Ecological Uses of Vertebrate Indicator Species: A Critique

Abstract: Plant and animal species have been used for decades as indicators of air and water quality and agricultural and range conditions. Increasingly, vertebrates are used to assess population trends and habitat quality for other species. In this paper we review the conceptual bases, assumptions, and published guidelines for selection and use of vertebrates as ecological indicators. We conclude that an absence of precise definitions and procedures, confounded criteria used to select species, and discordance with ecological literature severely weaken the effectiveness and credibility of using vertebrates as ecological indicators. In many cases the use of ecological indicator species is inappropriate, but when necessary, the following recommendations will make their use more rigorous: (1) clearly state assessment goals, (2) use indicators only when other assessment options are unavailable, (3) choose indicator species by explicitly defined criteria that are in accord with assessment goals, (4) include all species that fulfill stated selection criteria (5) know the biology of the indicator in detail, and treat the indicator as a formal estimator in conceptual and statistical models, (6) identify and define sources of subjectivity when selecting monitoring and intetpreting indicator species, (7) submit assessment design, methods of data collection and statistical analysis, interpretations, and recommendations to peer review and (8) direct research at developing an overall strategy for monitoring wildlife that accounts for natural variability in population attributes and incorporates concepts from landscape ecology.     

Quantifying the Indicator Power of an Indicator Species

Abstract:  Biodiversity indicator species are needed for classifying biotopes and sites for conservation, and a number of methods have been developed for determining indicator species for this purpose. Nevertheless, in addition to site classification, there is sometimes a need to define an indicator species that indicates the occurrence of another species. For example, when a species of interest (target species) is difficult to detect or identify, a reliable indicator species can function as a tool that saves time and money. We derived a method that provides a quantitative measure of the indicator power (IP) of an indicator species for the target species or any species assemblage. We calculated the measure of IP from a presence–absence matrix that covered several sites. The method provided a list of indicator species, the presence of which reliably indicated the presence of another species (e.g., a threatened or rare species in a given area). The IP of the species was highest when the number of shared occurrences between the indicator species and the target species was high and, simultaneously, when the indicator species and the target species occurred separately in only a few cases. The IP was also positively influenced by the number of sites with no occurrences of either the indicator or the target species. Our method can also be used to quantify different types of species occurrence indications. We refer to these types as presence–presence, presence–absence, absence–presence, and absence–absence indications. To clarify the use of the method, we examined the situation with red-listed polypores in White-backed Woodpecker (Dendrocopos leucotos) habitats in Fennoscandia and found some suitable indicator species. Our method provides a new, objective way to evaluate the IP of an indicator species.     

Vulnerability and Resilience of Tropical Forest Species to Land‐Use Change

Abstract: We provide a cross‐taxon and historical analysis of what makes tropical forest species vulnerable to extinction. Several traits have been important for species survival in the recent and distant geological past, including seed dormancy and vegetative growth in plants, small body size in mammals, and vagility in insects. For major past catastrophes, such as the five mass extinction events, large range size and vagility or dispersal were key to species survival. Traits that make some species more vulnerable to extinction are consistent across time scales. Terrestrial organisms, particularly animals, are more extinction prone than marine organisms. Plants that persist through dramatic changes often reproduce vegetatively and possess mechanisms of die back. Synergistic interactions between current anthropogenic threats, such as logging, fire, hunting, pests and diseases, and climate change are frequent. Rising temperatures threaten all organisms, perhaps particularly tropical organisms adapted to small temperature ranges and isolated by distance from suitable future climates. Mutualist species and trophic specialists may also be more threatened because of such range‐shift gaps. Phylogenetically specialized groups may be collectively more prone to extinction than generalists. Characterization of tropical forest species’ vulnerability to anthropogenic change is constrained by complex interactions among threats and by both taxonomic and ecological impediments, including gross undersampling of biotas and poor understanding of the spatial patterns of taxa at all scales.     

