Projected population persistence of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) using a stage-structured life-history model and population viability analysis

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Abstract

The population of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) in the Blue River, Indiana has undergone a dramatic decline over the last decade. Recruitment in these declining populations has been negligible, and populations are now composed almost entirely of older age classes (upwards of 20 years old). Given this dramatic decline, it is imperative to assess the impacts of these demographic patterns on population growth and long-term stability. Therefore, we developed a stage-structured, life-history model to examine the effects of varying levels of egg, juvenile, and adult survivorship on abundance, recruitment, and long-term population projections. We performed a sensitivity analysis of the model and determine which life-history parameters have the greatest potential to increase/stabilise hellbender population growth. Finally, we conducted a population viability analysis to determine the probability of extinction associated with varying management strategies. For eastern hellbender populations in Indiana, adults (especially females) are the most important component of long-term population viability. Sensitivity and elasticity analyses of the Lefkovitch matrix revealed that survival of adult and egg/larvae life-history stages are the most important for focused management efforts. Indeed, adults had the highest elasticity and reproductive value in the matrix model. Increasing survival by as little as 20% corresponded to the turning point at which the population ceased to decline and increased abundance (28% survival of egg/larvae). The importance of the transition from subadult to adult (transitional matrix element) was identified as an additional factor in maintaining abundance based on the relatively long period spent in this life-history stage (seven years for females). A population viability analysis was conducted to assess the likelihood and projected time frame of extinction for this population under no management (∼25 years to complete extirpation; probability of extinction = 1) and if management efforts such as captive rearing and headstarting are undertaken (probability of extinction <0.2 at 25–30% survival of egg/larvae). Adult females had the greatest effect in reducing growth rate and population abundance when removed in exploitation simulations (91.3% versus 51.8% reduction in population growth rate), indicating translocation efforts should be designed to maintain females in the breeding pool. These models indicated that conservation management strategies aimed at ensuring the presence of adult females while concomitantly ameliorating survival at early life stages (population augmentation, translocations, introduction of artificial nest structures) are needed to stabilise the Indiana population of eastern hellbenders. This stage-structured model is the first to model eastern hellbenders and has broad implications for use across the geographic range where populations of eastern hellbenders are monitored and vital rates can be estimated.

Introduction

Developing species-specific management strategies for long-lived species with multiple discrete life-history stages is an important challenge for conservation biologists. This difficulty is partially due to the fact that long-lived species with delayed maturation and low annual recruitment rates are particularly vulnerable to anthropogenic exploitation and extinction (Congdon et al., 1994, Musick, 1999). Moreover, long-lived species facing decline may exhibit high temporal variability between successful recruitment events, allowing catastrophic events to rapidly decrease their population size (Coulson et al. 2001). While population growth rates for species are usually thought to be most dependent on adult survival and reproduction (Heppell et al. 2000), there also is an increasing appreciation for the importance of juvenile survival in long-lived species (Sergio et al. 2011). For populations of long-lived species to remain stable over time, sufficient levels of reproduction and survivorship must occur at multiple life-history stages (Sibley & Hone 2002). Further, adult female survival is vital to ensure recruitment occurs over the long lifespan of iteroparous vertebrates (Eberhardt 2002). Therefore, determination of stage-dependent vital rates is essential for understanding population dynamics and planning conservation programs for imperiled species.

Stage-based matrices, such as the Lefkovitch stage-structured model (Lefkovitch 1965), are ideal for projecting population trends for long-lived species whose life histories are characterised by stage and not annual year classes (Caswell, 2001, Crowder et al., 1994). In addition, stage-based model approaches also can incorporate sensitivity and elasticity analyses for identification of life-history stages which have the greatest potential to positively influence population growth rates. Stage-structured models also can be used to simulate competing conservation and management strategies focused on increasing recruitment or repatriation of adults to bolster reproduction and to prioritise management decisions (Dodd and Seigel, 1991, Lubben et al., 2008).

Population viability analysis (PVA) is a method for predicting the risk of population extinction based on empirical life-history information using computer simulation (Brook et al. 2000). Such analyses are useful to either simulate the demographic effects of exploitation of individuals or supplementation efforts aimed at increasing abundance across life stages. These analyses also provide managers with objective, quantitative criteria on which decisions regarding extinction risks can be made (Armbruster et al. 1999). While stage-based models and PVAs have been used for a number of species of special conservation concern, surprisingly few have been developed for amphibians (Biek et al., 2002, Homyack and Haas, 2009), many of which are facing alarming rates of decline (Griffiths and Williams, 2000, Lips et al., 2005).

Eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) are long-lived, fully aquatic salamanders found across portions of the Midwest and eastern U.S. (Petranka 1998). Many populations are experiencing declines throughout their geographic range (Wheeler et al. 2003), which is attributed to a variety of factors such as emerging infectious diseases (Briggler, 2007, Souza et al., 2012), over-collection and exploitation (Nickerson & Briggler 2007), and sedimentation (Petranka 1998). Eastern hellbender declines are often characterised by a complete lack of recruitment, thus characterising survivorship of early life stages is vital as slight changes in egg and larval survival may have drastic effects for overall population growth rates (Crouse et al. 1987). In eastern hellbenders, it has been hypothesised that early life-history stage individuals may be sensitive to increased predation pressure (Gall & Mathis 2009) or may be negatively affected by increased turbidity and lower quality habitats as has been observed for the Japanese giant salamander Andrias japonicas (Okada et al. 2008). Clearly, factors which contribute to lower survival in the youngest life-history stages of eastern hellbenders must be understood in order to decipher the underlying changes in demography noted for declining populations of this subspecies.

Populations of eastern hellbenders within Indiana are currently confined to a 112 km stretch within the Blue River, Indiana. Several studies over the last two decades have documented not only dramatic declines in population abundance, but a general shift to a large-bodied and presumably geriatric population (Burgmeier et al., 2011, Kern, 1984). If this decline continues unabated, remnant river demes within the Blue River may become increasingly fragmented and suffer reduced reproductive potential (Allee, 1931, Berec et al., 2007). Repatriation (release of individuals into an area currently occupied by a species) and headstarting (HS; early life stages reared in captivity to a larger size then subsequently released) are two primary management techniques which have been used to augment amphibian populations (Dodd and Seigel, 1991, Lannoo, 2005). Therefore, it is essential to simulate the efficacy of repatriation of adults or subadults and headstarting programs aimed at increasing survival at early life stages for the declining population of eastern hellbenders in Indiana.

Herein, we developed a stage-structured, life-history model for eastern hellbenders in Indiana. Using this approach, our goal was to examine the effects of management aimed at increasing early life stages (eggs and larvae) of eastern hellbenders and translocation of adults and subadults on projected population dynamics of this species. The specific objectives were to utilise stage-structured modeling of eastern hellbenders in Indiana to: (1) examine the effects of varying levels of egg, juvenile, and adult survivorship on abundance, recruitment, and long-term population projections; (2) perform a sensitivity analysis of the model and determine which life-history parameters have the greatest potential to increase/stabilise hellbender population growth; and (3) conduct a population viability analysis to determine the probability of extinction associated with varying management strategies. This stage-structured modeling approach has broad-scale implications for other eastern hellbender populations with similar demographic profiles (e.g., all populations within the Ohio River drainage), and is especially relevant for current management and conservation needs considering the recent listing of the Ozark hellbender (Cryptobranchus alleganiensis bishopi) as federally endangered and candidate listing of the eastern hellbender subspecies for federal protection.

Section snippets

Study site and sample collection

Our study site, the Blue River watershed is located in southern Indiana, USA and flows 112 km until its confluence with the Ohio River near Leavenworth in southern Indiana. Land along the river corridor consists of mixed forest, agriculture, and small levels of development. River habitat consists of riffle and runs interspersed with long stretches of pooled water, and the dominant substrate types consist of a mixture of gravel, cobble, and bedrock. Sample sites within the Blue River were

Lefkovitch matrix model

The first step to parametising our model was to assess stage-specific survival rates, subadult transitional probabilities, and fecundity of the adult life-history stage. The probability of surviving and remaining a subadult was 0.711 and the probability of a subadult transitioning to an adult was 0.038 (Fig. 2). The fecundity was 90 eggs per female per year once the adult survival rate (80%), and breeding periodicity (30%) were incorporated into the model. Of the three main matrix parameters,

Discussion

We used various methods (matrix model, population projection, and PVA) to simulate the trajectory for the Indiana eastern hellbender population. We initially determined which life stages are likely to respond to management and then simulated the effect exploitation and conservation-management strategies would have on population growth. The results of this multi-modeling approach indicate that the most effective means to prevent extirpation is to concomitantly maintain adult female presence,

Acknowledgements

We thank many individuals who helped in the collection of field and genetic samples for this project including Zack Olson, Steve Kimble, Bart Kraus, Cody Marks, Lucas Woody, and Nick Burgmeier. We also thank members of the Williams lab and Dr. Gene Rhodes for their input regarding this manuscript. This project could not have been possible without support provided by the Indiana Department of Natural Resources (E2-07-WD0007). Animals were collected under permits issued by Indiana Department of

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