Translocation Experiments with Butterflies Reveal Limits to Enhancement of Poleward Populations Under Climate Change

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Translocation Experiments with Butterflies Reveal Limits to Enhancement of Poleward Populations Under Climate Change Translocation experiments with butterflies reveal limits to enhancement of poleward populations under climate change Shannon L. Pelinia,1, Jason D. K. Dzurisina, Kirsten M. Priora, Caroline M. Williamsb, Travis D. Marsicoa,2, Brent J. Sinclairb, and Jessica J. Hellmanna,3 aDepartment of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556; and bDepartment of Biology, University of Western Ontario, London, ON, Canada N6A 5B7 Edited by Paul R. Ehrlich, Stanford University, Stanford, CA, and approved May 13, 2009 (received for review January 12, 2009) There is a pressing need to predict how species will change their zation of new sites also could be limited by host plant availability in geographic ranges under climate change. Projections typically species that share their range boundary with host resources (6). assume that temperature is a primary fitness determinant and that In addition, populations at the range edge could be locally populations near the poleward (and upward) range boundary are adapted. Previous studies suggest that isolation, genetic drift, and preadapted to warming. Thus, poleward, peripheral populations local selection can lead to locally adapted forms, including at the will increase with warming, and these increases facilitate poleward range edge (7–9). If peripheral populations are not preadapted to range expansions. We tested the assumption that poleward, pe- warmer climates that are characteristic of their range center, ripheral populations are enhanced by warming using 2 butterflies climate change may not enhance peripheral populations (10–12). (Erynnis propertius and Papilio zelicaon) that co-occur and have Without enhancement to increase the number of potential colo- contrasting degrees of host specialization and interpopulation nists, poleward colonization could be restricted (3, 4, 13). Range genetic differentiation. We performed a reciprocal translocation contraction at the poleward boundary is even possible if peripheral experiment between central and poleward, peripheral populations populations decline and fail to colonize new locations. ECOLOGY in the field and simulated a translocation experiment that included These limitations on peripheral enhancement and associated alternate host plants. We found that the performance of both implications for the colonization of new habitats are generally not central and peripheral populations of E. propertius were enhanced considered in predictions under climate change (see 14–16). Yet, during the summer months by temperatures characteristic of the this process demands consideration just as natural and human- range center but that local adaptation of peripheral populations to caused dispersal limitation and lack of available habitat can con- winter conditions near the range edge could counteract that strain geographic range change (17). Furthermore, because fitness enhancement. Further, poleward range expansion in this species is is an integration of the total experience of an individual, life stages prevented by a lack of host plants. In P. zelicaon, the fitness of may differ or even counteract one another in their responses to central and peripheral populations decreased under extreme sum- climate change. For example, in Papilio canadensis (Lepidoptera: mer temperatures that occurred in the field at the range center. Papilionidae), increased temperatures are beneficial to growth and Performance in this species also was affected by an interaction of development rates when they occur during the growing season (18), temperature and host plant such that host species strongly medi- but they can have detrimental effects on mass and survivorship ated the fitness of peripheral individuals under differing simulated when they occur during late autumn, winter, or spring (19). temperatures. Altogether we have evidence that facilitation of In this study, we employ field and lab experiments to test the poleward range shifts through enhancement of peripheral popu- assumption of peripheral enhancement that underlies many pro- lations is unlikely in either study species. jections of climate-driven geographic range shifts. We examine the performance of 2 butterfly species, Erynnis propertius (Lepidop- Lepidoptera ͉ range center ͉ range expansion ͉ range periphery tera: Hesperiidae) and P. zelicaon (Lepidoptera: Papilionidae) at the poleward periphery and latitudinal center of their shared he biological impacts of climate change are likely to be multi- coastal geographic distribution. These species differ in resource Tfaceted, involving behavioral change, evolutionary change, and specialization and interpopulation gene