Estimating the normal background rate of species extinction

A key measure of humanity's global impact is by how much it has increased species extinction rates. Familiar statements are that these are 100–1000 times pre‐human or background extinction levels. Estimating recent rates is straightforward, but establishing a background rate for comparison is not. Previous researchers chose an approximate benchmark of 1 extinction per million species per year (E/MSY). We explored disparate lines of evidence that suggest a substantially lower estimate. Fossil data yield direct estimates of extinction rates, but they are temporally coarse, mostly limited to marine hard‐bodied taxa, and generally involve genera not species. Based on these data, typical background loss is 0.01 genera per million genera per year. Molecular phylogenies are available for more taxa and ecosystems, but it is debated whether they can be used to estimate separately speciation and extinction rates. We selected data to address known concerns and used them to determine median extinction estimates from statistical distributions of probable values for terrestrial plants and animals. We then created simulations to explore effects of violating model assumptions. Finally, we compiled estimates of diversification—the difference between speciation and extinction rates for different taxa. Median estimates of extinction rates ranged from 0.023 to 0.135 E/MSY. Simulation results suggested over‐ and under‐estimation of extinction from individual phylogenies partially canceled each other out when large sets of phylogenies were analyzed. There was no evidence for recent and widespread pre‐human overall declines in diversity. This implies that average extinction rates are less than average diversification rates. Median diversification rates were 0.05–0.2 new species per million species per year. On the basis of these results, we concluded that typical rates of background extinction may be closer to 0.1 E/MSY. Thus, current extinction rates are 1,000 times higher than natural background rates of extinction and future rates are likely to be 10,000 times higher. Estimación de la Tasa Normal de Extinción de Especies     

Extinction debt of forest plants persists for more than a century following habitat fragmentation

Following habitat fragmentation individual habitat patches may lose species over time as they pay off their "extinction debt." Species with relatively low rates of population extinction and colonization ("slow" species) may maintain extinction debts for particularly prolonged periods, but few data are available to test this prediction. We analyzed two unusually detailed data sets on forest plant distributions and land-use history from Lincolnshire, United Kingdom, and Vlaams-Brabant, Belgium, to test for an extinction debt in relation to species-specific extinction and colonization rates. Logistic regression models predicting the presence-absence of 36 plant species were first parameterized using data from Lincolnshire, where forest cover has been relatively low (approximately 5-8%) for the past 1000 years. Consistent with extinction debt theory, for relatively slow species (but not fast species) these models systematically underpredicted levels of patch occupancy in Vlaams-Brabant, where forest cover was reduced from approximately 25% to <10% between 1775 and 1900 (it is presently 6.5%). As a consequence, the ability of the Lincolnshire models to predict patch occupancy in Vlaams-Brabant was worse for slow than for fast species. Thus, more than a century after forest fragmentation reached its current level an extinction debt persists for species with low rates of population turnover.     

Extinction Rates of North American Freshwater Fauna

Abstract: Since 1900, 123 freshwater animal species have been recorded as extinct in North America. Hundreds of additional species of fishes, mollusks, crayfishes, and amphibians are considered imperiled. Using an exponential decay model, we derived recent and future extinction rates for North American freshwater fauna that are five times higher than those for terrestrial fauna. Assuming that imperiled freshwater species will not survive throughout the next century, our model projects a future extinction rate of 4% per decade, which suggests that North America's temperate freshwater ecosystems are being depleted of species as rapidly as tropical forests.     

Plant Species Lost in an Isolated Conservation Area in Metropolitan Boston from 1894 to 1993

