Contributed Paper
Critically evaluating best management practices for preventing freshwater turtle extinctions R.-J. Spencer
,1 ∗ J.U. Van Dyke,1 and Michael B. Thompson2
1
School of Science and Health, Hawkesbury Institute for the Environment, Western Sydney University, Building M15, Hawkesbury Campus, Locked Bag 1797, Penrith, NSW 2751, Australia 2 School of Life and Environmental Sciences, University of Sydney, Heydon-Laurence Building (A08), Sydney, NSW 2006, Australia
Abstract: Ex situ conservation tools, such as captive breeding for reintroduction, are considered a last resort to recover threatened or endangered species, but they may also help reduce anthropogenic threats where it is difficult or impossible to address them directly. Headstarting, or captive rearing of eggs or neonate animals for subsequent release into the wild, is controversial because it treats only a symptom of a larger conservation problem; however, it may provide a mechanism to address multiple threats, particularly near population centers. We conducted a population viability analysis of Australia’s most widespread freshwater turtle, Chelodina longicollis, to determine the effect of adult roadkill (death by collision with motor vehicles), which is increasing, and reduced recruitment through nest predation from introduced European red foxes (Vulpes vulpes). We also modeled management scenarios to test the effectiveness of headstarting, fox management, and measures to reduce mortality on roads. Only scenarios with headstarting from source populations eliminated all risks of extinction and allowed population growth. Small increases in adult mortality (2%) had the greatest effect on population growth and extinction risk. Where threats simultaneously affected other life-history stages (e.g., recruitment), eliminating harvest pressures on adult females alone did not eliminate the risk of population extinction. In our models, one source population could supply enough hatchlings annually to supplement 25 other similar-sized populations such that extinction was avoided. Based on our results, we believe headstarting should be a primary tool for managing freshwater turtles for which threats affect multiple life-history stages. We advocate the creation of source populations for managing freshwater turtles that are greatly threatened at multiple life-history stages, such as depredation of eggs by invasive species and adult mortality via roadkill. Keywords: Australia, Chelodina longicollis, ex situ conservation, foxes, harvest populations, headstarting, invasive predators, road mortality Evaluaci´ on Cr´ıtica de las Mejores Pr´acticas de Manejo para Prevenir las Extinciones de las Tortugas de Agua Dulce
Resumen: Las herramientas de conservaci´on ex situ, como la crianza en cautiverio para la reintroducci´on, son consideradas como el u ´ ltimo recurso para recuperar a las especies amenazadas o en peligro, pero tambi´en pueden ayudar a reducir las amenazas antropog´enicas en donde es dif´ıcil o imposible tratarlas directamente. El inicio con ventaja, o la crianza en cautiverio de huevos o animales neonatos para su liberaci´ on subsecuente a la vida libre, es controversial porque solamente trata un s´ıntoma de un problema mayor de la conservaci´ on; sin embargo, puede proporcionar un mecanismo para lidiar con m´ ultiples amenazas, particularmente cerca de los centros poblacionales. Realizamos un an´ alisis de viabilidad poblacional con la tortuga de agua dulce con mayor distribuci´ on en Australia, Chelodiina longicollis, para determinar el efecto de los atropellamientos de adultos (muerte por colisi´ on con autom´ oviles), los cuales son cada vez m´ as frecuentes, y redujimos el reclutamiento por medio de la depredaci´ on de nidos realizada por los zorros rojos Europeos introducidos (Vulpes vulpes). Tambi´en modelamos escenarios de manejo para evaluar la efectividad del inicio con ventaja, el manejo de los zorros y las medidas para reducir la mortalidad en los caminos. S´ olo los escenarios con inicio con ventaja a partir de poblaciones fuente eliminaron todos los riesgos de extinci´ on y permitieron el crecimiento de la poblaci´ on. Los peque˜ nos incrementos en la mortalidad adulta (2%) tuvieron el mayor efecto
∗ email
[email protected] Paper submitted November 21, 2016; revised manuscript accepted March 3, 2017.
1340 Conservation Biology, Volume 31, No. 6, 1340–1349 C 2017 Society for Conservation Biology DOI: 10.1111/cobi.12930
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sobre el crecimiento poblacional y el riesgo de extinci´ on. En donde las amenazas afectaron simult´ aneamente a otras etapas de la ontogenia (p. ej.: el reclutamiento), s´ olo controlar las presiones de cosecha sobre las hembras no elimin´ o el riesgo de extinci´ on de la poblaci´ on. En nuestros modelos, una poblaci´ on fuente pudo proporcionar suficientes cr´ıas para abastecer a otras 25 poblaciones de tama˜ no similar de tal forma que se evit´ o la extinci´ on. Con base en nuestros resultados, creemos que el inicio con ventaja deber´ıa ser una herramienta primaria para el manejo de tortugas de agua dulce para las cuales las amenazas afectan a m´ ultiples etapas de la ontogenia. Proponemos la creaci´ on de poblaciones fuente para el manejo de tortugas de agua dulce que est´ an enormemente amenazadas durante varias etapas de su historia de vida, como la depredaci´ on de los huevos por especies invasoras o la mortalidad adulta por atropellamientos.
