Variability in Population Abundance and the Classification of Extinction Risk

Abstract: Classifying species according to their risk of extinction is a common practice and underpins much conservation activity. The reliability of such classifications rests on the accuracy of threat categorizations, but very little is known about the magnitude and types of errors that might be expected. The process of risk classification involves combining information from many sources, and understanding the quality of each source is critical to evaluating the overall status of the species. One common criterion used to classify extinction risk is a decline in abundance. Because abundance is a direct measure of conservation status, counts of individuals are generally the preferred method of evaluating whether populations are declining. Using the thresholds from criterion A of the International Union for Conservation of Nature (IUCN) Red List (critically endangered, decline in abundance of >80% over 10 years or 3 generations; endangered, decline in abundance of 50–80%; vulnerable, decline in abundance of 30–50%; least concern or near threatened, decline in abundance of 0–30%), we assessed 3 methods used to detect declines solely from estimates of abundance: use of just 2 estimates of abundance; use of linear regression on a time series of abundance; and use of state‐space models on a time series of abundance. We generated simulation data from empirical estimates of the typical variability in abundance and assessed the 3 methods for classification errors. The estimates of the proportion of falsely detected declines for linear regression and the state‐space models were low (maximum 3–14%), but 33–75% of small declines (30–50% over 15 years) were not detected. Ignoring uncertainty in estimates of abundance (with just 2 estimates of abundance) allowed more power to detect small declines (95%), but there was a high percentage (50%) of false detections. For all 3 methods, the proportion of declines estimated to be >80% was higher than the true proportion. Use of abundance data to detect species at risk of extinction may either fail to detect initial declines in abundance or have a high error rate.     

Will Observation Error and Biases Ruin the Use of Simple Extinction Models?

Abstract: Estimating the risk of extinction for populations of endangered species is an important component of conservation biology. These estimates must be made from data that contain both environmental noise in the year-to-year transitions in population size (so-called "process error"), random errors in sampling, and possible biases in sampling ( both forms of observation errors). To determine how much faith to place in estimated extinction rates, it is important to know how sensitive they are to observation error. We used three simple, commonly employed models of population dynamics to generate simulated population time series. We then combined random observation error or systematic biases with those data, fit models to the time series data, and observed how close the extinction dynamics of the fitted models compared with the dynamics of the underlying models. We found that systematic biases in sampling rarely affected estimates of extinction risk. We also found that even moderate levels of random observation error do not significantly affect extinction estimates except over a small range of process errors, corresponding to the region where extinction risk is most uncertain. With more substantial sampling error, estimates of extinction risk degraded rapidly. Field census techniques for a variety of taxa often involve observation errors within ±32% of actual population sizes. For typical time series used in conservation, therefore, we often may not need to be overly concerned about observation errors as an extra source of imperfection in our estimated extinction rates.     

Fitting probability models to population dynamics data

Methods for modeling population dynamics in probability using the generalized point process approach are developed. The life history of these populations is such that seasonal reproduction occurs during a short time. Several models are developed and analyzed. Data about two species: colonial spiders (Stegodyphus dumicola) and a migratory bird (wood thrush, Hylocichla mustelina) are used to estimate model parameters with appropriate log maximum likelihood functions. For the spiders, the model is fitted to provide evolutionary feasible colony size based on maximum likelihood estimates of fecundity and survival data. For the migratory bird species, a maximum likelihood estimates are derived for the fecundity and survival rates of young and adult birds and immigration rate. The presented approach allows computation of quantities of interest such as probability of extinction and average time to extinction.     

A population viability analysis for the Island Fox on Santa Catalina Island,California