A recensus was undertaken of the Middlesex Fells (West), a 400-ha woodland park in Metropolitan Boston, to determine how species composition changed between 1894 (the time of first census) and 1993. This park is isolated by an 0.5-km-wide barrier of roads and development from the eastern half of the Fells preserve, is at least 5 km from other protected areas, and is strongly affected by human activity. Out of 422 original plant species, 155 species were no longer present in 1993. Sixty-four new species were recorded on the site in 1993, the majority of them exotic species. The proportion of native species in the flora went from 83% in 1894 to 74% in 1993. Overall, the number of native species is declining at a rate of O.36% per year, whereas the exotic species are increasing at a rate of 0.18% per year. Many of the native species lost were attractive and well-known components of the native flora, such as orchids and lobeliads. Many remaining native plant species have been reduced to one or a few small populations. Species of moist woods were disproportionately lost from the Fells. The loss of species has coincided with an increase in human activity, including ground fires, a greater number of trails and roads, thinning of the forest, and trampling of the vegetation, all of which may have contributed to species loss. A policy to stop and reverse this progressive loss of species might include preventing new trails from being developed, closing off some existing trails, excluding people from sensitive areas, and reintroducing some of the lost species.     

Nest Poaching in Neotropical Parrots

Abstract: Although the poaching of nestlings for the pet trade is thought to contribute to the decline of many species of parrots, its effects have been poorly demonstrated. We calculated rates of mortality due to nest poaching in 23 studies of Neotropical parrots, representing 4024 nesting attempts in 21 species and 14 countries. We also examined how poaching rates vary with geographic region, presence of active protection programs, conservation status and economic value of a species, and passage of the U.S. Wild Bird Conservation Act. The average poaching rate across all studies was 30% of all nests observed. Thirteen studies reported poaching rates of ≥20%, and four reported rates openface> 70%. Only six studies documented no nest poaching. Of these, four were conducted on islands in the Caribbean region, which had significantly lower poaching rates than the mainland Neotropics. The other two studies that showed no poaching were conducted on the two species with the lowest economic value in our sample ( U.S. retail price). In four studies that allowed direct comparison between poaching at sites with active nest protection versus that at unprotected sites, poaching rates were significantly lower at protected sites, suggesting that active protection efforts can be effective in reducing nest poaching. In those studies conducted both before and after the passage of the U.S. Wild Bird Conservation Act, poaching rates were found to be significantly lower following its enactment than in the period before. This result supports the hypothesis that the legal and illegal parrot trades are positively related, rather than inversely related as has been suggested by avicultural interests. Overall, our study indicates that poaching of parrot nestlings for economic gain is a widespread and biologically significant source of nest mortality in Neotropical parrots.     

Nonadditive effects among threats on rare plant species

The current loss of biodiversity has put 50,000 plant species at an elevated risk of extinction worldwide. Conserving at-risk species is often complicated by covariance or nonadditivity among threats, which makes it difficult to determine optimal management strategies. We sought to demographically quantify covariance and nonadditive effects of more threats on more rare plant species than ever attempted in a single analysis. We used 1082 population reports from 186 populations across 3 U.S. states of 27 rare, herbaceous plant species collected over 15 years by citizen scientists. We used a linear mixed-effects model with 4 threats and their interactions as fixed predictors, species as a random predictor, and annual growth rates as the response. We found a significant 3-way interaction on annual growth rates; rare plant population sizes were reduced by 46% during the time immediately after disturbance when populations were also browsed by deer (Odocoileus virginianus) and had high levels of encroachment by woody species. This nonadditive effect should be considered a major threat to the persistence of rare plant species. Our results highlight the need for comprehensive, multithreat assessments to determine optimal conservation actions.     

Quantifying Rarity, Losses, and Risks for Native Fishes of the Lower Colorado River Basin: Implications for Conservation Listing

Abstract:  We examined spatial distributions of fishes native to the lower basin of the Colorado River (25 species) at three scales to determine percent decline from historical distributions based on a regional biodiversity database. We cumulated records from 1843 to 1980 to develop a "historical distribution" for each species and used those occurrences recorded from 1981 to 1998 as "modern" records. We then contrasted historical and modern distributions to (1) quantify losses in spatial distribution; (2) determine how strongly these losses and fragmentation patterns corresponded to the perceived risk of extinction of each species, as represented by its status under the IUCN Red List of Endangered Species; and (3) update extinction risk rankings for 15 fishes endemic to the lower Colorado Basin according to the IUCN criteria. Based on presence and absence data, fish fauna of the lower Colorado Basin have suffered massive distributional losses. On average, ranges of extant species have diminished more than 45% relative to their historical distribution, and 35% of species have lost 50% or more of their occurrences. We provide nine new IUCN rankings and six updates to reflect more accurately the heightened imperilment of these species. Based on our new rankings, 7 of the 15 lower Colorado Basin endemics are critically endangered, 1 is endangered, 2 are vulnerable, and 1 is already extinct. We categorize the remaining 2 endemics as lower risk. This work demonstrates the utility of matching quantitative spatial metrics such as the scale-area slope statistic to extinction risk criteria for species whose persistence is strongly influenced by spatial distribution.     

