More than just indicators: A review of tropical butterfly ecology and conservation

Roughly 90% of butterfly species live in the tropics. Despite this, we know very little about tropical butterfly ecology particularly when compared to temperate butterfly systems. The relative scarcity of data on tropical butterfly populations hampers our ability to effectively conserve them. In this review we summarize recurring themes from ecological research on tropical butterflies to serve as a framework for understanding their conservation. Key themes include: (1) the tropics represent the evolutionary origins of butterfly diversity, (2) while some tropical butterflies exhibit relatively stable population dynamics, longer-lived adult stages, and more continuous age-specific reproduction compared to temperate zone species, the generality of these patterns is debatable, and (3) complex species interactions (e.g. mimicry, parasitism and predation) can have significantly greater influences on ecological and evolutionary processes in tropical butterflies than in temperate ones. This state of ecological knowledge, combined with scarce resources, has traditionally constrained tropical butterfly conservation efforts to habitat level approaches, unlike the species- and population-specific approaches familiar in North America and Europe. Consequently, much conservation research on butterflies in the tropics has focused on the relationship between habitat quality (e.g. forest fragmentation) and butterfly diversity, though predictive patterns even in this regard remain elusive. We argue that with the increasing threats of habitat destruction, fragmentation and climate change, it is necessary to move beyond this diversity and habitat relationship if we are to improve predictive capabilities when evaluating anthropogenic impacts on tropical butterfly communities. Tropical butterflies are more than just useful indicator species. They represent some of the most spectacular and visually appealing organisms in the world and play many vital roles in tropical ecosystems. We hope that this synthesis will lay the groundwork for future ecological studies of tropical butterfly populations, species, communities and conservation.     

The effects of invasive North American beavers on riparian plant communities in Cape Horn, Chile: Do exotic beavers engineer differently in sub-Antarctic ecosystems?

North American beavers (Castor canadensis) were introduced into southern South America in 1946. Since that time, their populations have greatly expanded. In their native range, beavers shape riparian ecosystems by selectively feeding on particular plant species, increasing herbaceous richness and creating a distinct plant community. To test their effects as exotic engineers on sub-Antarctic vegetation, we quantified beaver impacts on tree canopy cover and seedling abundance and composition, as well as their impacts on herbaceous species richness, abundance and composition on Navarino Island, Cape Horn County, Chile (55°S). Beavers significantly reduced forest canopy up to 30 m away from streams, essentially eliminating riparian forests. The tree seedling bank was greatly reduced and seedling species composition was changed by suppressing Nothofagus betuloides and Nothofagus pumilio, but allowing Nothofagus antarctica. Herbaceous richness and abundance almost doubled in meadows. However, unlike beaver effects on North American herbaceous plant communities, much of this richness was due to invasion by exotic plants, and beaver modifications of the meadow vegetation assemblage did not result in a significantly different community, compared to forests. Overall, 42% of plant species were shared between both habitat types. Our results indicate that, as predicted from North American studies, beaver-engineering increased local herbaceous richness. Unlike in their native range, though, they did not create a unique plant community in sub-Antarctic landscapes. Plus, the elimination of Nothofagus forests and their seedling bank and the creation of invasion pathways for exotic plants together threaten one of the world’s most pristine temperate forest ecosystems.     

Flower preferences of woodland butterflies in the UK: nectaring specialists are species of conservation concern

We report on a long-term study of the flower preferences of feeding adult butterflies undertaken in the Wyre Forest, UK. Examination of 5638 observations of nectar-feeding clearly demonstrates several findings: (i) that butterflies differ in their range of flower use, some are generalists and others specialists, respectively, exploiting more or less sources than expected; (ii) certain flower species are preferred over others. We find that (iii) generalism and specialism in flower use corresponds to generalism and specialism, respectively, in larval host range and biotope occupancy; that (iv) generalism in flower use is accounted for by life history and resource variables that increase opportunity for contact with a wider variety of flowering herbs; that (v) specialist flower users are more typically woodland butterflies and generalist flower users species of more open biotopes. A key finding is that (vi) many specialist flower users are butterfly species of conservation concern listed in Biodiversity Action Plans. We suggest that management of woodland sites for butterfly conservation should give as much consideration to nectar sources as to host plant sources.     

Conservation in a city: Do the same principles apply to different taxa?

