livestock. During the same period, populations of large wild herbivores have increased in the landscape. Usually studied in woodland ecosystems, these animals are found to disperse seeds from grasslands and other open habitats. We studied endozoochorous seed dispersal by roe deer (Capreolus capreolus) in fragmented grasslands and grassland remnants, comparing dispersed subcommunities of plant species to those in the established vegetation and the seed bank. A total of 652 seedlings of 67 species emerged from 219 samples of roe deer dung. This included many grassland species, and several local grassland specialists. Dispersal had potentially different effects on diversity at different spatial scales. Almost all sites received seeds of species not observed in the vegetation or seed bank at that site, suggesting that local diversity might not be dispersal limited. This pattern was less evident at the landscape scale, where fewer new species were introduced. Nonetheless, long-distance dispersal by large wild herbivores might still provide connectivity between fragmented habitats within a landscape in the areas in which they are active. Finally, as only a subset of the available species were found to disperse in space as well as time, the danger of future biodiversity loss might still exist in many isolated grassland habitats.     

Population Dynamics of the Andean Lizard Anolis heterodermus: Fast‐slow Demographic Strategies in Fragmented Scrubland Landscapes

Habitat fragmentation and loss affect population stability and demographic processes, increasing the extinction risk of species. We studied Anolis heterodermus populations inhabiting large and small Andean scrubland patches in three fragmented landscapes in the Sabana de Bogotá (Colombia) to determine the effect of habitat fragmentation and loss on population dynamics. We used the capture‐mark‐recapture method and multistate models to estimate vital rates for each population. We estimated growth population rate and the most important processes that affect λ by elasticity analysis of vital rates. We tested the effects of habitat fragmentation and loss on vital rates of lizard populations. All six isolated populations showed a positive or an equilibrium growth rate (λ = 1), and the most important demographic process affecting λ was the growth to first reproduction. Populations from landscapes with less scrubland natural cover showed higher stasis of young adults. Populations in highly fragmented landscapes showed highest juvenile survival and growth population rates. Independent of the landscape's habitat configuration and connectivity, populations from larger scrubland patches showed low adult survivorship, but high transition rates. Populations varied from a slow strategy with low growth and delayed maturation in smaller patches to a fast strategy with high growth and early maturation in large patches. This variation was congruent with the fast‐slow continuum hypothesis and has serious implications for Andean lizard conservation and management strategies. We suggest that more stable lizard populations will be maintained if different management strategies are adopted according to patch area and habitat structure.     

Nymphalid butterfly dispersal among forest fragments at Serra da Canastra National Park,Brazil

Organisms must possess good dispersal ability to persist in fragmented landscapes, as extinction in habitat patches is frequent and patches must be re-colonised to keep viable metapopulations. Thus, metapopulation maintenance is dependent on patch size and distance, although these affect species differently. In order to evaluate the ability of Nymphalid butterfly species to live in naturally fragmented small forest fragments we marked and released 3,415 butterflies in 16 of these areas separated in two networks at the Serra da Canastra National Park (PNSC), south-eastern Brazil. Subsequent recaptures in different forest fragments enabled us to assess the dispersal rates and distances for several Nymphalid species. Seventeen butterflies from 11 out of the 50 species captured were directly observed to disperse from 500 m to 870 m. Dispersal rates varied between 1 and 7% of the marked individuals and were directly correlated to the mean forewing length of each butterfly species population. The connectivity of the forest fragments through creeks appear to facilitate butterfly dispersal among fragments within micro-basins, as only one out of 50 dispersing individuals was observed to fly from one micro-basin to the other. Several species had viable populations in the small-fragment network. The distance between fragments is crucial as the coarser fragment network was unlikely to sustain viable populations of most of the species. The protection of large forest fragments located outside of the PNSC may be necessary to promote colonization of the smaller forest fragments inside the Park.     

