Heavy Extinctions of Forest Avifauna in Singapore: Lessons for Biodiversity Conservation in Southeast Asia

Abstract: The consequences of rapid rainforest clearance on native avifauna are poorly understood. In Southeast Asia, Singapore, a newly developing country, has had 95% of its native lowland rainforest cleared. Most of the rainforest was lost in the mid- to late-nineteenth century. We compared avifauna checklists from 1923, 1949, and 1998 to determine the extent of extinctions between 1923 and 1998 in Singapore. Of 203 diurnal bird species, 65 were extirpated in Singapore in the past 75 years. Four of these species were nonforest- dependent species, whereas 61 (94%) were forest bird species dependent on the primary or old secondary forest to survive. Twenty-six forest bird species became extinct between 1923 and 1949, whereas 35 forest species disappeared after 1949. We compared the body lengths, feeding guilds, and vertical feeding zones between extinct and extant forest bird species to determine whether extinction patterns were dependent on these characteristics. Larger forest bird species went extinct between 1923 and 1949. Body sizes, however, did not affect the loss of forest bird species between 1949 and 1998. We observed high losses of insectivorous birds; the insectivore-carnivore and insectivore-granivore guilds lost> 80% of the species present in 1923. The highest losses were among birds that fed in the canopy. None of the forest bird species are currently common (>100 individuals/species) within Singapore. Our study shows that more than half the forest avifauna became locally extinct after extensive deforestation. Based on this fact, the countries within Southeast Asia should reconsider their heavy deforestation practices.     

Dynamic reserve design with the union-find algorithm

When reserve networks are established over time, there is a risk that sites will be developed in areas planned for future reservation, reducing the effectiveness of reserves. We developed a dynamic reserve design model that maximizes the expected number of species conserved, taking account of the risk of future habitat loss and fragmentation. The model makes use of the union-find algorithm, which is an efficient method for maintaining a list of connected regions in a graph as nodes and edges are inserted. A simple extension of the algorithm allows us to efficiently determine, for each species, when a sequence of site selections results in a reserve in which the species can persist. The extension also allows us to determine when a sequence of deforestation events results in the species becoming non-viable. The dynamic reserve design model is much more effective than commonly used heuristics, particularly when multiple connected sites are required for species persistence. The model also is able to solve much larger problems with greater effectiveness than the only previous dynamic reserve design model that considered site connectivity relationships. The union-find algorithm has much scope for addressing ecological management problems in which dynamic connectivity needs to be considered.     

Variation in species losses from islands: artifacts, extirpation rates, or pre-fragmentation diversity?

Species are being lost from isolated reserves as predicted by ecological theory, prompting calls for larger reserves with higher species immigration rates. However, some large islands have lost a large proportion of their species, whereas some small islands have not lost any. Conservation efforts would be more efficient if the cause of such variation in the relationships among number of species lost, island size, and immigration rate were known. Observed species losses could be affected by the time since islands were isolated, species immigration rates, species extirpation rates, the pre-fragmentation diversity of the region relative to steady state, or overestimation of the pre-fragmentation diversity of islands. To test the last three hypotheses, I compared the intersection points of the island, intraprovincial, and interprovincial species-area relationships of terrestrial mammals from nine archipelagos of land-bridge islands and terrestrial habitat isolates. Species losses from three archipelagos were greater than expected due to reduced immigration rates alone, although I could not resolve if this was due to increased extirpation rates or overestimation of the pre-fragmentation diversity of the islands. Analysis of six archipelagos indicates that the diversity of mammals in two regions of North America is currently below steady state, probably due to the extinction of mammals and glacial retreat during the late Pleistocene. These results have direct implications for reserve planning. When provincial diversity is below steady state, some combinations of reserve size and species immigration rate will allow reserves to maintain their pre-isolation diversity. However, the diversity of provinces relative to steady state is likely to vary, so conservation of a given proportion of a province may not always conserve the same proportion of its species. I present a new species-area relationship for islands formed by fragmentation that replaces the parameter c (fitted constant) with a rotation point. Estimation of this rotation point will allow reserve planners to separate the effects of extirpation and immigration rates on species losses from islands, identify provinces that are below steady-state diversity, and estimate the combinations of reserve size and immigration rate that will prevent loss of species from reserves.     

