Letters
Reintroduction As an Ecosystem Restoration Technique The primary motivation for animal reintroductions remains the recovery of single species and not ecosystem restoration (Seddon et al. 2007). Nevertheless, the extirpation of any species (especially keystone species) likely will have effects on other species or attributes of the ecosystem; thus, reintroductions may play a key role in ecosystem restoration and in the reestablishment of ecosystem functions (Lipsey & Child 2007). Loss of a species affects ecosystem function, yet the functional relation between the 2 is still debated (Hillebrand & Matthiessen 2009). Studying the effect of species’ losses on ecosystems is difficult because baseline data on ecosystem functions prior to the species’ extirpation are usually unavailable and experimentation at adequate scales is almost impossible because in situ removal of populations and long-term monitoring to detect systematic changes are required (Loreau et al. 2001). By contrast, successful reintroductions can be viewed as natural, spatially extensive experiments that can be used to examine the effect of a species on ecosystem functions (Sarrazin & Barbault 1996). Furthermore, extirpations often occur decades before the reintroduction, so we expect the effect of the extirpation to have cascaded through the system at measurable levels. Of 890 peer-reviewed articles on reintroduction published between 1980 and 2009 (ISI Web of Knowledge, search term: species reintroduction), 63 (7.6%) examine how a reintroduction affects an ecosystem. Of these, 47 articles are on mammals (18 on the gray wolf [Canis lupus] reintroduction to Yellowstone National Park, U.S.A., and 7 on Eurasian beaver [Castor fiber] reintroductions in Europe). The number of articles on reintroduction that are ecosystem oriented increased from 18 between 1990 and 1999 to 45 between 2000 and 2009 (zero articles before 1990). The main issues addressed in these articles were disease transmission (15 articles) by reintroduced species (e.g.,Viggers et al. 1993); interactions of the introduced species with another local species (13 papers; e.g., a prey species’ response to a reintroduced predator [Mao et al. 2005]) or resource competition between the reintroduced and local species (Carrera et al. 2008); and changes in abundance and community composition of local plants due to grazing (Johnson & Cushman 2007) or of local animals due to predation by the reintroduced species (12 424 Conservation Biology, Volume 25, No. 3, 424–427 C 2011 Society for Conservation Biology DOI: 10.1111/j.1523-1739.2011.01669.x
articles). From 1990 through 1999, all articles except one address these topics, and 72% (18 articles) address harmful effects to the ecosystem caused by reintroductions, especially disease transmission (11 articles). From 2000 through 2009, only 13% (6 articles) address harmful effects, whereas the rest discuss restoration effects, considering topics such as trophic cascades (9 articles of which 7 are about wolf reintroduction to Yellowstone National Park), reestablishment of ecosystem functions (6 articles; e.g., seed dispersal and food augmentation of prey), and ecosystem engineering (i.e., changes induced by the reintroduced species in the physical attributes of the ecosystem that affect the other biota [VanNimwegen et al. 2008]) (7 articles). We believe that studies on the role of reintroductions in restoring ecosystem functions should be integrated into broad reintroduction programs. Temporal trends in key ecosystem functions, hypothesized to have been affected by the original extirpation, should be addressed. By comparing these temporal trends between areas occupied by the reintroduced species and similar areas within the historical range that are yet unoccupied, the role of the reintroduced species in restoring ecosystem functions can be elucidated. We believe a systematic approach to examining the effects of reintroductions on ecosystem functions is no less important than conserving the reintroduced species. Tal Polak and David Saltz Mitrani Department of Desert Ecology, Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, 84990 Midreshet Ben-Gurion, Israel, email
[email protected]
Literature cited Carrera, R., W. Ballard, P. Gipson, B. T. Kelly, P. R. Krausman, M. C. Wallace, C. Villalobos, and D. B. Wester. 2008. Comparison of Mexican wolf and coyote diets in Arizona and New Mexico. Journal of Wildlife Management 72:376–381. Hillebrand, H., and B. Matthiessen. 2009. Biodiversity in a complex world: consolidation and progress in functional biodiversity research. Ecology Letters 12:1405–1419. Johnson, B. E., and J. H. Cushman. 2007. Influence of a large herbivore reintroduction on plant invasions and community composition in a California grassland. Conservation Biology 21:515–526. Lipsey, M. K., and M. F. Child. 2007. Combining the fields of reintroduction biology and restoration ecology. Conservation Biology 21:1387–1388. Loreau, M., et al. 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808.