The island fox (Urocyon littoralis) on Santa Catalina Island is among the most imperiled species on the Channel Islands due to a recent outbreak of canine distemper virus (CDV). The western subpopulation, which was not exposed to CDV, is a crucial element in the recovery of foxes by providing a source of animals for translocation and captive breeding. Using the program VORTEX, we developed a population viability analysis for the Santa Catalina Island fox to (1) address the likelihood of population persistence, (2) estimate the current susceptibility of the population to catastrophic events, and (3) evaluate the efficacy of current restoration strategies of releasing captive bred foxes and transplanting wild animals. Overall, we found the population to be susceptible to catastrophic events; a 50% increase in mortality every 20 years was sufficient to elevate the extinction risk above 5%. Current management activities entail the transplanting of 12 juvenile foxes annually, which may reduce the viability of the western subpopulation. A minimum population size of at least 150 foxes should be maintained in each subpopulation to reduce the risk of extinction due to demographic stochasticity. Releases of translocated and captive bred animals affect the speed of recovery on the eastern half of Catalina Island, but not the probability of extinction, which is near zero under current conditions. We conducted a sensitivity analysis for demographic parameters by incrementally varying survival, fecundity and density-dependence parameters, while holding all other parameters constant. Sensitivity analyses identified mortality and mean litter size as the most sensitive parameters, while the implementation of density-dependence and environmental variation of model parameters did not seem to affect population performance. We conclude that the population of island foxes on Santa Catalina is currently at a critically low population level, but recovery of the species appears possible.     

Demography of Two Mexican Spotted Owl Populations

Abstract: The Mexican Spotted Owl ( Strix occidentalis lucida ) is a threatened subspecies of the southwestern United States and northern Mexico. Although threatened, little is known about its population status. We studied the demography of the Mexican Spotted Owl in one study area in Arizona and one in New Mexico from 1991 to 1997. We estimated annual survival rates (φ), fecundity rates (   b ), and abundance (   N ) to test the hypothesis that population trends were stationary. Although annual fecundity rates (   b ^ = 0.494 for Arizona and 0.380 for New Mexico) and annual juvenile survival rates ( φ^ = 0.179 for Arizona and 0.109 for New Mexico) differed in magnitude between the study areas, they exhibited similar temporal patterns. Annual survival for territorial owls varied randomly in Arizona but declined linearly in New Mexico. Mean annual survival for territorial owls was 0.814 in Arizona and 0.832 for owls ≥3 years old and 0.644 for owls 1–2 years old in New Mexico. Based on survival and fecundity estimates, the annual rates of change (λ^) indicated that both populations were declining at ≥10% a year. These estimates were corroborated by observed declines in abundance. Some regional factor may have been affecting fecundity, whereas a combination of factors may have been affecting survival. Two possible reasons for the population declines are declines in habitat quality and regional trends in climate.     

Extinction Rate Estimates for Plant Populations in Revisitation Studies: Importance of Detectability

Abstract:  Many researchers have obtained extinction-rate estimates for plant populations by comparing historical and current records of occurrence. A population that is no longer found is assumed to have gone extinct. Extinction can then be related to characteristics of these populations, such as habitat type, size, or species, to test ideas about what factors may affect extinction. Such studies neglect the fact that a population may be overlooked, however, which may bias estimates of extinction rates upward. In addition, if populations are unequally detectable across groups to be compared, such as habitat type or population size, comparisons become distorted to an unknown degree. To illustrate the problem, I simulated two data sets, assuming a constant extinction rate, in which populations occurred in different habitats or habitats of different size and these factors affected their detectability. The conventional analysis implicitly assumed that detectability equalled 1 and used logistic regression to estimate extinction rates. It wrongly identified habitat and population size as factors affecting extinction risk. In contrast, with capture-recapture methods, unbiased estimates of extinction rates were recovered. I argue that capture-recapture methods should be considered more often in estimations of demographic parameters in plant populations and communities.     

Stereological methods applied to reproductive cycle of Tapes rhomboides

A population of Tapes rhomboides (Pennant) in the Bay of St. Malo, France, was studied for one and a half years (July 1984–October 1985) to determine spawning frequency and fecundity under natural conditions, using the techniques of qualitative histological staging, condition index calculation and quantitative stereology. Spawning took place twice a year, in late May and in July/September. There was an extended winter resting period. Gonad development and oocyte production were positively correlated with female body size. The annual fecundity in a 40 mm clam was about 5x10⁵. Stereological techniques provided accurate information on oocyte dynamics within a gonad and the relationship with atretic processes. Each oocyte generation from the onset of the cycle to the winter resting stage was spawned eventually if conditions were suitable, or the oocytes were resorbed. Atresia of oocytes was seen throughout the reproductive period, but especially after the spring spawning and at the end of the summer.     