Factors shaping overall species richness and representation of endangered species of vascular flora and butterflies were determined in 48 nature reserves in Prague, Czech Republic. Total species richness of both groups, and the presence of endangered butterflies, reflect the present status of habitats, while that of endangered plants reflects habitat composition at the time of reserve establishment. Reserve area has a much stronger effect on the species richness of sessile plants than mobile butterflies which, especially endangered species, respond more positively to heterogeneity than to area. Both species richness and endangered species peak in reserves half covered with forest, likely because they harbor species of both woodland and non-woodland habitats, and edge specialists. Solely relying on area and disregarding habitat quality, or a failure to conserve small but high quality sites, may be counterproductive for conserving endangered plant and butterfly species. To conserve diversity of plants and butterflies current management practices, often aimed at maintaining large blocks of pre-selected plant communities, should change to include maintenance of fallows, edges and transient zones.     

Does butterfly diversity predict moth diversity? Testing a popular indicator taxon at local scales

Indicator taxa are often proposed as efficient ways of identifying conservation priorities, but the correlation between putative indicators and other taxa has not been adequately tested. We examined whether a popular indicator taxon, the butterflies, could provide a useful surrogate measure of diversity in a closely related but relatively poorly known group, the moths, at a local scale relevant to many conservation decisions (10⁰-10¹ km²). We sampled butterflies and moths at 19 sites representing the three major terrestrial habitats in sub-alpine Colorado: meadows, aspen forests, and conifer forests. We found no correlation between moth and butterfly diversity across the 19 sites, using any of five different diversity measures. Correlations across only meadow sites (to test for correlation within a single, species-rich habitat) were also not significant. Butterflies were restricted largely to meadows, where their host plants occur and thermal environment is favorable. In contrast, all three habitats contained substantial moth diversity, and several moth species were restricted to each habitat. These findings suggest that (1) butterflies are unlikely to be useful indicators of moth diversity at a local scale; (2) phylogenetic relatedness is not a reliable criterion for selecting appropriate indicator taxa; and (3) a habitat-based approach would more effectively conserve moth diversity in this landscape and may be preferable in many situations where indicator taxa relationships are untested.     

Assessing habitat quality for butterflies on intensively managed arable farmland

The conservation and management of biodiversity requires accurate, repeatable and cost-effective monitoring techniques. In this study, a simple and rapid methodology was employed to measure the quality of different habitats for butterfly species on 10 arable farms in lowland Britain. This habitat monitoring was seven times more rapid than the traditional species-based butterfly monitoring. Data on butterfly abundance were combined with the information gathered on habitat quality at five of the farms using stepwise regression. These models had a consistently high degree of explanatory power for the summary variables of total butterfly abundance and species richness, and the functional groupings of mobile and immobile species. There was good agreement between observed and predicted estimates of species richness and abundance when the models were validated on a further five independent sites. Models to predict the abundance of 11 common butterfly species were also produced. These varied considerably in their predictive power and validity between species. The results clearly demonstrated the beneficial effects of targeted habitat creation for butterflies which is promoted under the Agri-environment Schemes, especially the recently introduced pollen and nectar seed mixtures (WM2) available under the Countryside Stewardship Scheme. The models confirmed the importance of shelter, floristically diverse field margins and the availability of nectar resources from legume species in explaining the abundance of immobile butterfly species in arable landscapes. These sources of nectar and the presence of larval host plants in the crucifer family were important factors in explaining the abundance of mobile species. The results are discussed in terms of the potential of this approach for: (i) assessing habitat quality for butterflies in intensively managed landscapes; (ii) enhancing the value of butterfly monitoring schemes in explaining changes in butterfly abundance at the site and national scale; and (iii) informing habitat management and restoration guidelines for butterfly conservation on arable farmland.     

Impacts of insect herbivores on rare plant populations

Population-level impacts of insect herbivory on rare and endangered plants are poorly understood, being frequently suggested but seldom quantified. We compiled 37 studies from the primary literature encompassing 35 rare plant species and at least 63 insect herbivore species, and assessed patterns in the effects of insect herbivores on rare plant populations and vital rates. Only three studies directly quantified effects of insect herbivory on population size or growth rate, with the vast majority instead extrapolating from vital rates to population size. Few studies (eight) studied herbivory experimentally, and feeding guilds other than seed predators have been relatively neglected. Estimates of population-level impacts vary extremely widely, but for many rare plants insect herbivores cause major reductions in survivorship or fecundity or can even drive local extinctions. Four studies documented positive (plant-) density dependence in insect attack, suggesting that herbivores may have a stabilizing influence on plant populations and thus may play a role in regulating rare plant population size. Most reported herbivores of rare plants are oligophagous or polyphagous, but monophagous herbivores of rare plants do exist, and there was no detectable difference in impact among specialization classes. Attack on rare plants by escaped biocontrol agents can sometimes have significant population-level effects, but such cases appear uncommon. Because insect herbivory can strongly suppress rare plant populations or vital rates, we need to know much more about what ecological and evolutionary factors determine the population-level impacts of insect herbivores. We suggest several ways in which the results of such research could inform conservation practices for rare plant species – for example, the possibility of different management regimes for plants under attack by monophagous, oligophagous, and polyphagous herbivores.     