Letters Mao, J. S., M. S. Boyce, D. W. Smith, F. J. Singer, D. J. Vales, J. M. Vore, and E. H. Merrill. 2005. Habitat selection by elk before and after wolf reintroduction in Yellowstone National Park. Journal of Wildlife Management 69:1691–1707. Sarrazin, F., and R. Barbault. 1996. Reintroduction: challenges and lessons for basic ecology. Trends in Ecology & Evolution 11:474–478. Seddon, P. J., D. P. Armstrong, and R. F. Maloney. 2007. Developing the science of reintroduction biology. Conservation Biology 21:303–312. VanNimwegen, R. E., J. Kretzer, and J. F. Cully Jr. 2008. Ecosystem engineering by a colonial mammal: how prairie dogs structure rodent communities. Ecology 89:3298–3305. Viggers, K. L., D. B. Lindenmayer, and D. M. Spratt. 1993. The importance of disease in reintroduction programs. Wildlife Research 20:687–698.
Temperature Constraint of Elevational Range of Tropical Amphibians: Response to Forero-Medina et al. Introduction Forero-Medina et al. (2011) propose a novel approach to evaluation of constraints on species’ range shifts in response to increasing temperatures by simulating upslope movement of montane tropical amphibians. Their approach is original because it goes beyond predicting how species will respond to climate change under different climatic scenarios. They used a spatially explicit framework to examine how topographical barriers could limit the movement of organisms across the landscape. Although their approach is innovative, several assumptions on which their model is based are not well grounded in the natural history of tropical amphibians. Thus, the model de-emphasizes the importance of the behavior of individuals and population processes in determining species’ responses to climate change. Furthermore, model predictions cannot be tested for amphibian species that may already be extinct.
Temperature Constraints on Elevational Distribution The core assumption Forero-Medina et al. apply in their model is that the narrow elevational range of tropical amphibians reflects their narrow thermal tolerances. This assumption stems from Janzen’s (1967) hypothesis that tropical mountain passes are stronger barriers to organismal dispersal than temperate passes at similar elevations. Janzen bases his hypothesis on the assumption that a mountain pass is a greater barrier to dispersal if the overlap in temperature ranges between the foothill and the top of the mountain is small. Janzen (1967) proposes that high-elevation areas have low overlap in
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temperature ranges with the lowlands and that tropical organisms will evolve narrow physiological tolerances and thus be less apt to cross mountain passes. In the late 1960s tropical ecosystems were perceived as having little temperature variation. Nevertheless, high-elevation tropical sites can experience daily temperature fluctuations that exceed annual thermal variation (Navas 1996a; Ghalambor et al. 2006). Therefore, high-elevation organisms are exposed to a broader range of temperatures and may have greater physiological tolerances than lowland organisms. The assumption that montane tropical amphibians have narrow physiological tolerances is not supported by physiological research. Navas (1996b, 1997) has shown that high-elevation frogs in the Colombian Andes have much broader performance breadths than congeneric lowland species and that differences in metabolism and behavior among frog species from different elevations are small. High-elevation species of several frog genera, for example, can swim as well at 5 ◦ C as they can at 25 ◦ C (Navas 1996b), a temperature that is much warmer than the average temperature of their habitats. Therefore, the lower bound of the