Projected population persistence of eastern hellbenders (Cryptobranchus alleganiensis alleganiensis) using a stage-structured life-history model and population viability analysis
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
References (76)
- et al.
Assessing the value of follow-up translocations: A case study using New Zealand robins
Biological Conservation
(2001) - et al.
Multiple Allee effects and population management
Trends in Ecology & Evolution
(2007) - et al.
The use and abuse of population viability analysis
Trends in Ecology and Evolution
(2001) - et al.
Using long-term data and a stage-classified matrix to assess conservation strategies for an endangered turtle (Clemmys guttata)
Biological Conservation
(2008) - et al.
Long-term effects of experimental forest harvesting on abundance and reproductive demography of terrestrial salamanders
Biological Conservation
(2009) - et al.
Management recommendations based on matrix projection models: The importance of considering biological limits
Biological Conservation
(2008) - et al.
Vital rate sensitivity analysis as a tool for assessing management actions for the desert tortoise
Biological Conservation
(2009) - et al.
Variation in age-structured vital rates of a long-lived raptor: Implications for population growth
Basic and Applied Ecology
(2011) - et al.
Population declines of a long-lived salamander: A 20+-year study of hellbenders, Cryptobranchus alleganiensis
Biological Conservation
(2003) Animal aggregations. A study in general sociology
(1931)
Natural mortality of eggs and larvae of Ambystoma t. tigrinum
Ecology
Time frames for population viability analysis of species with long generations: An example with Asian elephants
Animal Conservation
Movement patterns and habitat use of soft-released translocated spur-thighed tortoises, Testudo graeca
European Journal of Wildlife Research
Estimation of survival rate and extinction probability for stage-structured populations with overlapping life stages
Population Ecology
The ecology of post-metamorphic Bufo marinus in central Amazonian savanna
What is missing in amphibian decline research: Insights from ecological sensitivity analysis
Conservation Biology
Ambient UV-B radiation causes deformities in amphibian embryos
Proceedings of the National Academy of Sciences of USA
Survival and body condition of captive-reared juvenile Ozark hellbenders (Cryptobranchus alleganiensis bishopi) following translocation to the wild
Copeia
Cryptobranchus alleganiensis (Hellbender) Chytrid fungus
Herpetological Review
Construction and use of artificial shelters to supplement habitat for hellbenders (Cryptobranchus alleganiensis)
Herpetological Review
Predicting accuracy of population viability analysis in conservation biology
Nature
Population status of the eastern hellbender (Cryptobranchus alleganiensis alleganiensis) in Indiana
Journal of Herpetology
The Bender board: A new design for the restraint and measurement of hellbenders
Herpetological Review
Matrix population models: Construction, analysis, and interpretation
Effect of capture date on nest-attempt rate of translocated sharp-tail grouse Tympanuchus phasianellus
Wildlife Biology
Demographics of common snapping turtles (Chelydra serpentina): Implications for conservation and management of long-lived organisms
American Zoologist
A stage-based population model for loggerhead sea turtles and implications for conservation
Ecology
Predicting the impact of turtle excluder devices on loggerhead sea turtle populations
Ecological Applications
Elasticity: The relative contribution of demographic parameters to population growth rate
Ecology
Relocation, repatriation, and translocation of amphibians and reptiles: Are they conservation strategies that work?
Herpetological
A paradigm for population analysis of long-lived vertebrates
Ecology
Models for management of wildlife populations: Lessons from spectacled bears in zoos and grizzly bears in Yellowstone
System Dynamics Review
A vital rate sensitivity analysis for nonstable age distributions and short-term planning
Journal of Wildlife Management
Population status of hellbender salamanders (Cryptobranchus alleganiensis) in the Allegheny River drainage of New York State
Journal of Herpetology
Viability of the southern elephant seal population of the Falkland Islands
Animal Conservation
Innate predator recognition and the problem of introduced trout
Ethology
Suitability of amphibian and reptiles for translocation
Conservation Biology
Insights into the mating habits of the tiger salamander (Ambystoma tigrinum tigrinum) as revealed by genetic parentage analyses
Molecular Ecology
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