Palabras Clave: Australia, Chelodina longicollis, conservaci´on ex situ, depredadores invasores, inicio con ventaja, mortalidad en carreteras, poblaciones de cosecha, zorros
Introduction Captive breeding and headstarting for reintroduction and population augmentation is a conservation strategy used to help recover threatened or endangered species (Bowkett 2009; Conde et al. 2011). Such strategies provide a valuable management tool where reducing threats directly is difficult or ineffective. In essence, captive breeding aims to replace individuals that are killed by on-going threats, but they have been criticized for low rates of success and high costs (Wolf et al. 1996; Fischer & Lindenmayer 2000), and are unlikely to work unless integrated into a broader recovery plan (IUCN-SSC 2013). Although the benefits of headstarting are only now being evaluated critically (e.g., Canessa et al. 2016), headstarting is the basis of conservation strategies for many taxa; few more high profile than the headstarting of marine turtles. Headstarting, or captive rearing of eggs or hatchling turtles for release into the wild, is controversial (e.g., Huff 1989; Burke 1991; Frazer 1992; Seigel & Dodd Jr 2000; Bell et al. 2005) because it is a symptomatic treatment of a larger conservation problem (a “halfway technology” [Frazer 1992]); may alter behavior of head-started individuals (Woody 1991); and may disrupt population genetics (Rasberry 2015) and ecological function (Bowen et al. 1994). From a population point of view, eggs and juveniles have been considered life-history stages that have minimal impact on population growth (Heppell 1998). Thus, headstarting has been seen primarily as a strategy to promote ecotourism and attract funding for alternative conservation methods, especially for marine turtle conservation (Tisdell & Wilson 2005). The effectiveness of headstarting marine turtles as a population management strategy has not been assessed thoroughly, largely because the time between release and maturity of an individual (when a released juvenile may return to nest) is over 20 years in some species (Ernst & Barbour 1989). However, results of recent studies suggest that headstarting (in conjunction with other management strategies) may be effective. Once declining or endangered, marine turtle populations are now stable or increasing (Crowder & Heppell 2011).
Headstarting is not commonly used as a conservation strategy for freshwater turtles. High financial costs and landscape-level disconnectivity among populations have probably restricted its use, and past population modeling suggests that conservation efforts are more effective when focused on reducing adult mortality (e.g., Heppell et al. 1996; Heppell 1998). Elasticity values of adult survival are orders of magnitude greater than for any other stage (Heppell 1998), meaning that the survival of 1 adult has far greater impact on population stability than the survival of individuals from any other stage. Elasticity quantifies how many individuals of each stage would be required to maintain population stability or growth. Although increasing population growth by 1% requires the survival of far fewer adults than eggs (e.g., Heppell et al. 1996; Heppell 1998), increasing adult survival, from a management perspective, may be far more costly or complicated than harvesting eggs from nests or gravid females or protecting nests. Thus, the benefits of protecting many eggs over fewer adults may prove more cost-effective and logistically feasible. Headstarting has become an acceptable method for turtle management and conservation despite model projections. The Turtle Survival Alliance is currently headstarting at least 11 species, including freshwater turtles and land tortoises (Burke 2015). However, there is little evidence that headstarting restores freshwater turtle populations (Burke 2015). Freshwater turtles face threats that affect all life-history stages. Turtle life histories are characterized by high, fluctuating rates of egg and juvenile mortality. That mortality is balanced by extreme iteroparity (i.e., individuals are long lived and highly fecund) and the generally low threat to adult survival. In Australia, this life history has been affected by predation by invasive foxes (Vulpes vulpes) on eggs, young, (Thompson 1983), and nesting females, and by adult mortality from collisions with motor vehicles (Spencer 2002). In the Murray River, Australia, egg mortality due to foxes has increased to over 93% (Thompson 1983; Spencer 2002). As a result, turtles in the River Murray are in serious decline; abundances are 69–91% lower than 40 years ago (Chessman 2011). Apart from road deaths and predation, turtles are also struck by
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boats, drowned in fishing nets or in irrigation pumps, and killed by anglers, and human activities that affect water quality are increasing the prevalence of wildlife diseases (Kennett et al. 2009). With multiple threats affecting multiple life-history stages of freshwater turtles, the dilemma for conservation is garnering the capacity to implement diverse, broadscale management strategies to address each threat. Headstarting may allow for simultaneous management of a range of threats affecting freshwater turtles. We sought to evaluate a range of headstarting and fox control management strategies based on a case study of Australia’s most common and widespread freshwater turtle, the Eastern Long-necked Turtle (Chelodina longicollis), which is highly mobile and inhabits wetlands throughout southeastern Australia, including cities and urban areas (Cann 1998). Nest predation rates are high because invasive foxes occur throughout their range, but they are also particularly threatened by motor vehicles and habitat fragmentation associated with urban infrastructure (Hamer et al. 2016) because they frequently