The Influence of Large Tree Density on Howler Monkey (Alouatta palliata mexicana) Presence in Very Small Rain Forest Fragments

The populations of the Mexican mantled howler monkey ( Alouatta palliata mexicana ) in the Los Tuxtlas region, Mexico, have declined drastically due to habitat loss and fragmentation. Nevertheless, several troops still inhabit very small and isolated rain forest fragments. We identified the main vegetation attributes that can favor the presence of howlers within 18 small (< 10-ha) fragments that did not differ significantly in size, shape, and isolation (nine occupied and nine unoccupied by howlers). We found that habitat quality ( i.e. , food resources and vegetation structure) affected howler incidence in small fragments. Particularly, the occupied fragments showed greater density of big trees (dbh > 60 cm), greater total basal area, greater basal area of persistent tree species, and greater basal area of top food species than the unoccupied fragments; suggesting that even for small fragments the loss of big trees and particularly the decrease in size class of the top food species can negatively affect howler distribution in highly fragmented landscapes. These findings could be used to establish foreground conservation areas for this critically endangered subspecies in fragmented landscapes of Los Tuxtlas.     

Understory bird communities in Amazonian rainforest fragments: species turnover through 25 years post-isolation in recovering landscapes

Inferences about species loss following habitat conversion are typically drawn from short-term surveys, which cannot reconstruct long-term temporal dynamics of extinction and colonization. A long-term view can be critical, however, to determine the stability of communities within fragments. Likewise, landscape dynamics must be considered, as second growth structure and overall forest cover contribute to processes in fragments. Here we examine bird communities in 11 Amazonian rainforest fragments of 1-100 ha, beginning before the fragments were isolated in the 1980s, and continuing through 2007. Using a method that accounts for imperfect detection, we estimated extinction and colonization based on standardized mist-net surveys within discreet time intervals (1-2 preisolation samples and 4-5 post-isolation samples). Between preisolation and 2007, all fragments lost species in an area-dependent fashion, with loss of as few as <10% of preisolation species from 100-ha fragments, but up to 70% in 1-ha fragments. Analysis of individual time intervals revealed that the 2007 result was not due to gradual species loss beginning at isolation; both extinction and colonization occurred in every time interval. In the last two samples, 2000 and 2007, extinction and colonization were approximately balanced. Further, 97 of 101 species netted before isolation were detected in at least one fragment in 2007. Although a small subset of species is extremely vulnerable to fragmentation, and predictably goes extinct in fragments, developing second growth in the matrix around fragments encourages recolonization in our landscapes. Species richness in these fragments now reflects local turnover, not long-term attrition of species. We expect that similar processes could be operating in other fragmented systems that show unexpectedly low extinction.     

Removing interactions,rather than species,casts doubt on the high robustness of pollination networks

In the last 15 years, a complex networks perspective has been increasingly used in the robustness assessment of ecological systems. It is therefore crucial to assess the reliability of such tools. Based on the traditional simulation of node (species) removal, mutualistic pollination networks are considered to be relatively robust because of their 1) truncated power‐law degree distribution, 2) redundancy in the number of pollinators per plant and 3) nested interaction pattern. However, species removal is only one of several possible approaches to network robustness assessment. Empirical evidence suggests a decline in abundance prior to the extinction of interacting species, arguing in favour of an interaction removal‐based approach (i.e. interaction disruption), as opposed to traditional species removal. For simulated networks, these two approaches yield radically different conclusions, but no tests are currently available for empirical mutualistic networks. This study compared this new robustness evaluation approach based on interaction extinction versus the traditional species removal approach for 12 alpine and subalpine pollination networks. In comparison with species removal, interaction removal produced higher robustness in the worst‐case extinction scenario but lower robustness in the best‐case extinction scenario. Our results indicate that: 1) these two approaches yield very different conclusions and 2) existing assessments of ecological network robustness could be overly optimistic, at least those based on a disturbance affecting species at random or beginning with the least connected species. Therefore, further empirical study of plant–pollinator interactions in disturbed ecosystems is imperative to understand how pollination networks are disassembled.     