A Successful Predictive Model of Species Richness Based on Indicator Species

Abstract:  Because complete species inventories are expensive and time-consuming, scientists and land managers seek techniques to alleviate logistic constraints on measuring species richness, especially over large spatial scales. We developed a method to identify indicators of species richness that is applicable to any taxonomic group or ecosystem. In an initial case study, we found that a model based on the occurrence of five indicator species explained 88% of the deviance of species richness of 56 butterflies in a mountain range in western North America. We validated model predictions and spatial transferability of the model using independent, newly collected data from another, nearby mountain range. Predicted and observed values of butterfly species richness were highly correlated with 93% of the observed values falling within the 95% credible intervals of the predictions. We used a Bayesian approach to update the initial model with both the model-building and model-validation data sets. In the updated model, the effectiveness of three of the five indicator species was similar, whereas the effectiveness of two species was reduced. The latter species had more erratic distributions in the validation data set than in the original model-building data set. This objective method for identifying indicators of species richness could substantially enhance our ability to conduct large-scale ecological assessments of any group of animals or plants in any geographic region and to make effective conservation decisions.     

Use of Market Data to Assess Bushmeat Hunting Sustainability in Equatorial Guinea

Abstract: Finding an adequate measure of hunting sustainability for tropical forests has proved difficult. Many researchers have used urban bushmeat market surveys as indicators of hunting volumes and composition, but no analysis has been done of the reliability of market data in reflecting village offtake. We used data from urban markets and the villages that supply these markets to examine changes in the volume and composition of traded bushmeat between the village and the market (trade filters) in Equatorial Guinea. We collected data with market surveys and hunter offtake diaries. The trade filters varied depending on village remoteness and the monopoly power of traders. In a village with limited market access, species that maximized trader profits were most likely to be traded. In a village with greater market access, species for which hunters gained the greatest income per carcass were more likely to be traded. The probability of particular species being sold to market also depended on the capture method and season. Larger, more vulnerable species were more likely to be supplied from less‐accessible catchments, whereas there was no effect of forest cover or human population density on probability of being sold. This suggests that the composition of bushmeat offtake in an area may be driven more by urban demand than the geographic characteristics of that area. In one market, traders may have reached the limit of their geographical exploitation range, and hunting pressure within that range may be increasing. Our results demonstrate that it is possible to model the trade filters that bias market data, which opens the way to developing more robust market‐based sustainability indices for the bushmeat trade.     

Protected-Area Monitoring Dilemmas: a New Tool to Assess Success

Abstract:  Understanding factors that influence the success of protected areas in curbing unsustainable resource consumption is essential for determining best management strategies and allocating limited resources to those projects most likely to succeed. I used a law-enforcement and monitoring game-theory model from the political science literature to identify three key variables useful in predicting the success of a protected area: costs of monitoring for rule breakers, benefits of catching a rule breaker, and probability of catching a rule breaker if monitoring. Although assigning exact values for each of these variables was difficult, the variables had a strong predictive capacity even when coded as coarse ordinal values. A model in which such values were used correctly predicted the outcome of 88 of 116 protected areas sampled from the peer-reviewed literature. The model identified a critical zone of common mismatch between protected-area circumstances and management policies. In situations where the costs of monitoring were greater than the product of the probability of catching a rule breaker and the benefit of doing so, conservation was unlikely to succeed. Control of illegal use of protected resources was reported in only 8% of such cases, regardless of strategies to motivate potential users to cooperate with conservation. My model does not prescribe a best management policy for conserving natural resources; rather, it can be used as a tool to help predict whether a proposed management policy will likely succeed in a given situation.     