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.     

Predicting the Risk of Extinction through Hybridization

Abstract: Natural hybridization threatens a substantial number of plant and animal species with extinction, but extinction risk has been difficult to evaluate in the absence of a quantitative assessment of risk factors. We investigated a number of ecological parameters likely to affect extinction risk, through an individual-based model simulating the life cycle of two hybridizing annual plant species. All parameters tested, ranging from population size to variance in pollen-tube growth rates, affected extinction risk. The sensitivity of each parameter varied dramatically across parameter sets, but, overall, the competitive ability, initial frequency, and selfing rate of the native taxon had the strongest effect on extinction. In addition, prezygotic reproductive barriers had a stronger influence on extinction rates than did postzygotic barriers. A stable hybrid zone was possible only when habitat differentiation was included in the model. When there was no habitat differentiation, either one of the parental species or the hybrids eventually displaced the other two taxa. The simulations demonstrated that hybridization is perhaps the most rapidly acting genetic threat to endangered species, with extinction often taking place in less than five generations. The simulation model was also applied to naturally hybridizing species pairs for which considerable genetic and ecological information is available. The predictions from these "worked examples" are in close agreement with observed outcomes and further suggest that an endemic cordgrass species is threatened by hybridization. These simulations provide guidance concerning the kinds of data required to evaluate extinction risk and possible conservation strategies.     

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.     

Modeling biodiversity dynamics in countryside landscapes

The future of biodiversity hinges to a great extent on the conservation value of countryside, the growing fraction of Earth's surface heavily influenced by human activities. How many species, and which species, can persist in such landscapes (and analogous seascapes) are open questions. Here we explore two complementary theoretical frameworks to address these questions: species-area relationships and demographic models. We use the terrestrial mammal fauna of Central America to illustrate the application of both frameworks. We begin by proposing a multi-habitat species-area relationship, the countryside species-area relationship, to forecast species extinction rates. To apply it, we classify the mammal fauna by affinity to native and human-dominated habitats. We show how considering the conservation value of countryside habitats changes estimates derived from the classic species-area approach We also examine how the z value of the species-area relationship affects extinction estimates. Next, we present a framework for assessing the relative vulnerability of species to extinction in the countryside, based on the Skellam model of population dynamics. This model predicts the minimum area of contiguous native habitat required for persistence of a species, which we use as an indicator of vulnerability to habitat change. To apply the model, we use our habitat affinity classification of mammals and we estimate life-history parameters by species and habitat type. The resulting ranking of vulnerabilities is significantly correlated with the World Conservation Union (IUCN) Red List assessment.     

A Study of Plant Species Extinction in Singapore: Lessons for the Conservation of Tropical Biodiversity

The native vascular plant flora of the Republic of Singapore has suffered the extinction of 594 out of a total 2277 species. These represent local, not global, species extinctions. Coastal habitats, including mangroves, have lost 39% of their species, while inland forests have last 29%. Epiphytic species (62% loss) appear particularly prone to extinction, which is reflected in a similar disposition exhibited by the Orchidaceae. Deforestation and disturbance have been the main cause of plant species extinction in Singapore. The rich mangrove epiphyte flora has been totally exterminated, and a number of tree species are reduced to populations of a few mature individuals. Many more species continue to survive than the species-area relationship would predict given the 99.8% loss of primary forest. This is interpreted as a result of the failure of equilibrium to be achieved yet in the remnant forest fragments, even after more than a century of isolation. Singapore's secondary forests appear to accrete plant diversity very slowly, even if contiguous with primary forest areas. We conclude that remnant fragments of primary tropical forest, even of very small size, can play a major role in the conservation of tropical biodiversity. The patterns of extinction observed in Singapore indicate that coastal and estuarine sites are in greatest demand for development and therefore must be given high priority for conservation despite their somewhat lower biodiversity. Epiphyte and orchid diversity appear to be very good indicators of the degree of disturbance suffered by a habitat in the humid tropics.     