Characterising extinction debt following habitat fragmentation using neutral theory

Habitat loss leads to species extinctions, both immediately and over the long term as ‘extinction debt’ is repaid. The same quantity of habitat can be lost in different spatial patterns with varying habitat fragmentation. How this translates to species loss remains an open problem requiring an understanding of the interplay between community dynamics and habitat structure across temporal and spatial scales. Here we develop formulas that characterise extinction debt in a spatial neutral model after habitat loss and fragmentation. Central to our formulas are two new metrics, which depend on properties of the taxa and landscape: ‘effective area’, measuring the remaining number of individuals and ‘effective connectivity’, measuring individuals’ ability to disperse through fragmented habitat. This formalises the conventional wisdom that habitat area and habitat connectivity are the two critical requirements for long‐term preservation of biodiversity. Our approach suggests that mechanistic fragmentation metrics help resolve debates about fragmentation and species loss.     

Range shifting on a fragmented landscape

Projected responses of species' to climate change have so far included few of the factors that are important determinants of species' distributions within its range. In this paper we utilise a spatially explicit cellular lattice, colonisation–extinction model to investigate the effect of habitat loss, fragmentation and species characteristics on range shifting in response to climate change. Contrary to the predictions of patch occupancy in static climate models we show that fragmentation can have a positive effect on species survival when species have high colonisation rates. For species with low colonisation rates aggregative behaviours prevent success on fragmented landscapes at high levels of habitat loss, and range shifting is more successfully achieved where habitat is correlated. At levels of habitat loss near the extinction threshold, less fragmented landscapes can facilitate range shifting even for the best colonisers. We discuss how imposing a climate window may reduce percolation routes and have implications for the area of usable habitat at any given level of habitat availability. We demonstrate the importance of landscape structure for range shifting dynamics and argue that management of reserve networks needs to consider the requirements of species with different life history characteristics.     

Traits related to species persistence and dispersal explain changes in plant communities subjected to habitat loss

Aim Habitat fragmentation is a major driver of biodiversity loss but it is insufficiently known how much its effects vary among species with different life‐history traits; especially in plant communities, the understanding of the role of traits related to species persistence and dispersal in determining dynamics of species communities in fragmented landscapes is still limited. The primary aim of this study was to test how plant traits related to persistence and dispersal and their interactions modify plant species vulnerability to decreasing habitat area and increasing isolation. Location Five regions distributed over four countries in Central and Northern Europe. Methods Our dataset was composed of primary data from studies on the distribution of plant communities in 300 grassland fragments in five regions. The regional datasets were consolidated by standardizing nomenclature and species life‐history traits and by recalculating standardized landscape measures from the original geographical data. We assessed the responses of plant species richness to habitat area, connectivity, plant life‐history traits and their interactions using linear mixed models. Results We found that the negative effect of habitat loss on plant species richness was pervasive across different regions, whereas the effect of habitat isolation on species richness was not evident. This area effect was, however, not equal for all the species, and life‐history traits related to both species persistence and dispersal modified plant sensitivity to habitat loss, indicating that both landscape and local processes determined large‐scale dynamics of plant communities. High competitive ability for light, annual life cycle and animal dispersal emerged as traits enabling species to cope with habitat loss. Main conclusions In highly fragmented rural landscapes in NW Europe, mitigating the spatial isolation of remaining grasslands should be accompanied by restoration measures aimed at improving habitat quality for low competitors, abiotically dispersed and perennial, clonal species.     

The conservation value of small, isolated fragments of lowland tropical rain forest

Deforestation is occurring at an alarming rate in the lowland tropics. In many tropical regions, rain forest is restricted to small (<100 ha), isolated fragments. While only the preservation of large areas of tropical rain forest can safeguard the complete biota, recent research has shown that a substantial number of forest species can persist for decades in fragmented forest, though large vertebrates are susceptible to habitat fragmentation. Inevitably, small fragments will become the last refuges of many rainforest species that are on the brink of extinction. In areas with little rain forest remaining, fragments can be the 'seeds' from which to re-establish extensive forest.     