Effects of anthropogenic land use on forest birds and butterflies in Subic Bay, Philippines

Despite the loss of 83% of native forests in the Philippines, little is known on the effects of this massive habitat loss and degradation on its forest biotas. This is a cause for concern because of the threat posed to the country’s large number of endemic taxa. To investigate the impacts of anthropogenic disturbance, forest birds and butterflies were surveyed in closed and open canopy forests, as well as suburban, rural and urban areas within the Subic Bay Watershed Reserve and Olongapo City in western Luzon. Measures of forest species richness and population densities for both taxa were similar in the two forest types, but showed different patterns in the other habitats. Indirect gradient analysis showed that forest bird species were positively correlated with vegetation variables (i.e., canopy cover, tree density, height to inversion and ground cover), while forest butterflies were not strongly correlated to any of the measured habitat variables. Community composition of birds in forests was distinct from those in modified habitats, while butterfly communities were more similar. A simulation showed that canopy cover of 60% or higher was required by 24 of the 26 bird species that were sensitive to canopy loss. Endemicity and nesting strata were the significant predictors of vulnerability to habitat disturbance for birds, while endemicity and larval hostplant specificity were significant for butterflies. Both taxa were negatively affected by anthropogenic disturbance but may respond to different components in the habitat (i.e., structure and resources), and thus cannot be used as surrogates of each other. Conservation of forests with contiguous canopy cover should be prioritized, and more ecological research is needed to improve the knowledge on the effects of disturbance on Philippine biodiversity.     

Applying IUCN criteria to invertebrates: How red is the Red List of European butterflies?

The IUCN is the leading authority on assessing species’ extinction risks worldwide and introduced the use of quantitative criteria for the compilation of Red Lists of threatened species. Recently, we assessed the threat status of the 483 European butterfly species, using semi-quantitative data on changes in distribution and in population sizes provided by national butterfly experts. We corrected distribution trends for the observation that coarse-scale grid cells underestimate actual population trends by 35%. To account for uncertainty, we included a 5% error margin on the distribution and population trends provided. The new Red List of European butterflies determined one species as Regionally Extinct, 37 species as threatened (Critically Endangered, Endangered or Vulnerable) and a further 44 as Near Threatened. The use of semi-quantitative data on distribution and population trends permitted us to use IUCN criteria to compile a scientifically underpinned Red List of butterflies in Europe. However, a comparison of detailed monitoring data for some grassland species showed that coarse-scale grid cell data and population trends strongly underestimate extinction risks, and the list should be taken as a conservative estimate of threat. Finally, combining the new Red List status with the data provided by the national butterfly experts, allowed us to determine simple criteria to delineate conservation priorities for butterflies in Europe, so called SPecies of European conservation Concern (SPEC’s). Using European butterflies, our approach illustrated how Red Listing can be performed when data are incomplete for some IUCN criteria or vary strongly among countries.     

Rarity,species richness and conservation: Butterflies of the Atlas Mountains in Morocco

A study was made of the butterflies associated with different biotopes in the Atlas mountains in Morocco. Geographically restricted species were found to be biotope specialists. These tend to be vulnerable species which warrant conservation measures, and are not necessarily the species which appear low in a rank species abundance curve. Butterfly species richness was correlated with plant species richness, and butterfly density with percentage ground cover of the vegetation. Many butterflies were restricted to particular seral stages. A comparison is made of the potential effectiveness of species versus ecosystem conservation in Morocco. As most species are poorly studied, probably the best conservation strategy for butterflies is to protect as wide a variety of biotopes as possible. Subsequently a species approach may be applied to species not encompassed by this policy.     