move between wetlands (Spencer & Thompson 2005). They occupy a wide range of wetland types and are a late-maturing species; males mature at 7–8 years and females at 10–12 years (Kennett et al. 2009). Mortality of adult turtles can drive species to extinction (Heppell 1998), and combined with reduced recruitment levels because of invasive predators, C. longicollis may be at particular risk of extinction. Given their proximity to population centers, management of the multiple threats to this species is complex and difficult. We conducted population viability analyses to assess the risk of extinction of C. longicollis under conditions of increasing adult mortality, particularly effects of female mortality via roadkill (death via collision with motor vehicles), and reduced recruitment due to fox predation of nests. We also modeled a range of management scenarios to test the effectiveness of headstarting, reduction of nest destruction via fox management, and measures that reduce adult mortality via roadkill.
Methods Chelodina longicollis is the most widespread freshwater turtle in Australia (Cann 1998). Their range broadly overlaps the capital cities of Brisbane, Melbourne, Canberra, Adelaide, and Sydney (Cann 1998; Kennett et al. 2009). Chelodina longicollis occupies a range of habitats, such as shallow ephemeral swamps, farm dams (Chessman 1988; Wong & Burgin 1997), and flowing rivers (Chessman 1988). Their lifespan is not known, but they are slow growing and may live over 100 years (Parmenter 1976; Thompson 1993). Females emerge from the water annually to oviposit one clutch of 10–20 eggs (Vestjens 1969; Parmenter 1976; Thompson 1993), and both sexes frequently migrate overland among water
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bodies to exploit ephemeral swamps (Stott 1987; Kennett & Georges 1990). They are carnivorous, consuming primarily aquatic insects and carrion (Chessman 1988). Estimates of population densities range from 26 to 400 turtles/ha (Parmenter 1976; Chessman 1978). These estimates are based on populations sampled through trapping (i.e., early juvenile or embryonic stages are not accounted for). In our models, we arbitrarily set the upper limits of the trappable population in the wild to 2000 to accommodate a wide range of wetland sizes and varying population densities. We constructed matrix population-projection models (PopTools; Hood et al. 2009) and used Vortex 10.0 (Lacy & Pollak 2015) to assess the population viability of current C. longicollis populations (Supporting Information). This represents the pre-European-settlement scenario prior to invasion of foxes and the development of roads, in which nest-predation levels were high but highly variable and minimal adult mortality occurred on land. In the post-European-settlement scenario, nest predation rates were modeled as very high and less variable; 0%, 1%, and 2% of the adult-female starting population modeled as killed each year and at 3-year intervals. We modeled a management scenario in which hatchling turtles from a separate source populations were added to the population in question at annual (and 5-year intervals) rates of 15%, 30%, 45%, 60%, and 75% of the initial adult population size. We also modeled a scenario in which foxes were managed such that nest predation rates decreased in increments of 5% up to a 70% reduction from current rates of predation (e.g., Spencer et al. 2016). We investigated the relationship between fox activity and nest-predation rate throughout much of the range of C. longicollis in southeastern Australia. From 2014 to 2016, we created nest sites with commercially purchased unfertilized chicken and quail eggs around wetlands along the Murray River (35.9561° S, 144.3693° E), Winton Wetlands (36.5496° S, 145.9834° E), and Hawkesbury (33.5965° S, 150.7505° E) regions of southeastern Australia. Two to 5 eggs were placed in an artificial nest, and 5–30 nests were created in a 200-m2 area at each site. We placed camera traps in each area and created a foxactivity index by calculating the number of days (24 h) a fox was observed by the traps and dividing that number by the number of days the camera was set. Trials were conducted for 4–9 weeks and nest-predation rates were assessed at the end of each trial. Logistic regression analyses were conducted to examine the relationship between fox activity and nest-predation rate. TurtleSAT is a citizen science tool through which incidental sightings of turtles (or their activity) can be recorded via a website, iOS, or Android App (http:// TurtleSAT.org.au). Users answer a series of questions and can upload a photograph. The entire form is geolocated automatically with the device’s in-built global positioning system. TurtleSAT has been active since May 2014,
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Figure 1. Effect of (a) mortality on adult C. longicollis populations in a pre-European environment, where nest-predation rates vary (75% ± 25%) and adult-female mortality rates are 0% (dark gray), 1% (gray), and 2% (light gray) of the starting adult-female population and effect of (b) nest predation on population growth of C. longicollis in a pre-European environment, where nest-predation rates vary (75% ± 25%) (dark gray), and a post-European environment (light gray), where nest-predation rates are high (95% ± 10%) and no adults are killed. and the database has >4700 records as October 2016. TurtleSAT is promoted by an active social media campaign (Facebook and Twitter), and numerous community groups and government agencies in each state use it to record incidental sightings of turtles. We used TurtleSAT data to map terrestrial turtle deaths (primarily road mortalities) throughout eastern Australia. Our goal was not to quantify the rates of mortality per population; rather, we sought to demonstrate the spatial scale over which mortality is occurring.