Climate Change, Elevational Range Shifts, and Bird Extinctions

Abstract:  Limitations imposed on species ranges by the climatic, ecological, and physiological effects of elevation are important determinants of extinction risk. We modeled the effects of elevational limits on the extinction risk of landbirds, 87% of all bird species. Elevational limitation of range size explained 97% of the variation in the probability of being in a World Conservation Union category of extinction risk. Our model that combined elevational ranges, four Millennium Assessment habitat-loss scenarios, and an intermediate estimate of surface warming of 2.8° C, projected a best guess of 400–550 landbird extinctions, and that approximately 2150 additional species would be at risk of extinction by 2100. For Western Hemisphere landbirds, intermediate extinction estimates based on climate-induced changes in actual distributions ranged from 1.3% (1.1° C warming) to 30.0% (6.4° C warming) of these species. Worldwide, every degree of warming projected a nonlinear increase in bird extinctions of about 100–500 species. Only 21% of the species predicted to become extinct in our scenarios are currently considered threatened with extinction. Different habitat-loss and surface-warming scenarios predicted substantially different futures for landbird species. To improve the precision of climate-induced extinction estimates, there is an urgent need for high-resolution measurements of shifts in the elevational ranges of species. Given the accelerating influence of climate change on species distributions and conservation, using elevational limits in a tested, standardized, and robust manner can improve conservation assessments of terrestrial species and will help identify species that are most vulnerable to global climate change. Our climate-induced extinction estimates are broadly similar to those of bird species at risk from other factors, but these estimates largely involve different sets of species.     

Brooding of the sub-Antarctic heart urchin, <Emphasis Type="Italic">Abatus cavernosus</Emphasis> (Spatangoida: Schizasteridae), in southern Patagonia

The reproductive cycle of the sub-Antarctic spatangoid sea urchin, Abatus cavernosus, was examined during a 2-year period in southern Patagonia, Argentina. The population studied is the northernmost known coastal population in the austral oceans, and is influenced by a greater annual range of seawater temperature than other Abatus species. The sex ratio of the overall A. cavernosus population did not differ significantly from 1:1, but was not homogeneous across size classes. A clearly defined annual reproductive cycle was found. Spawning occurred from May to July and was synchronous between sexes. Females were observed to be brooding within a 9-month period, from May to February. Juveniles were released during the austral summer, from January to February. The length at which 50% of the females were brooding occurred at a test length of 25.9 mm. A. cavernosus had a large egg size (mean diameter = 1.4 mm) and low fecundity (maximum = 57 eggs per female) compared to closely related species. The number of eggs within each brood pouch was highest in larger anterior brood pouch, which is close to two gonopores, as opposed to the other anterior and two smaller posterior pouches. Significant interannual variation was observed in gonad cycles, fecundity, and embryo development such as: brood size decreased during 2001; adjusted gonad dry weight and fecundity were higher during 2003. Hypotheses concerning the gonadal and brooding cycles and fecundity of sub-Antarctic and Antarctic Schizasteridae are discussed. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Hidden demographic impacts of fishing and environmental drivers of fecundity in a sea turtle population

Fisheries bycatch is a critical threat to sea turtle populations worldwide, particularly because turtles are vulnerable to multiple gear types. The Canary Current is an intensely fished region, yet there has been no demographic assessment integrating bycatch and population management information of the globally significant Cabo Verde loggerhead turtle (Caretta caretta) population. Using Boa Vista island (Eastern Cabo Verde) subpopulation data from capture–recapture and nest monitoring (2013–2019), we evaluated population viability and estimated regional bycatch rates (2016–2020) in longline, trawl, purse-seine, and artisanal fisheries. We further evaluated current nesting trends in the context of bycatch estimates, existing hatchery conservation measures, and environmental (net primary productivity) variability in turtle foraging grounds. We projected that current bycatch mortality rates would lead to the near extinction of the Boa Vista subpopulation. Bycatch reduction in longline fisheries and all fisheries combined would increase finite population growth rate by 1.76% and 1.95%, respectively. Hatchery conservation increased hatchling production and reduced extinction risk, but alone it could not achieve population growth. Short-term increases in nest counts (2013–2021), putatively driven by temporary increases in net primary productivity, may be masking ongoing long-term population declines. When fecundity was linked to net primary productivity, our hindcast models simultaneously predicted these opposing long-term and short-term trends. Consequently, our results showed conservation management must diversify from land-based management. The masking effect we found has broad-reaching implications for monitoring sea turtle populations worldwide, demonstrating the importance of directly estimating adult survival and that nest counts might inadequately reflect underlying population trends.     