Deforestation Predicts the Number of Threatened Birds in Insular Southeast Asia

The world's tropical forests are being cleared rapidly, and ecologists claim this is causing a massive loss of species. This claim has its critics. Can we predict extinctions from the extent of deforestation? We mapped the percentage of deforestation on the islands of the Philippines and Indonesia and counted the number of bird species found only on these islands. We then used the species-area relationship to calculate the number of species predicted to become globally extinct following deforestation on these islands. Next, we counted the numbers of insular southeast Asian endemic bird species considered threatened—i.e., those having "a high probability of extinction in the wild in the medium-term future"—in the latest summary Red Data Book. The numbers of extinctions predicted from deforestation and the numbers of species actually threatened are strikingly similar. This suggests we can estimate the size of the extinction crisis in once-forested regions from the extent of deforestation. The numbers of extinctions will be large. Without rapid and effective conservation, many of the species endemic to insular southeast Asia will soon be lost.     

Minimum viable metapopulation size, extinction debt, and the conservation of a declining species.

A key question facing conservation biologists is whether declines in species' distributions are keeping pace with landscape change, or whether current distributions overestimate probabilities of future persistence. We use metapopulations of the marsh fritillary butterfly Euphydryas aurinia in the United Kingdom as a model system to test for extinction debt in a declining species. We derive parameters for a metapopulation model (incidence function model, IFM) using information from a 625-km2 landscape where habitat patch occupancy, colonization, and extinction rates for E. aurinia depend on patch connectivity, area, and quality. We then show that habitat networks in six extant metapopulations in 16-km2 squares were larger, had longer modeled persistence times (using IFM), and higher metapopulation capacity (lambdaM) than six extinct metapopulations. However, there was a > 99% chance that one or more of the six extant metapopulations would go extinct in 100 years in the absence of further habitat loss. For 11 out of 12 networks, minimum areas of habitat needed for 95% persistence of metapopulation simulations after 100 years ranged from 80 to 142 ha (approximately 5-9% of land area), depending on the spatial location of habitat. The area of habitat exceeded the estimated minimum viable metapopulation size (MVM) in only two of the six extant metapopulations, and even then by only 20%. The remaining four extant networks were expected to suffer extinction in 15-126 years. MVM was consistently estimated as approximately 5% of land area based on a sensitivity analysis of IFM parameters and was reduced only marginally (to approximately 4%) by modeling the potential impact of long-distance colonization over wider landscapes. The results suggest a widespread extinction debt among extant metapopulations of a declining species, necessitating conservation management or reserve designation even in apparent strongholds. For threatened species, metapopulation modeling is a potential means to identify landscapes near to extinction thresholds, to which conservation measures can be targeted for the best chance of success.     

The Value of Biodiversity in Reserve Selection: Representation, Species Weighting, and Benefit Functions

Abstract:  The limited availability of resources for conservation has led to the development of many quantitative methods for selecting reserves that aim to maximize the biodiversity value of reserve networks. In published analyses, species are often considered equal, although some are in much greater need of protection than others. Furthermore, representation is usually treated as a threshold: a species is either represented or not, but varying levels of representation over or under a given target level are not valued differently. We propose that a higher representation level should also have higher value. We introduce a framework for reserve selection that includes species weights and benefit functions for under- and overrepresentation (number of locations for each species). We applied the method to conservation planning for herb-rich forests in southern Finland. Our use of benefit functions and weighting changed the identity of about 50% of the selected sites at different funding levels and improved the representation of rare and threatened species. We also identified a small area of additional land that would substantially enhance the existing reserve network. We suggest that benefit functions and species weighting should be considered as standard options in reserve-selection applications.     