Is plant community richness regulated over time? Contrasting results from experiments and long-term observations

There is considerable debate among ecologists as to whether or not communities are saturated. In saturated communities, species richness should remain relatively constant over time, despite compositional turnover, because richness is negatively correlated with colonization and positively correlated with local extinction. Few studies have tested for saturation using temporal observational data as well as diversity-perturbation experiments. We analyzed 10 years of data for plant species richness at 71 sites on contrasting serpentine and non-serpentine soils within Californian (USA) grasslands. We also manipulated local richness and measured its effects on immigration and extinction. Consistent with saturation, we observed that richness was positively correlated with extinction rates and negatively correlated with colonization rates, and randomization tests confirmed that diversity fluctuated less than expected by chance. However, experimental species additions and removals did not affect extinction or colonization, suggesting that richness is not regulated by local species interactions. Instead, we propose three reasons why richness may fluctuate within narrow limits causing the appearance of saturation in temporal observational data sets: negatively autocorrelated patterns of biotic response to yearly conditions, differential affinities of particular species for local conditions, or stochastic abundance-dependent colonization and extinction rates. We illustrate the latter using a metacommunity model.     

The Silent Mass Extinction of Insect Herbivores in Biodiversity Hotspots

Abstract: Habitat loss is silently leading numerous insects to extinction. Conservation efforts, however, have not been designed specifically to protect these organisms, despite their ecological and evolutionary significance. On the basis of species–host area equations, parameterized with data from the literature and interviews with botanical experts, I estimated the number of specialized plant‐feeding insects (i.e., monophages) that live in 34 biodiversity hotspots and the number committed to extinction because of habitat loss. I estimated that 795,971–1,602,423 monophagous insect species live in biodiversity hotspots on 150,371 endemic plant species, which is 5.3–10.6 monophages per plant species. I calculated that 213,830–547,500 monophagous species are committed to extinction in biodiversity hotspots because of reduction of the geographic range size of their endemic hosts. I provided rankings of biodiversity hotspots on the basis of estimated richness of monophagous insects and on estimated number of extinctions of monophagous species. Extinction rates were predicted to be higher in biodiversity hotspots located along strong environmental gradients and on archipelagos, where high spatial turnover of monophagous species along the geographic distribution of their endemic plants is likely. The results strongly support the overall strategy of selecting priority conservation areas worldwide primarily on the basis of richness of endemic plants. To face the global decline of insect herbivores, one must expand the coverage of the network of protected areas and improve the richness of native plants on private lands.     

Ecological Correlates of Extinction Proneness in Tropical Butterflies

Abstract:  Widespread and rapid losses of natural habitats and biodiversity have made the identification of extinction-prone species a major challenge in conservation biology. We assessed the relative importance of biologically relevant species traits (e.g., body size, ecological specialization) obtained from published records to determine the extinction probability of butterflies in a highly disturbed tropical landscape (i.e., Singapore). We also developed a taxon-specific model to estimate the extinction proneness of butterflies in Southeast Asia. Logistic regression analyses showed that adult habitat specialization, larval host plant specificity, geographical distribution, sexual dichromatism, and congenor density were significant and independent determinants of butterfly extinctions in Singapore. Among these traits, specificity of larval host plant and adult habitat specialization were the best correlates of extinction risks. We used this phenomenological extinction-regression model to estimate the relative extinction proneness of 416 butterfly species in Southeast Asia. Our results illustrate the utility of available taxon-specific data for a localized area in estimating the extinction proneness of closely related species on a regional scale. When intensive field studies are not forthcoming, especially in regions suffering from rapid biodiversity losses (e.g., Southeast Asia), similar approaches could be used to estimate extinction threats for other taxonomic groups.     

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.     