Rapid Extinction of Mountain Sheep Populations Revisited

Abstract: Predicting extinction probabilities for populations of various sizes has been a primary focus of conservation biology. Berger (1990) presented an empirically based extinction model for mountain sheep ( Ovis canadensis ) populations in five southwestern states that predicted disappearance within 50 years of all populations estimated to number 50 sheep or fewer, but essentially no loss in that time period of populations estimated at over 100. The majority of the 122 populations he used in his analysis were from California, but his analysis did not use many of the historical size estimates for these populations. I tested Berger's (1990) model using the complete data set from California and found—contrary to his results—that, for all size classes of population estimates, at least 61% of the populations persisted for 50 years. Also, two predictions from Berger's model were not consistent with the data from California: (1) 10 populations have increased from estimates of 50 or fewer animals to over 100, whereas the Berger model predicted that these populations would only decline to extinction; and (2) of 27 extant populations with long enough records, 85% were estimated at least 50 years ago to be 50 individuals or fewer and should therefore be extinct by now. Berger's model has now failed tests in three states and therefore does not support the strong population size effect on extinction probability that it first appeared to provide, and it may serve conservation poorly through misdirected effort if it is used as the basis for setting policies or taking actions.     

Conserving the abundance of nonthreatened species

Human modification of the environment is driving declines in population size and distributional extent of much of the world's biota. These declines extend to many of the most abundant and widespread species, for which proportionally small declines can result in the loss of vast numbers of individuals, biomass, and interactions. These losses could have major localized effects on ecological and cultural processes and services without elevating a species’ global extinction risk. Although most conservation effort is directed at species threatened with extinction in the very near term, the value of retaining abundance regardless of global extinction risk is justifiable based on many biodiversity or ecosystem service metrics, including cultural services, at scales from local to global. The challenges of identifying conservation priorities for widespread and abundant species include quantifying the effects of species’ abundance on services and understanding how these effects are realized as populations decline. Negative effects of population declines may be disconnected from the threat processes driving declines because of species movements and environment flows (e.g., hydrology). Conservation prioritization for these species shares greater similarity with invasive species risk assessments than extinction risk assessments because of the importance of local context and per capita effects of abundance on other species. Because conservation priorities usually focus on preventing the extinction of threatened species, the rationale and objectives for incorporating declines of nonthreatened species must be clearly articulated, going beyond extinction risk to encompass the range of likely harmful effects (e.g., secondary extinctions, loss of ecosystem services) if declines persist or are not reversed. Research should focus on characterizing the effects of local declines in species that are not threatened globally across a range of ecosystem services and quantifying the spatial distribution of these effects through the distribution of abundance. The case for conserving abundance in nonthreatened species can be made most powerfully when the costs of losing this abundance are better understood.     

Demographic Viability of a Relict Population of the Critically Endangered Plant Borderea chouardii

Abstract:   In addition to human-caused changes in the environment, natural stochasticity may threaten species persistence, and its impact must be taken into account when priorities are established and management plans are designed. Borderea chouardii is a Tertiary relict at risk of extinction that occurs in only one location in the world, where the probability of human disturbance is low. Its persistence, therefore, is mainly linked to its response to natural threats such as stochasticity. Over 8 years I monitored up to 25% of this rupicolous small geophyte. The population had an unbalanced size structure and 90% failure in seed arrival at appropriate microhabitats, which suggests a problem with recruitment. I used matrix models to describe its population dynamics, conducted hand sowings, and performed stochastic simulations to investigate the effect of environmental stochasticity on population trend and viability. I modeled several scenarios to represent a variety of ecological situations, such as population reduction, episodic or persistent disease, and enhancement or decrease of recruitment. Population growth rate (λ) was never significantly different from unity over the study period. The risk of extinction was null over the next five centuries under current conditions. Increase of mortality and decrease of recruitment reduced stochastic population growth rate, but no factor except a persistent increase of 10% mortality resulted in extinction. These results are the consequence of the plant's extremely long life span (over 300 years) and low temporal variability of key vital rates. Even though hand sowing significantly increased the stochastic population growth rate, other approaches may be more important for the persistence of this species. The extremely slow capacity for recovery following disturbances renders habitat preservation essential. In addition, the founding of new populations would reduce the risk associated with habitat destruction.     