flow from the center to the local and global extinction, but a well-documented response is periphery of the species’ ranges (3). Zakharov and Hellmann (3) geographic range change. Given a species that is completely occu- found that peripheral populations of the smaller-bodied and more pying its thermal niche, warming should open poleward (or upward) specialized species, E. propertius, are strongly differentiated from territory to population establishment (1, 2). In most cases we would their central counterparts whereas P. zelicaon exhibits more gene expect establishment to be driven by populations at the poleward flow across its geographic range. We expected to find that periph- eral populations of P. zelicaon are more likely than E. propertius to (or elevational) periphery of a species’ range. If these peripheral be enhanced by warming because we hypothesize that local adap- populations are preadapted to warmer conditions, due to gene tation occurs in E. propertius (4). Further, P. zelicaon can move swamping from the center of the range or historical selection under poleward without host plant limitations while lack of host plants warmer conditions, we would expect them to increase with warming and thereby enhance the colonization process (3, 4). The assump- tions underlying this ‘‘peripheral enhancement,’’ however, have not Author contributions: S.L.P., C.M.W., B.J.S., and J.J.H. designed research; S.L.P., J.D.K.D., been tested despite their significance in determining geographic K.M.P., C.M.W., and T.D.M. performed research; S.L.P. and C.M.W. analyzed data; and range change under climate change. S.L.P., C.M.W., B.J.S., and J.J.H. wrote the paper. A number of factors could prevent peripheral population en- The authors declare no conflict of interest. hancement. Resource availability and quality in peripheral locales This article is a PNAS Direct Submission. could limit the growth of poleward populations or the colonization 1Present Address: Harvard Forest, Harvard University, Petersham, MA 01366. of poleward locales. In herbivorous insects, for example, interac- 2Present address: Department of Biological Sciences, Mississippi State University, Mississippi tions with host plants could change under climate change, poten- State, MS 39762. tially counteracting any direct effects of warming (5). The coloni- 3To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0900284106 PNAS Early Edition ͉ 1of6 Downloaded by guest on September 30, 2021 will prohibit immediate colonization of poleward habitats by A B E. propertius. Erynnis propertius (Propertius duskywing) is a small-bodied (4-cm wingspan) oak (Quercus spp. [Fagaceae]) specialist that ranges along the coast from Baja California, Mexico to southeast Van- couver Island, British Columbia (20). It overwinters as a sixth instar caterpillar and is univoltine in most of its range (21). In the southern portion of its range, it consumes a wide range of oak species including Q. agrifolia and Q. kelloggii (22). Northward of southern Oregon, the butterfly feeds only on Q. garryana (Garry oak) (20, 23), and there are no suitable host plants beyond its current range boundary. The geographic distribution of Q. garryana is expected to shift poleward under climate change (24), but the differential dispersal abilities and generation times of E. propertius and Q. Fig. 1. Field translocation survivorship (A) and body size (B) results for E. garryana will likely create a lag, initially prohibiting E. propertius propertius. Black bars show performance of larvae from the center, and gray are those from the periphery of the species’ range. (A) Mean (Ϯ95% CI) from colonizing poleward locales. proportion of larvae surviving to the end of the experiment in each cage. (B) Papilio zelicaon (Anise swallowtail) is a larger (8-cm wingspan) Mean (Ϯ95% CI) of total mass of surviving fifth instar larvae in each cage. Data butterfly that feeds on plants in the Apiaceae family including both shown are untransformed (see Materials and Methods). *, denotes a statisti- native (e.g., Lomatium spp.) and non-native plants (e.g., garden cally significant difference between rearing regions (P Ͻ 0.05). plants such as parsley, carrot, etc.) in a variety of habitats (20, 25). It occurs throughout western North America and overwinters in pupal diapause (26). Host plants that are potentially suitable occur effect on survivorship (larval source: F1,51 ϭ 0.97, P ϭ 0.33; rearing northward of the current range limit. Populations throughout the region: F1,51 ϭ 0.31, P ϭ 0.58), with no significant interaction (F1,51 species’ range vary in voltinism, depending upon weather and host ϭ 2.4, P ϭ 0.12) (Fig. 1A). Enclosures containing larvae from the plant phenology (23). The 2 butterflies share a coastal, northern range periphery had marginally higher larval mass than those from range limit where open, oak-dominated
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