The Ethics of Reviving Long Extinct Species

There now appears to be a plausible pathway for reviving species that have been extinct for several decades, centuries, or even millennia. I conducted an ethical analysis of de‐extinction of long extinct species. I assessed several possible ethical considerations in favor of pursuing de‐extinction: that it is a matter of justice; that it would reestablish lost value; that it would create new value; and that society needs it as a conservation last resort. I also assessed several possible ethical arguments against pursuing de‐extinction: that it is unnatural; that it could cause animal suffering; that it could be ecologically problematic or detrimental to human health; and that it is hubristic. There are reasons in favor of reviving long extinct species, and it can be ethically acceptable to do so. However, the reasons in favor of pursuing de‐extinction do not have to do with its usefulness in species conservation; rather, they concern the status of revived species as scientific and technological achievements, and it would be ethically problematic to promote de‐extinction as a significant conservation strategy, because it does not prevent species extinctions, does not address the causes of extinction, and could be detrimental to some species conservation efforts. Moreover, humanity does not have a responsibility or obligation to pursue de‐extinction of long extinct species, and reviving them does not address any urgent problem. Therefore, legitimate ecological, political, animal welfare, legal, or human health concerns associated with a de‐extinction (and reintroduction) must be thoroughly addressed for it to be ethically acceptable. La Ética de Revivir Especies Extintas Hace Mucho Tiempo Sandler     

Ex situ collections and their potential for the restoration of extinct plants

The alarming current and predicted species extinction rates have galvanized conservationists in their efforts to avoid future biodiversity losses, but for species extinct in the wild, few options exist. We posed the questions, can these species be restored, and, if so, what role can ex situ plant collections (i.e., botanic gardens, germplasm banks, herbaria) play in the recovery of plant genetic diversity? We reviewed the relevant literature to assess the feasibility of recovering lost plant genetic diversity with using ex situ material and the probability of survival of subsequent translocations. Thirteen attempts to recover species extinct in the wild were found, most of which used material preserved in botanic gardens (12) and seed banks (2). One case of a locally extirpated population was recovered from herbarium material. Eight (60%) of these cases were successful or partially successful translocations of the focal species or population; the other 5 failed or it was too early to determine the outcome. Limiting factors of the use of ex situ source material for the restoration of plant genetic diversity in the wild include the scarcity of source material, low viability and reduced longevity of the material, low genetic variation, lack of evolution (especially for material stored in germplasm banks and herbaria), and socioeconomic factors. However, modern collecting practices present opportunities for plant conservation, such as improved collecting protocols and improved cultivation and storage conditions. Our findings suggest that all types of ex situ collections may contribute effectively to plant species conservation if their use is informed by a thorough understanding of the aforementioned problems. We conclude that the recovery of plant species currently classified as extinct in the wild is not 100% successful, and the possibility of successful reintroduction should not be used to justify insufficient in situ conservation.     

Changes in Species Abundance, Distribution, and Diversity in a Central European Bird Community

We analyzed possible causes of changes in species abundance, range size, and diversity as well as extinctions and colonizations in a central European bird community. Using data from the semiquantitative "Lake Constance" breeding bird atlas, we demonstrated that changes in regional abundances from 1980–1981 to 1990–1992 of 151 coexisting bird species were influenced by breeding habitat and migratory status. Significant declines were found in populations of farmland species and long-distance migrants. Farmland species lost parts of their ranges but hardly changed in local abundance in sites where they still occurred. In contrast, declines in long-distance migrants were caused by significant declines in local abundance with only slight loss of occupied range. Regional extinctions and colonizations were predictable from overall population trends. For example, all species that went extinct were either farmland species or long-distance migrants. Avian community composition was influenced by disproportionate declines of abundant species. This led to declines in the total number of breeding pairs and in community biomass and to increases in community evenness, but to only slight declines in species richness. Future conservation efforts in Europe need to focus more on farmland species and on understanding causes for the declines of long-distance migrants.     

The Boundary-Quality Penalty: a Quantitative Method for Approximating Species Responses to Fragmentation in Reserve Selection

Abstract:  Aggregation of reserve networks is generally considered desirable for biological and economic reasons: aggregation reduces negative edge effects and facilitates metapopulation dynamics, which plausibly leads to improved persistence of species. Economically, aggregated networks are less expensive to manage than fragmented ones. Therefore, many reserve-design methods use qualitative heuristics, such as distance-based criteria or boundary-length penalties to induce reserve aggregation. We devised a quantitative method that introduces aggregation into reserve networks. We call the method the boundary-quality penalty (BQP) because the biological value of a land unit (grid cell) is penalized when the unit occurs close enough to the edge of a reserve such that a fragmentation or edge effect would reduce population densities in the reserved cell. The BQP can be estimated for any habitat model that includes neighborhood (connectivity) effects, and it can be introduced into reserve selection software in a standardized manner. We used the BQP in a reserve-design case study of the Hunter Valley of southeastern Australia. The BQP resulted in a more highly aggregated reserve network structure. The degree of aggregation required was specified by observed (albeit modeled) biological responses to fragmentation. Estimating the effects of fragmentation on individual species and incorporating estimated effects in the objective function of reserve-selection algorithms is a coherent and defensible way to select aggregated reserves. We implemented the BQP in the context of the Zonation method, but it could as well be implemented into any other spatially explicit reserve-planning framework .     