elevational range of montane species does not seem to be constrained by the frogs’ thermal tolerances. The narrow elevational range of these organisms may not be a consequence of constraints imposed by their thermal physiology. An additional limitation of Forero-Medina et al.’s model is that it does not incorporate basic differences in behavior among frogs (Navas 1996a). These differences are important because what affects behavior at the individual level are temperatures that amphibians experience in their microhabitats (Bakken 1982; Stevenson 1985). Diurnal amphibians may be more vulnerable to warming because they are most active when environmental temperatures are closer to their daily maxima. In contrast, nocturnal behavior could keep many lowland amphibians from experiencing stressful temperatures during critical periods for foraging and breeding. Furthermore, avenues of heat exchange, such as sunlight and evaporative water loss, differ significantly between diurnal and nocturnal amphibians, which influences the amphibians’ abilities to physiologically and behaviorally respond to suboptimal temperatures (Navas 1996a). Forero-Medina et al.’s model did not include variation in lapse rate and increased temperatures along the elevational gradient; instead, temperature changes were modeled as gradual increases with a constant lapse rate. Both lapse rate and degree of warming are known or predicted to vary as a function of elevation in Neotropical mountains (Urrutia & Vuille 2009). On the basis of regional climate models, it is predicted that high-elevation areas will warm faster than lowlands (but see Vuille et al. 2003). Incorporating these sources of variation in the model may strengthen (or weaken) topographic barriers at higher elevations.
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Importance of Reproductive Mode A potential pitfall in modeling amphibian habitat quality as a function of temperature is that amphibians differ significantly in how they reproduce and in their reliance on water. Many Neotropical montane amphibians inhabit steep slopes, where runoff quickly drains downhill through fast-flowing streams. These amphibians are mostly stream- or terrestrial-breeding species. Whereas forest cover and the availability of moist leaf litter are the main constraints to reproduction in terrestrial-breeding species, stream-breeding species are likely limited by how streams are distributed and connected. Pond-breeding species from the lowlands will not be able to colonize steep slopes because these landscapes lack breeding habitats. The scarcity or absence of lentic areas at intermediate elevations is likely to be a stronger constraint to upward shift of lowland species than temperature and land cover. In Forero-Medina et al.’s model, pond availability could be modeled as a function of topographic slope. Steep terrain without ponds could then be identified as a barrier to the dispersal of pond-breeding species.
Testing Model Predictions for Declining Taxa Many montane Neotropical amphibians are disappearing quickly (Lips et al. 2006; Catenazzi et al. 2011). I think steep population declines and amphibian extinctions from the mountains of Central and South America should be taken into consideration when developing models that will form the basis of conservation actions. The predictions of Forero-Medina et al.’s model cannot be tested with species that may already be extinct: none of the 5 species of Atelopus they considered, for example, has been reported in the past 18 years (La Marca et al. 2005; Lips et al. 2008). Conservation strategies will greatly benefit from models that incorporate current knowledge on physiology, behavior, and natural history of endangered organisms.