High Conservation Value of Forest Fragments for Plant and Frugivore Communities in a Fragmented Forest Landscape in South Africa

Fragmentation is a major threat factor for plant–frugivore communities in tropical and subtropical forests. Resulting changes in the distribution of traits within these communities, e.g., a loss in large‐bodied frugivores, may lead to strong changes in plant–frugivore interactions in fragmented forests. Yet, we still lack a thorough understanding of the interplay between forest fragmentation, the trait‐composition of communities and resulting plant–frugivore interactions on a community‐scale. In a fragmented South African landscape comprising different forest categories—i.e., continuous natural forest, forest fragments surrounded by natural grassland, and forest fragments surrounded by sugarcane—we investigated the relationship between communities of fruiting plants and their frugivore visitors in response to forest fragmentation, as well as the interactive effects of forest fragmentation and fruit size of the plants on the number of frugivore visitors and their body size. Neither the fruit size of plant nor the body mass of frugivore communities differed between natural forest sites and forest fragments. Moreover, in‐depth analyses of frugivore assemblages visiting plant species revealed no effect of forest category on the number of frugivore visits or their mean body mass. The number of visits and body mass of frugivores were merely determined by the crop and fruit size of the focal plant species. Overall, our results suggest that frugivory of plant species with differently sized fruits was not reduced in forest fragments. Thus, fragments with high fruit availability may be key elements maintaining the functional connectivity of a heterogeneous forest landscape.     

Do forest plants conform to the theory of island biogeography: the case study of bog islands

Biodiversity conservation is confronted with increasing risk of extinction in isolated small-area remnants and the limitation of species to colonize recently formed habitats. We hypothesized that the equilibrium pattern of forest herb layer in long-term fragmented landscape should comply with the theory of island biogeography. Forests on mineral soil islands located in large mires of western Estonia were considered as dispersal target habitats, and forests on mainland and peninsulas in mires as sources. Species richness was the lowest in mainland forests and the effect was confounded by habitat structure, suggesting a negative effect of silvicultural management in easily accessible forests. We observed the ‘small island effect’, i.e. greater overall species richness in small-area habitats, which was determined by the habitat preference of shade tolerant generalists. The average species richness of common mainland forest specialists varied little, but capitalizing on the traditional approach and analyzing only island data, weak effects of distance and habitat quality were detected. At single species level, unexpectedly, many habitat specialists were observed to have successfully dispersed to islands, indicating insufficient knowledge of the long-distance dispersal mechanisms of forest-dwelling plants. In fragmented forest landscapes the theory of island biogeography can be applied to habitat specialist plant species, but only regarding the effect of isolation and in conditions of persistent forest structural quality. In the light of global changes, optimized conservation planning should primarily target on (i) the conservation of ancient habitat fragments independent of their current area, and (ii) the promotion of diversity of potential dispersal vectors in the landscape.     

Female-biased dispersal, low female recruitment, unpaired males, and the extinction of small and isolated bird populations

Small and isolated populations are usually assumed to be at a high risk of extinction due to environmental or demographic stochasticity, genetic problems, or too little immigration. In birds, natal dispersal is usually female-biased, but the consequences of such a pattern on vulnerability to extinction of isolated populations has not received much attention before. In this paper I derive predictions as to how female-biased natal dispersal may differentially affect the extinction risk of populations and species with contrasting distributions, migratory behaviours, life histories and mating systems. Female-biased dispersal will lead to male-biased sex ratios in small, isolated or fragmented populations, in particular because recent research has shown that females often have a limited ability to search for mates and may therefore effectively be lost from the breeding population if they disperse into areas empty of conspecifics. I reviewed published studies on birds and found that a high proportion of unpaired males is common in isolated populations or populations in small habitat fragments. Dispersal of females may therefore increase the vulnerability to extinction of small or isolated populations, or populations at the periphery of a species' distribution range. I also predict that vulnerability to extinction should be greater for migratory than for resident species and greater for short-lived than for long-lived species because of differences in the time available for females to locate unpaired males. Further, extinction risk may also be greater for birds than for mammals due to differences in which sex disperses and patterns of parental care. Finally, mating system will also affect vulnerability to extinction when natal dispersal leads to biased sex ratios. I review available evidence for these predictions (e.g. songbird declines in North America) and discuss implications for conservation.