Conservation Status as a Biodiversity Trend Indicator: Recommendations from a Decade of Listing Species at Risk in British Columbia

Abstract:  Species conservation status is commonly used as a broad-scale indicator of the state of biological diversity. To learn about its value for tracking trends, we examined provincial lists of terrestrial vertebrate species and subspecies at risk in British Columbia, Canada, for 1992 and 2002 to see whether changes in these lists reflected changes in the status of the taxa they represent. Examination of the case histories of individual species and subspecies showed that 65% of additions and deletions to the British Columbia Red List were the result of improvement in knowledge of species status, changes in assessment procedures, and refinements in taxonomy rather than actual changes in a species' status. Comparison to an alternate set of rank scores provided by NatureServe for taxa that appeared on both 1992 and 2002 British Columbia Red Lists revealed changes in status that were not reflected by movement from the list. Estimates of historical conservation status for species on the 1992 British Columbia Red List demonstrated ambiguity around the natural baseline with regard to tracking changes in list composition over time. We discourage the continued use of indicators based solely on conservation status as a means of tracking biodiversity. Instead we recommend advancing strategic indicators around species at risk based on long-term monitoring data, deliberate and explicitly stated baselines, and consistent methods of conservation ranking.     

Forest Restoration on a Closed Landfill: Rapid Addition of New Species by Bird Dispersal

Urban areas often contain sizeable pockets of degraded land, such as inactive landfills, that could be reclaimed as wildlife habitat and as connecting links to enhance remnant natural areas. In the northeastern U.S., many such lands fail to undergo natural succession to woodland, instead retaining a weedy, herbaceous cover for many years. We hypothesize that seed dispersal is a limiting factor, and that a form of secondary succession could be stimulated by introducing clusters of trees and shrubs to attract avian seed dispersers. As a direct test, we censused a 1.5-ha experimental plantation on the Fresh Kills Landfill (Staten Island, New York) one year after installation, in search of evidence that the plantation was spreading or increasing in diversity. The 17 planted species, many from coastal scrub forests native to this region, were surviving well but contributed almost no seedlings to the area, in part because only 20% of the installed trees or shrubs were reproductive. Of the 1079 woody seedlings found, 95% came from sources outside the plantation; most (71%) were from fleshy-fruited, bird-dispersed plants from nearby woodland fringes. Although the restoration planting itself had not begun to produce seedlings, it did function as a site for attracting dispersers, who enriched the young community with 20 new species. One-fourth of all new recruits were from nine additional wind-dispersed species. Locations with a high ratio of trees to shrubs had proportionately more recruits, indicating that plant size contributed to disperser attraction. The density of new recruits of each species was dependent on distance from the nearest potential seed source. Introducing native species with the capacity to attract avian dispersers may be the key to success of many restoration programs.     

Use-Values of Tree Species in a Communal Forest Reserve in Northeast Peru

Abstract: Several rural villages in the department of Loreto, in northeast Peru, have sought to protect local control over access to natural resources by establishing communal reserves. Most of Loreto's villages have heterogeneous populations of detribalized Indians and mestizos, called ribereños (people of the riverbanks). The communal reserves of ribereño villages currently have no legal status, but are regulated by written communal rules and are actively guarded by community members.
An inventory of trees greater than 10 cm in diameter was conducted in one ribereño communal reserve, a fifty-year-old secondary forest. A doubly random sampling procedure was used producing a total sample size of 7.5 ha Tree species utilized by community members were found to comprise 60% of the total number of species sampled. Uses were divided into six categories: food construction, crafts remedy, commerce, and other "use-values" were assigned to each species, based on an ordinal system developed by Prance et al. (1987). The presence or absence of markets for specific forest products was found to be a major determinant of that species' overall use-value to ribereño populations. Neither the existing markets nor the lack of firm land or resource tenure for ribereño communal reserves encourages sustained management of forest resources.     

Use of Large‐Scale Acoustic Monitoring to Assess Anthropogenic Pressures on Orthoptera Communities