Exotic invasive knotweeds (Fallopia spp.) negatively affect native plant and invertebrate assemblages in European riparian habitats

Invasive plants are, simply by occupying a large amount of space in invaded habitats, expected to impose a significant impact on the native vegetation and their associated food webs. However, little is known about the impact of invasive plants both on native vegetation and on different invertebrate feeding guilds at the habitat level. Yet, studies addressing multiple trophic levels, e.g. plant species, herbivores, predators and detrivores, are likely to yield additional insight into how and under which conditions invasive weeds alter ecosystem structures and processes. We set out to assess whether plant species richness and invertebrate assemblages in European riparian habitats invaded by exotic knotweeds (Fallopia spp.) differed from those found in native grassland- or bush-dominated riparian habitats, which are both potentially threatened by knotweed invasion. Our findings suggest that riparian habitats invaded by knotweeds support lower numbers of plant species and lower overall abundance and morphospecies richness of invertebrates, compared to native grassland-dominated and bush-dominated habitats. Total invertebrate abundance and morphospecies richness in Fallopia-invaded riparian habitats were correlated with native plant species richness, suggesting that there is a link between the replacement of native plant species by exotic Fallopia species and the reduction in overall invertebrate abundance and morphospecies richness. Moreover, biomass of invertebrates sampled in grassland and bush-dominated habitats was almost twice as high as that in Fallopia-invaded habitats. Large-scale invasion by exotic Fallopia species is therefore likely to seriously affect biodiversity and reduce the quality of riparian ecosystems for amphibians, reptiles, birds and mammals whose diets are largely composed of arthropods.     

Movement of invasive aquatic plants into Minnesota (USA) through horticultural trade

The extent to which invasive aquatic plants move via accidental inclusion in aquatic plant orders or sale of prohibited species is unknown. Forty orders were placed to 34 aquatic plant vendors across the US between May and September 2001 to determine the prevalence of movement into Minnesota via horticultural trade. Federal noxious weeds or Minnesota prohibited exotic species were acquired 92% of the time they were ordered and included Alternanthera sessilis, Butomus umbellata, Hydrocharis morsus-ranae, Potamogeton crispus, and Lythrum salicaria. Ninety three percent of orders received from aquatic plant vendors contained a plant or animal species not specifically requested; 10% of these purchases contained federal noxious weeds or Minnesota exotic species. Lemna minor was the most common incidental receipt found per taxa and per purchase, although Hydrilla verticillata, Lythrum salicaria, Salvinia molesta, and Potamogeton crispus (all prohibited taxa) were also found. Misidentified plants were found in 18% of the orders; unordered seeds in 43%. The sale and transport of prohibited aquatic plants likely presents the greatest risk associated with the aquatic plant trade. Other important factors include misidentification leading to the unintentional sale of invasive plants and the incidental inclusion of species during translocation.     

Nectar plant sources for the threatened Apollo butterfly (Parnassius apollo L. 1758) in populations of central Spain

The use of flowers by the apollo butterfly at several sites along the Sierra de Guadarrama (central Spain) is documented. The Apollo butterfly uses a narrow range of flowers as nectar sources. Males feed more frequently on Armeria arenaria, Jasione montana and Carduus carpetanus. Females feed on the same species as males, but incorporate other species in their diet (Jurinea humilis, Thymus bracteata and Anthyllis lotoides). These observations also indicate that Parnassius apollo generally direct their foraging activities towards a limited number of the available plants but that the plants used can differ slightly between sites and change within sites through time. These data on resources for the adult butterflies should serve for the management of the species in future conservation programmes.     

Species groups occupying different trophic levels respond differently to the invasion of semi-natural vegetation by Solidago canadensis

We studied the impact of the invasive plant species Solidago canadensis on the species richness of vascular plants and the abundance, species richness and diversity of butterflies, hoverflies and carabid beetles in herbaceous semi-natural habitats near Ljubljana, Slovenia. The species groups were sampled in sites dominated by S. canadensis and paired nearby sites covered by semi-natural vegetation. Plant species richness and species richness, abundance and diversity of butterfly species were lower in plots dominated by S. canadensis. Hoverfly abundance, diversity and species richness were negatively affected only in July just before the onset of flowering of S. canadensis, but tended to be positively affected in August during the height of flowering of S. canadensis. Only the abundance of carabid beetles was reduced in plots dominated by S. canadensis. The responses of the insect groups seem largely driven by the effects of Solidago on the availability of essential resources like food or larval host plants. Our results suggest that insect species that are closely related to plant species composition are more vulnerable to the effects of invasive plant species than those that are loosely or only indirectly related to plant species composition.     