Acknowledgments I thank D. Moreno-Mateos, J. I. Watling, S. M. Whitfield, and 3 anonymous reviewers for comments on the manuscript. Alessandro Catenazzi Department of Integrative Biology, University of California at Berkeley, Berkeley, CA 94707, U.S.A., email
[email protected]
Literature cited Bakken, G. S. 1992. Measurement and application of operative and standard operative temperatures in ecology. American Zoologist 32:194–216. Catenazzi, A., E. Lehr, L. O. Rodr´ıguez, and V. T. Vredenburg. 2011. Batrachochytrium dendrobatidis and the collapse of anu-
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Letters ran species richness and abundance in the upper Manu National Park, southeastern Peru. Conservation Biology DOI:10.1111/j.1523– 1739.2010.01604.x. Forero-Medina, G., L. Joppa, and S. L. Pimm. 2011. Constraints to species’ elevational range shifts as climate changes. Conservation Biology 25:163–171. Ghalambor C. K., R. B. Huey, P. R. Martin, J. J. Tewksbury, and G. Wang. 2006. Are mountain passes higher in the tropics? Janzen’s hypothesis revisited. Integrative and Comparative Biology 46:5–17. La Marca, E., et al. 2005. Catastrophic population declines and extinctions in Neotropical harequin frogs (Bufonidae: Atelopus). Biotropica 37:190–201. Lips, K. R., F. Brem, R. Brenes, J. D. Reeve, R. A. Alford, J. Voyles, C. Carey, L. Livo, A. P. Pessier, and J. P. Collins. 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences USA 103:3165–3170. Lips K. R., J. Diffendorfer., J. R. Mendelson III, and M. W. Sears. 2008. Riding the wave: reconciling the roles of disease and climate change in amphibian declines. Public Library of Science Biology 6 DOI: 10.1371/journal.pbio.0060072. Navas, C. A. 1996a. Implications of microhabitat selection and patterns of activity on the thermal ecology of high elevation Neotropical anurans. Oecologia 108:617–626. Navas, C. A. 1996b. Metabolic physiology, locomotor performance, and thermal niche breadth in neotropical anurans. Physiological Zoology 69:1481–1501. Navas, C. A. 1997. Thermal extremes at high elevations in the Andes: physiological ecology of frogs. Journal of Thermal Biology 22:467–477. Stevenson, R. D. 1985. The relative importance of behavioral and physiological adjustments controlling body temperature in terrestrial ectotherms. The American Naturalist 126:362–386. Urrutia, R., and M. Vuille. 2009. Climate change projections for the tropical Andes using a regional climate model: temperature and precipitation simulations for the end of the 21st century. Journal of Geophysical Research 114 DOI:10.1029/2008JD011021. Vuille, M., R. Bradley, M. Werner, and F. Keimig. 2003. 20th century climate change in the tropical Andes: observations and model results. Climate Change 59:75–99.
Thermal Tolerance, Range Expansion, and Status of Tropical Amphibians: Reply to Catenazzi We thank Catenazzi for his extensive discussion of temperature constraints of tropical amphibians and agree that many factors constrain their movement. Indeed, our paper details them. Catenazzi’s response errs in three ways, however. First, we do not assume these species have “narrow thermal tolerances,” only that their observed elevational ranges are accurate. Second, one should not proliferate unneeded hypotheses. No evidence suggests the extent of species’ elevational or thermal ranges increases if the animals migrate to locations with cooler climates. Were this to be so generally, climate change would not represent a threat for any species. Third, our observations and recent literature demonstrate that several of the species he references as possibly extinct or unreported are extant and procreating (Carvajalino-Fernandez et al. 2008; Granda-Rodriguez et al. 2008a, 2008b).
Letters
German Forero-Medina,∗ Lucas Joppa,† and Stuart L. Pimm∗ ∗ Nicholas
School of the Environment, Duke University, Durham, NC 27708, U.S.A. †Microsoft Research, 7 JJ Thomson Avenue, Cambridge CB3 0FB, United Kingdom
Literature Cited Carvajalino-Fernandez, J. M., B. Cuadrado-Pena, and M. P. RamirezPinilla. 2008. Additional records of Atelopus nahumae and Atelopus
427 laetissimus from Sierra Nevada de Santa Marta, Colombia. Actualidades Biologicas 30(88):97–103. Available from http://www.scielo. unal.edu.co/scielo.php?script=sci arttext&pid=S0304–358420080 00100008&lng=en&nrm=iso (accessed January 2011). Granda-Rodriguez, H. D., A. Del Portillo-Mozo, and J. M. Renjifo. 2008a. Range extension of the harlequin frog Atelopus nahumae (Anura:Bufonidae). Herpetotropicos 4:85–86. Granda-Rodriguez, H. D., A. Del Portillo-Mozo, and J. M. Renjifo. 2008b. Uso de habitat en Atelopus laetissimus (Anura:Bufonidae) en una localidad de la Sierra Nevada de Santa Marta, Colombia. Herpetotropicos 4:87–93.
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