A robust nonparametric method for quantifying undetected extinctions

How many species have gone extinct in modern times before being described by science? To answer this question, and thereby get a full assessment of humanity's impact on biodiversity, statistical methods that quantify undetected extinctions are required. Such methods have been developed recently, but they are limited by their reliance on parametric assumptions; specifically, they assume the pools of extant and undetected species decay exponentially, whereas real detection rates vary temporally with survey effort and real extinction rates vary with the waxing and waning of threatening processes. We devised a new, nonparametric method for estimating undetected extinctions. As inputs, the method requires only the first and last date at which each species in an ensemble was recorded. As outputs, the method provides estimates of the proportion of species that have gone extinct, detected, or undetected and, in the special case where the number of undetected extant species in the present day is assumed close to zero, of the absolute number of undetected extinct species. The main assumption of the method is that the per‐species extinction rate is independent of whether a species has been detected or not. We applied the method to the resident native bird fauna of Singapore. Of 195 recorded species, 58 (29.7%) have gone extinct in the last 200 years. Our method projected that an additional 9.6 species (95% CI 3.4, 19.8) have gone extinct without first being recorded, implying a true extinction rate of 33.0% (95% CI 31.0%, 36.2%). We provide R code for implementing our method. Because our method does not depend on strong assumptions, we expect it to be broadly useful for quantifying undetected extinctions.     

Variance and Uncertainty in the Expected Number of Occurrences in Reserve Selection

Abstract:  Reserve selection often concerns the design of reserve networks for the long-term maintenance of biodiversity. We considered uncertainty in the context of three common reserve-selection formulations, the expected number of populations, proportional coverage of land-cover types, and the probability of having at least one population. By uncertainty, we mean variance in the outcome of any probability-based reserve selection formulation. A typical reserve-selection formulation might ask for the least expensive set of sites that contains n populations per species. It is implicit here that this requirement concerns the expected number of populations, which actually is obtained only with a 50% chance. If the requirement is changed to select the least expensive set of sites that gives n populations per species with a 95% probability, the number of sites required in the solution increases and the identity of the sites is changed toward sites that have high probabilities of persistence (or occurrence) and low associated binomial variance. Anthropogenic threat is one factor that may cause probabilistic uncertainty in the context of proportional area coverage.     

Extinction in a hyperdiverse endemic Hawaiian land snail family and implications for the underestimation of invertebrate extinction

The International Union for Conservation of Nature (IUCN) Red List includes 832 species listed as extinct since 1600, a minuscule fraction of total biodiversity. This extinction rate is of the same order of magnitude as the background rate and has been used to downplay the biodiversity crisis. Invertebrates comprise 99% of biodiversity, yet the status of a negligible number has been assessed. We assessed extinction in the Hawaiian land snail family Amastridae (325 species, IUCN lists 33 as extinct). We did not use the stringent IUCN criteria, by which most invertebrates would be considered data deficient, but a more realistic approach comparing historical collections with modern surveys and expert knowledge. Of the 325 Amastridae species, 43 were originally described as fossil or subfossil and were assumed to be extinct. Of the remaining 282, we evaluated 88 as extinct and 15 as extant and determined that 179 species had insufficient evidence of extinction (though most are probably extinct). Results of statistical assessment of extinction probabilities were consistent with our expert evaluations of levels of extinction. Modeling various extinction scenarios yielded extinction rates of 0.4‐14.0% of the amastrid fauna per decade. The true rate of amastrid extinction has not been constant; generally, it has increased over time. We estimated a realistic average extinction rate as approximately 5%/decade since the first half of the nineteenth century. In general, oceanic island biotas are especially susceptible to extinction and global rate generalizations do not reflect this. Our approach could be used for other invertebrates, especially those with restricted ranges (e.g., islands), and such an approach may be the only way to evaluate invertebrates rapidly enough to keep up with ongoing extinction.     