Transient dynamics of invasive competition: barred owls, spotted owls, habitat, and the demons of competition present

The recent range expansion of Barred Owls (Strix varia) into the Pacific Northwest, where the species now co-occurs with the endemic Northern Spotted Owl (Strix occidentalis caurina), resulted in a unique opportunity to investigate potential competition between two congeneric, previously allopatric species. The primary criticism of early competition research was the use of current species' distribution patterns to infer past processes; however, the recent expansion of the Barred Owl and the ability to model the processes that result in site occupancy (i.e., colonization and extinction) allowed us to address the competitive process directly rather than inferring past processes through current patterns. The purpose of our study was to determine whether Barred Owls had any negative effects on occupancy dynamics of nesting territories by Northern Spotted Owls and how these effects were influenced by habitat characteristics of Spotted Owl territories. We used single-species, multi-season occupancy models and covariates quantifying Barred Owl detections and habitat characteristics to model extinction and colonization rates of Spotted Owl pairs in southern Oregon, USA. We observed a strong, negative association between Barred Owl detections and colonization rates and a strong positive effect of Barred Owl detections on extinction rates of Spotted Owls. We observed increased extinction rates in response to decreased amounts of old forest at the territory core and higher colonization rates when old-forest habitat was less fragmented. Annual site occupancy for pairs reflected the strong effects of Barred Owls on occupancy dynamics with much lower occupancy rates predicted for territories where Barred Owls were detected. The strong Barred Owl and habitat effects on occupancy dynamics of Spotted Owls provided evidence of interference competition between the species. These effects increase the importance of conserving large amounts of contiguous, old-forest habitat to maintain Northern Spotted Owls in the landscape.     

Habitat Loss and Changes in the Species-Area Relationship

Abstract: The species-area relationship (SAR) has been used successfully to predict extinction from extent of habitat reduction. These extinction estimates assume that species have uniformly distributed range requirements and a minimum abundance level required for persistence; how many species are lost depends solely on how much habitat is removed, not on where it is removed. We consider another limiting case in which range requirements, rather than abundances, determine extinctions. We used a new method for constructing SARs based on assumptions about geographic ranges of species. Our results show that habitat destruction can change the SAR and consequently the number of species predicted to be lost due to habitat destruction. Our method generates SARs that vary in shape according to the specific distributions of geographic range and occupancy but that have the common feature of being described by a power law with an exponent of <1. When the geographic range of species was included in the SAR, the way habitat was lost became important. Although the SAR before habitat destruction is often used to predict species loss after habitat destruction, assumptions must be clearly stated. To predict the damage caused by habitat loss with our model, it is necessary to know the fraction of aggregated species, the distribution of geographic ranges, the form of habitat destruction, and the sampling protocol. The remaining theoretical challenge is to develop a full theory that links abundance and range.     

Value of Small Patches in the Conservation of Plant-Species Diversity in Highly Fragmented Rainforest

Abstract:  We evaluated the importance of small (<5 ha) forest patches for the conservation of regional plant diversity in the tropical rainforest of Los Tuxtlas, Mexico. We analyzed the density of plant species (number of species per 0.1 ha) in 45 forest patches of different sizes (1–700 ha) in 3 landscapes with different deforestation levels (4, 11, and 24% forest cover). Most of the 364 species sampled (360 species, 99%) were native to the region, and only 4 (1%) were human-introduced species. Species density in the smallest patches was high and variable; the highest (84 species) and lowest (23 species) number of species were recorded in patches of up to 1.8 ha. Despite the small size of these patches, they contained diverse communities of native plants, including endangered and economically important species. The relationship between species density and area was significantly different among the landscapes, with a significant positive slope only in the landscape with the highest deforestation level. This indicates that species density in a patch of a given size may vary among landscapes that have different deforestation levels. Therefore, the conservation value of a patch depends on the total forest cover remaining in the landscape. Our findings revealed, however, that a great portion of regional plant diversity was located in very small forest patches (<5 ha), most of the species were restricted to only a few patches (41% of the species sampled were distributed in only 1–2 patches, and almost 70% were distributed in 5 patches) and each landscape conserved a unique plant assemblage. The conservation and restoration of small patches is therefore necessary to effectively preserve the plant diversity of this strongly deforested and unique Neotropical region.