Results With no adult mortality in a pre-European environment, population growth was positive and there was a 2% risk of extinction (Table 1). As adult mortality increased, population growth rates declined (Fig. 1a) and the risk of extinction increased by approximately 40% for each 1% increase in adult mortality per year (Supporting Information). In the post-European environment, fox predation on nests increased significantly, and even when there was
no adult-female mortality populations declined (Fig. 1b) and the risk of extinction increased by 30% (Table 1). As expected, the combination of both sources of mortality led to extinction within 100 years (Table 1).
Headstarting Supplementing populations with hatchlings at a rate of 30% of the initial population size negated the impact of adult mortality and high-nest predation rates from foxes (Fig. 2a). Based on an average clutch size of 15 eggs, headstarting of hatchlings from an extra 4% of the adultfemale population replicated pre-European population growth (Fig. 2a). Lower levels of hatchling headstarting buffered the combined impacts of higher adult mortality and high nest predation rates (Fig. 2a). Translocating hatchlings into a population stabilized populations even when translocation was not made annually. Supplementing populations at the rate of 45%, 60%, and 75% of the starting adult population size every 5 years eliminated the risk of extinction (Table 1), although this pulse recruitment did not replicate pre-European conditions (Fig. 2b).
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1344 Table 1. Population growth and risk of extinction of Chelodina longicollis in Australia. Model scenario Reducing adult mortality to 0% pre-European settlement post-European settlement headstarting—post-European settlement (7.5% supplementation per year) headstarting—post-European settlement (15% supplementation per 5 years) headstarting—post-European settlement (30% supplementation per 5 years) fox management—post-European settlement (10% reduction in nest predation) fox management—post-European settlement (5% reduction in nest predation) Adult mortality at 1% of the female population pre-European settlement post-European settlement headstarting—post-European settlement (15% supplementation per year) fox management—post-European settlement (10% reduction in nest predation) fox management—post-European settlement (15% reduction in nest predation) Adult mortality at 2% of the female population pre-European settlement post-European settlement (high fox predation) headstarting—post-European settlement (15% supplementation per year) headstarting—post-European settlement (30% supplementation per year) headstarting—post-European settlement (45% supplementation per 5 years) headstarting—post-European settlement (60% supplementation per 5 years) headstarting—post-European settlement (75% supplementation per 5 years) fox management—post-European settlement (30% reduction in nest predation) fox management—post-European settlement (45% reduction in nest predation) fox management—post-European settlement (70% reduction in nest predation) pre-European settlement (harvesting at per 3 years) post-European settlement (harvesting per 3 years)
Stochastic population growth rate
Risk of extinction (0–1)
0.0485 −0.02 0.0032
0.02 0.32 0
−0.0027
0
0.0013
0
0.0309
0.01
0.0124
0.01
0.0288 −0.0442 0.006
0.41 1 0
0.0106
0.48
0.0287
0.2
0.0025 −0.0603 −0.0012 0.0155
0.96 1 0 0
−0.006
0
−0.003
0
0.0017
0
0.0363
0.55
0.0368
0.54
0.0793
0.32
0.0271 −0.044
0.39 1
Pre-European conditions include variable nest-predation rates (75% ± 25%), whereas the post-European environment includes high nestpredation rates (95% ± 10%). Headstarting, fox-management, and adult-mortality scenarios are compared. Rates of hatchling supplementation are based on initial adult population size.
Reducing Nest Predation
Preventing Adult Mortality
The effect of reducing nest predation was highly dependent on the degree of adult mortality per year. Where adult mortality rates were high, nest-predation rates had to be reduced by 70% to effectively replicate preEuropean population growth (Supporting Information), but the risk of extinction remained at 32% (Table 1). In populations with adult mortality rates of