Maximal yields from multispecies fisheries systems: rules for systems with multiple trophic levels.

Increasing centralization of the control of fisheries combined with increased knowledge of food-web relationships is likely to lead to attempts to maximize economic yield from entire food webs. With the exception of predator-prey systems, we lack any analysis of the nature of such yield-maximizing strategies. We use simple food-web models to investigate the nature of yield- or profit-maximizing exploitation of communities including two types of three-species food webs and a variety of six-species systems with as many as five trophic levels. These models show that, for most webs, relatively few species are harvested at equilibrium and that a significant fraction of the species is lost from the web. These extinctions occur for two reasons: (1) indirect effects due to harvesting of species that had positive effects on the extinct species, and (2) intentional eradication of species that are not themselves valuable, but have negative effects on more valuable species. In most cases, the yield-maximizing harvest involves taking only species from one trophic level. In no case was an unharvested top predator part of the yield-maximizing strategy. Analyses reveal that the existence of direct density dependence in consumers has a large effect on the nature of the optimal harvest policy, typically resulting in harvest of a larger number of species. A constraint that all species must be retained in the system (a "constraint of biodiversity conservation") usually increases the number of species and trophic levels harvested at the yield-maximizing policy. The reduction in total yield caused by such a constraint is modest for most food webs but can be over 90% in some cases. Independent harvesting of species within the web can also cause extinctions but is less likely to do so.     

Protected Areas and Prospects for Endangered Species Conservation in Canada

Abstract:  Reserve networks figure prominently in conservation strategies that aim to reduce extinction rates. We tested the effectiveness of the current reserve network at protecting species at risk in Canada, where relatively extensive wilderness areas remain. We compared numbers of terrestrial species at risk included in existing reserves to randomly generated networks with the same total area and number of reserves. Existing reserve networks rarely performed better than randomly selected areas and several included fewer endangered species than expected by chance, particularly in the most biologically imperiled regions. The extent of protected area and density of species at risk were unrelated at either broad (countrywide) or finer spatial scales (50 × 50 km grids), although there was a tendency for the most threatened regions of the country to have few or no protected areas (1.5% of areas with >30 endangered species were in reserves). Although reserves will play a useful role in conserving endangered species that occur within them, reducing extinction rates in a region with much of the world's remaining wilderness will require integrating conservation strategies with agricultural and urban land-use plans outside formally protected areas.     

Reserve networks based on richness hotspots and representation vary with scale.

While the importance of spatial scale in ecology is well established, few studies have investigated the impact of data grain on conservation planning outcomes. In this study, we compared species richness hotspot and representation networks developed at five grain sizes. We used species distribution maps for mammals and birds developed by the Arizona and New Mexico Gap Analysis Programs (GAP) to produce 1-km2, 100-kmn2, 625-km2, 2500-km2, and 10,000-km2 grid cell resolution distribution maps. We used these distribution maps to generate species richness and hotspot (95th quantile) maps for each taxon in each state. Species composition information at each grain size was used to develop two types of representation networks using the reserve selection software MARXAN. Reserve selection analyses were restricted to Arizona birds due to considerable computation requirements. We used MARXAN to create best reserve networks based on the minimum area required to represent each species at least once and equal area networks based on irreplaceability values. We also measured the median area of each species' distribution included in hotspot (mammals and birds of Arizona and New Mexico) and irreplaceability (Arizona birds) networks across all species. Mean area overlap between richness hotspot reserves identified at the five grain sizes was 29% (grand mean for four within-taxon/state comparisons), mean overlap for irreplaceability reserve networks was 32%, and mean overlap for best reserve networks was 53%. Hotspots for mammals and birds showed low overlap with a mean of 30%. Comparison of hotspots and irreplaceability networks showed very low overlap with a mean of 13%. For hotspots, median species distribution area protected within reserves declined monotonically from a high of 11% for 1-km2 networks down to 6% for 10,000-km2 networks. Irreplaceability networks showed a similar, but more variable, pattern of decline. This work clearly shows that map resolution has a profound effect on conservation planning outcomes and that hotspot and representation outcomes may be strikingly dissimilar. Thus, conservation planning is scale dependent, such that reserves developed using coarse-grained data do not subsume fine-grained reserves. Moreover, preserving both full species representation and species rich areas may require combined reserve design strategies.     