Impacts of selective logging on canopy and ground assemblages of tropical forest butterflies: Implications for sampling

Commercial selective logging is a major cause of habitat disturbance in Southeast Asian rainforests, yet despite much research there is little consensus on impacts of disturbance on biodiversity. There is also little consensus on the most appropriate methods for sampling tropical species, making it difficult to draw general conclusions from published studies. For example, many studies have used butterflies to assess impacts of selective logging but sampling has usually been conducted at ground level and the canopy fauna has often been ignored. In this study, we investigate the importance of sampling in the canopy by using fruit-baited traps to investigate impacts of selective logging on Nymphalid butterflies in primary forest and forest selectively logged 15 years previously in Sabah (Malaysian Borneo). Analysing combined data from canopy (≈25 m above ground level) and ground-level traps showed significantly lower diversity in selectively logged forest. However, this difference was not observed when data from only ground traps were analysed. Primary forest supported a butterfly assemblage comprising species with more restricted geographical ranges, and thus higher conservation value, compared with selectively logged forest. This result was observed regardless of whether or not canopy data were included in this analysis. We conclude that sampling in the canopy is critical when producing species inventories, but of little importance when determining the impacts of selective logging on restricted-range species.     

白头叶猴采食植物的再研究

2006年使用了较先进的录像设备,结合单筒望远镜对白头叶猴进行了全天候的跟踪观察和录像,使我们有可能更准确地仔细鉴定白头叶猴采食的植物及采食部位,也为动物生态的研究提供一个可重复验证的方法。经统计分析发现:白头叶猴属热带分布的灵长类动物,全以植物的各部分器官为食;被采食的植物大多数为热带分布的物种,是当地植被重要的建群种或优势种;在白头叶猴采食的物种中,有一部分是人类使用的药用植物;其中落叶成分和喜钙植物都较多;初步认为白头叶猴对不同的植物其喜食程度有明显不同。     

Flora and lepidoptera fauna adversely affected by invasive Lupinus polyphyllus along road verges

An increasing number of invasive species are changing ecosystems around the world. Road verges have commonly become the first footholds of non-native species in the new environments. Regularly mown road verges also offer habitats for meadow flora and fauna, which in Europe have suffered from the radical decline of semi-natural biotopes due to the agricultural modernization. We studied impacts of an invasive plant Lupinus polyphyllus on the plant and Lepidoptera species composition along road verges. The plant species composition was studied on 15 sites (with 1 m² quadrats) and butterflies and diurnal moths along 15 transects (with weekly censuses) in SE Finland, each site and transect representing equally lupine invaded verge and an adjacent non-lupine verge. The species richness and diversity of flora and the cover and species richness of low growing (<20 cm) species, in particular, was lower in lupine verges compared to non-lupine verges. Also, the abundance of butterflies was lower in lupine verges. As the lupine cover approached 100%, fewer butterflies were observed in lupine transects compared to the adjacent non-lupine transects and a higher proportion of individuals were flying. Our results suggest that the changes in plant species assemblages and lower plant species richness in lupine invaded areas had “bottom-up” effects on higher trophic levels. Further studies on the control of lupine are urgently needed, but meanwhile we suggest regular mowing before the lupines have shed their seeds, together with the removal of the cuttings, to be the best management option.     

Nematofauna associated with exotic and native leguminous plant species in West Africa: effect of<Emphasis Type="Italic"> Glomus intraradices</Emphasis> arbuscular mycorrhizal symbiosis

Ten leguminous trees, four exotic species (Australian Acacia) and six indigenous species (three Sahelian Acacia spp. and three Sesbania spp.), were grown for 4 months in a natural Sahelian soil inoculated with or without the endomycorrhizal fungus, Glomus intraradices. In control trials, the determinant factor structuring the soil nematode fauna was the plant species, related plants having a similar influence on the nematode community in the soil. Soil nematode abundance increased from exotic acacias (3.3 g^-1 dry soil) to native acacias (11.5 g^-1 dry soil) and Sesbania species (17.6 g^-1 dry soil). Plant feeding nematodes (mainly Scutellonema and Tylenchorhynchus) were significantly less abundant under exotic acacias (1.4 g^-1 dry soil) than under native acacias (7.2 g^-1 dry soil) or Sesbania species (7.3 g^-1 dry soil). Bacterial feeding nematode density increased from exotic acacias (1.2 g^-1 dry soil) to native acacias (3.0 g^-1 dry soil) and Sesbania species (7.7 g^-1 dry soil) as total densities. However, the differences in the structure of the nematode communities between plant groups were suppressed in the presence of the mycorrhizal fungus. In fact, no difference in nematode densities remained between plant groups when G. intraradices developed in several dominant taxa belonging to different trophic groups, particularly: Tylenchorhynchus, Apelenchina, Cephalobus and Dorylaimoidea. This study clearly indicated that inoculation with the arbuscular mycorrhizal fungus G. intraradices diminished the plant-specific effect on the structure of the soil nematode community.