Biodiversity monitoring at large spatial and temporal scales is greatly needed in the context of global changes. Although insects are a species‐rich group and are important for ecosystem functioning, they have been largely neglected in conservation studies and policies, mainly due to technical and methodological constraints. Sound detection, a nondestructive method, is easily applied within a citizen‐science framework and could be an interesting solution for insect monitoring. However, it has not yet been tested at a large scale. We assessed the value of a citizen‐science program in which Orthoptera species (Tettigoniidae) were monitored acoustically along roads. We used Bayesian model‐averaging analyses to test whether we could detect widely known patterns of anthropogenic effects on insects, such as the negative effects of urbanization or intensive agriculture on Orthoptera populations and communities. We also examined site‐abundance correlations between years and estimated the biases in species detection to evaluate and improve the protocol. Urbanization and intensive agricultural landscapes negatively affected Orthoptera species richness, diversity, and abundance. This finding is consistent with results of previous studies of Orthoptera, vertebrates, carabids, and butterflies. The average mass of communities decreased as urbanization increased. The dispersal ability of communities increased as the percentage of agricultural land and, to a lesser extent, urban area increased. Despite changes in abundances over time, we found significant correlations between yearly abundances. We identified biases linked to the protocol (e.g., car speed or temperature) that can be accounted for ease in analyses. We argue that acoustic monitoring of Orthoptera along roads offers several advantages for assessing Orthoptera biodiversity at large spatial and temporal extents, particularly in a citizen science framework. El Uso de Monitoreos Acústicos a Gran Escala para Estudiar las Presiones Antropogénicas sobre Comunidades de Orthoptera     

Use of Stress‐Hormone Levels and Habitat Selection to Assess Functional Connectivity of a Landscape for an Amphibian

Abstract: The influence of landscape matrix on functional connectivity has been clearly established. Now methods to assess the effects of different land uses on species’ movements are needed because current methods are often biased. The use of physiological parameters as indicators of the level of resistance to animal movement associated with different land uses (i.e., matrix resistance) could provide estimates of energetic costs and risks to animals migrating through the matrix. To assess whether corticosterone levels indicate matrix resistance, we conducted experiments on substrate choice and measured levels of corticosterone before and after exposure of toads (Bufo bufo) to 3 common substrates (ploughed soil, meadow, and forest litter). We expected matrix resistance and hormone levels to increase from forest litter (habitat of the toad) to meadows to ploughed soil. Adult toads had higher corticosterone levels on ploughed soil than on forest litter or meadow substrates. Hormone levels did not differ between forest litter and meadow. Toads avoided moving onto ploughed soil. Corticosterone levels in juvenile toads were not related to substrate type; however, hormone levels decreased as humidity increased. Juveniles, unlike adults, did not avoid moving over ploughed soil. The difference in responses between adult and juvenile toads may have been due to differences in experimental design (for juveniles, entire body used to measure corticosterone concentration; for adults, saliva alone); differences in the scale of sensory perception of the substrate (juveniles are much smaller than adults); or differences in cognitive processes between adult and juvenile toads. Adults probably had experience with different substrate types, whereas juveniles first emerging from the water probably did not. As a consequence, arable lands could act as ecological traps for juvenile toads.     

Use of Surrogates to Predict the Stressor Response of Imperiled Species

Abstract: Rare or narrowly distributed species may be threatened by stressors to which they have never been exposed or for which data are very limited. In such cases the species response cannot be predicted on the basis of directly measured data, but may be inferred from the response of one or more appropriate surrogate species. Here, I propose a practical way to use the stressor response of one or more surrogate species to develop a working hypothesis or model of the stressor response of the target species. The process has 4 steps: (1) identify one or more candidate surrogate species, (2) model the relationship between the stressor and the response variable of interest for the surrogate species, (3) adapt the stressor–response relationship from the surrogate species to a model for the target species, possibly using Bayesian methods, and (4) incorporate additional data as they become available and adjust the response model of the target species appropriately. I applied the approach to an endangered fish species, the amber darter (Percina antesella), which is potentially threatened by urbanization. I used a Bayesian approach to combine data from a surrogate species (the bronze darter[Percina palmaris]) with available data for the amber darter to produce a model of expected amber darter response. Although this approach requires difficult decisions on the part of the manager, especially in the selection of surrogate species, its value lies in the fact that all assumptions are clearly stated in the form of hypotheses, which may be scrutinized and tested. It therefore provides a rational basis for instituting management policy even in the face of considerable uncertainty.