Reliability of Absolute and Relative Predictions of Population Persistence Based on Time Series

Abstract:  Conventional population viability analysis (PVA) is often impractical because data are scarce for many threatened species. For this reason, simple count-based models are being advocated. The simplest of these models requires nothing more than a time series of abundance estimates, from which variance and autocorrelation in growth rate are estimated and predictions of population persistence are generated. What remains unclear, however, is how many years of data are needed to generate reliable estimates of these parameters and hence reliable predictions of persistence. By analyzing published and simulated time series, we show that several decades of data are needed. Predictions based on short time series were very unreliable mainly because limited data yielded biased, unreliable estimates of variance in growth rate, especially when growth rate was strongly autocorrelated. More optimistically, our results suggest that count-based PVA is sometimes useful for relative risk assessment (i.e., for ranking populations by extinction risk), even when time series are only a decade long. However, some conditions consistently lead to backward rankings. We explored the limited conditions under which simple count-based PVA may be useful for relative risk assessment.     

On the choice of statistical models for estimating occurrence and extinction from animal surveys

In surveys of natural animal populations the number of animals that are present and available to be detected at a sample location is often low, resulting in few or no detections. Low detection frequencies are especially common in surveys of imperiled species; however, the choice of sampling method and protocol also may influence the size of the population that is vulnerable to detection. In these circumstances, probabilities of animal occurrence and extinction will generally be estimated more accurately if the models used in data analysis account for differences in abundance among sample locations and for the dependence between site-specific abundance and detection. Simulation experiments are used to illustrate conditions wherein these types of models can be expected to outperform alternative estimators of population site occupancy and extinction.     

Genetic and demographic consequences of importing animals into a small population: a simulation model of the Texas State Bison Herd (USA)

The extant 40 bison (Bison bison) constituting the Texas State Bison Herd (TSBH; USA) are directly and exclusively descended from a bison herd assembled by Charles Goodnight in the 1880s, representing a historically and genetically valuable resource. The population currently suffers from low genetic variation, low heterozygosity, high calf mortality, and low natality rates compared with other closed bison populations. Population viability analysis using the VORTEX program previously indicated a 99% chance of population extinction within the next 41 years [J. Mamm. 85 (2004) in press]. We developed a stochastic simulation model to evaluate the genetic and demographic consequences of various management scenarios for the TSBH using genotypic data from 51 microsatellite loci and demographic information recorded over a 6-year period. Our results reveal that without the introduction of new genetic variation, approximately 37% of the representative microsatellite loci will become fixed as the TSBH continues to lose genetic variation at a staggering rate of 30–40% within the next 50 years. Furthermore, if the current trends in natality and mortality rates continue, our model indicates the TSBH faces a 99% chance of extinction in the next 51 years. With the importation of unrelated male bison into the TSBH, and under the assumption of increased fitness, the probability of population survival in the next 100 years increases to 100%, and the population will reach the approximate carrying capacity of 200 bison in 15–16 years. Furthermore, our model predicts increases in genetic diversity and heterozygosity of 24.7–48.4% and 17.5–36.5%, respectively, in the next 100 years following the addition of new genetic variation. We conclude that the importation of bison into the TSBH is necessary to prevent extinction and ensure long-term population survival.     