Modeling the impacts of hunting on the population dynamics of red howler monkeys (Alouatta seniculus)

Overexploitation of wildlife populations occurs across the humid tropics and is a significant threat to the long-term survival of large-bodied primates. To investigate the impacts of hunting on primates and ways to mitigate them, we developed a spatially explicit, individual-based model for a landscape that included hunted and un-hunted areas. We used the large-bodied neotropical red howler monkey (Alouatta seniculus) as our case study species because its life history characteristics make it vulnerable to hunting. We modeled the influence of different rates of harvest and proportions of landscape dedicated to un-hunted reserves on population persistence, population size, social dynamics, and hunting yields of red howler monkeys. In most scenarios, the un-hunted populations maintained a constant density regardless of hunting pressure elsewhere, and allowed the overall population to persist. Therefore, the overall population was quite resilient to extinction; only in scenarios without any un-hunted areas did the population go extinct. However, the total and hunted populations did experience large declines over 100 years under moderate and high hunting pressure. In addition, when reserve area decreased, population losses and losses per unit area increased disproportionately. Furthermore, hunting disrupted the social structure of troops. The number of male turnovers and infanticides increased in hunted populations, while birth rates decreased and exacerbated population losses due to hunting. Finally, our results indicated that when more than 55% of the landscape was harvested at high (30%) rates, hunting yields, as measured by kilograms of biomass, were less than those obtained from moderate harvest rates. Additionally, hunting yields, expressed as the number of individuals hunted/year/km², increased in proximity to un-hunted areas, and suggested that dispersal from un-hunted areas may have contributed to hunting sustainability. These results indicate that un-hunted areas serve to enhance hunting yields, population size, and population persistence in hunted landscapes. Therefore, spatial regulation of hunting via a reserve system may be an effective management strategy for sustainable hunting, and we recommend it because it may also be more feasible to implement than harvest quotas or restrictions on season length.     

Predator-prey spatial game as a tool to understand the effects of protected areas on harvester-wildlife interactions

No-take reserves are sometimes implemented for sustainable population harvesting because they offer opportunities for animals to spatially avoid harvesters, whereas harvesters can benefit in return from the reserve spillover. Here, we used the framework of predator-prey spatial games to understand how protected areas shape spatial interactions between harvesters and target species and determine animal mortality. In these spatial games, the "predator" searches for "prey" and matches their habitat use, unless it meets spatial constraints offering the opportunity for prey to avoid the mortality source. However, such prey refuges could attract predators in the surroundings, which questions the potential benefits for prey. We located, in the Geneva Basin (France), hunting dogs and wild boar Sus scrofa L. during hunting seasons with global positioning systems and very-high-frequency collars. We quantified how the proximity of the reserve shaped the matching between both habitat uses using multivariate analyses and linked these patterns to animals' mortality with a Cox regression analysis. Results showed that habitat uses by both protagonists disassociated only when hunters were spatially constrained by the reserve. In response, hunters increased hunting efforts near the reserve boundary, which induced a higher risk exposure for animals settled over the reserve. The mortality of adult wild boar decreased near the reserve as the mismatch between both habitat uses increased. However the opposite pattern was determined for younger individuals that suffered from the high level of hunting close to the reserve. The predator-prey analogy was an accurate prediction of how the protected area modified spatial relationships between harvesters and target species. Prey-searching strategies adopted by hunters around reserves strongly impacted animal mortality and the efficiency of the protected area for this harvested species. Increasing reserve sizes and/or implementing buffer areas with harvesting limitations can dampen this edge effect and helps harvesters to benefit durably from source populations of reserves. Predator-prey spatial games therefore provide a powerful theoretical background for understanding wildlife-harvester spatial interactions and developing substantial application for sustainable harvesting.     

Catastrophe management and inter-reserve distance for marine reserve networks

We consider the optimal spacing between marine reserves for maximising the viability of a species occupying a reserve network. The closer the networks are placed together, the higher the probability of colonisation of an empty reserve by an occupied reserve, thus increasing population viability. However, the closer the networks are placed together, the higher the probability that a catastrophe will cause extinction of the species in both reserves, thus decreasing population viability. Using a simple discrete-time Markov chain model for the presence or absence of the species in each reserve we determine the distance between the two reserves which provides the optimal trade-off between these processes, resulting in maximum viability of the species.