Incidence,occurrence and distribution of the nematode Echinomermella matsi in its echinoid host,Strongylocentrotus droebachiensis,in northern Norway

The incidence, occurrence and distribution of the nematode Echinomermella matsi (Jones and Hagen) in its host, the echinoid Strongylocentrotus droebachiensis Müller, were examined in Norwegian waters from Nordmre (63° N) to the Russian border (70° N) in a range of habitats (e.g. kelp cover and community type) from 1982 to 1992. The results are used to examine the likely influence of the parasite on fitness (individual growth and gonad production) and its potential in regulating the population size of its echinoid host. The nematode infections are restricted to areas between Vikna (Vega) and middle Troms, with the highest prevalence (40 to 88% infected) in the Bodø area, the focus of the distribution. The prevalence rates are similar on kelp beds and barren grounds. No difference in growth rates between infected and noninfected sea urchins was found. Nematode-infected sea urchins in kelp bed populations had gonads weighing about one-sixth of those of equivalent uninfected individuals. This indicates that nematodes are really parasites causing reduced reproductive capacity. Areas with high prevalence (>40% infected) of nematodes had low sea urchin densities. High nematode intensities were found in the areas with high prevalence. The mean abundance in high prevalence areas was highest (eight nematodes) in the 4-to 7-yr-old age group and decreased to zero among the oldest age groups. The ratio of variance/mean abundance was also highest among 5-to 8-yr-old sea urchins. At highly and slightly infected locations, the relationships between the log of the variance and the log of the mean abundance of parasites were 1.35 and 1.69, respectively. Measurements of the frequency distribution of nematodes in sea urchins and the corresponding estimates of the negative binomial distribution showed significantly higher counts in estimated than observed subpopulations exceeding 20 nematodes per sea urchin. These results may explain nematode-induced sea urchin mortality. The low density of the host in the Bodø area, which had high prevalence, may be a result of increased host mortality caused by nematodes, by lower recruitment because of reduced gonad production, or by other factors. Low prevalence among older sea urchins may be caused by nematodeinduced host mortality or by cycles in infection. However, studies on the life cycle of the nematode and long term investigations of host density and nematode intensity/prevalence will be needed before any true conclusions can can be drawn.     

The Role of Translocation in Recovery of Woodland Caribou Populations

Abstract: Maintenance of viable populations of many endangered species will require conservation action in perpetuity. Efforts to conserve these species are more likely to be successful if their reliance on conservation actions is assessed at the population level. Woodland caribou (Rangifer tarandus caribou) were extirpated recently from Banff National Park, Canada, and translocations of caribou to Banff and neighboring Jasper National Park are being considered. We used population viability analysis to assess the relative need for and benefits from translocation of individuals among caribou populations. We measured stochastic growth rates and the probability of quasi extinction of four populations of woodland caribou with and without translocation. We used two vital rates in our analysis: mean adult female survival and mean number of calves per breeding‐age female as estimates of mean fecundity. We isolated process variance for each vital rate. Our results suggested the Tonquin caribou population in Jasper is likely to remain viable without translocation, but that translocation is probably insufficient to prevent eventual extirpation of the two other populations in Jasper. Simulated reintroductions of caribou into Banff resulted in a 53–98% probability of >8 females remaining after 20 years, which suggests translocation may be an effective recovery tool for some caribou populations.     

Generation lengths of the world's birds and their implications for extinction risk

Birds have been comprehensively assessed on the International Union for Conservation of Nature (IUCN) Red List more times than any other taxonomic group. However, to date, generation lengths have not been systematically estimated to scale population trends when undertaking assessments, as required by the criteria of the IUCN Red List. We compiled information from major databases of published life-history and trait data for all birds and imputed missing life-history data as a function of species traits with generalized linear mixed models. Generation lengths were derived for all species, based on our modeled values of age at first breeding, maximum longevity, and annual adult survival. The resulting generation lengths varied from 1.42 to 27.87 years (median 2.99). Most species (61%) had generation lengths <3.33 years, meaning that the period of 3 generations—over which population declines are assessed under criterion A—was <10 years, which is the value used for IUCN Red List assessments of species with short generation times. For these species, our trait-informed estimates of generation length suggested that 10 years is a robust precautionary value for threat assessment. In other cases, however, for whole families, genera, or individual species, generation length had a substantial impact on their estimated extinction risk, resulting in higher extinction risk in long-lived species than in short-lived species. Although our approach effectively addressed data gaps, generation lengths for some species may have been underestimated due to a paucity of life-history data. Overall, our results will strengthen future extinction-risk assessments and augment key databases of avian life-history and trait data.