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Diversifying Coevolution Between Crossbills and Conifers

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Diversifying Coevolution Between Crossbills and Conifers Evo Edu Outreach (2010) 3:47–53 DOI 10.1007/s12052-009-0190-8 ORIGINAL SCIENTIFIC ARTICLE Diversifying Coevolution between Crossbills and Conifers Craig W. Benkman Published online: 16 December 2009 # Springer Science+Business Media, LLC 2009 Abstract Coevolution between granivorous crossbills Crossbill Diversity (Loxia spp.) and conifers has been a prominent process in the diversification of crossbills. A striking example occurs Twenty years ago, I began experiments to test a hypothesis in western North America where coevolution between for the ecological basis of Red Crossbill (Loxia curvirostra crossbills and Rocky Mountain lodgepole pine (Pinus complex) diversity. I had been studying crossbills in eastern contorta latifolia) is ongoing in isolated ranges without North America, and I had hypothesized that each species of the crossbill’s dominant competitor for seeds, the red crossbill was adapted for foraging on a different species of squirrel (Tamiasciurus hudsonicus). Preferential foraging conifer that had certain characteristics that allowed for by crossbills on lodgepole pine cones in the South Hills and specialization (Benkman 1987a, b). Although crossbills are Albion Mountains, two small mountain ranges in southern highly specialized seed predators (Fig. 1)thatmightbe Idaho where red squirrels are absent, has led to the evolution expected to coevolve with conifers, I had largely dismissed of larger, thicker-scaled cones than in nearby ranges where red such coevolution. The prevailing view by those studying squirrels are present. This in turn has favored the evolution of bird–plant interactions was that strong coevolutionary inter- larger-billed crossbills that have diverged from other cross- actions were rare (e.g., Wheelwright and Orians 1982; bills in the region. However, such diversifying coevolution, Feinsinger 1983; see Thompson 1994). Moreover, the classic resulting from geographic variation in the distribution studies on seed-eating birds (e.g., Newton 1972; Schluter of strongly interacting species, is vulnerable to species and Grant 1984; Pulliam 1985) indicated that considerable introductions. For example, the introduction of red squirrels insight could be gained without considering whether plants caused the precipitous decline and perhaps extinction of the were evolving defenses in response to selection exerted by Newfoundland crossbill and perhaps a crossbill endemic to birds (but see Pulliam and Brand 1975). the Cypress Hills, Canada. In general, species introductions There are two groups of crossbills globally. One group is act to reduce the geographic variation in species interactions, comprised of three distinct taxa with white wing bars. The which may be critical for the diversification of many taxa. Two-barred Crossbill (Loxia leucoptera bifasciata)in Eurasia, the White-winged Crossbill (Loxia leucoptera Keywords Crossbills . Conifers . Coevolution . leucoptera) in the northern boreal forests of North America, Competition . Loxia . Tamiasciurus . Pinus contorta and the Hispaniolan Crossbill (Loxia megaplaga) endemic to the pine forests atop two mountain ranges on Hispaniola. The other group, called Red Crossbills in the New World and Common Crossbills in the Old World, is much more diverse morphologically (Fig. 2) than the “wing-barred” crossbills and is widespread in the pine (Pinus spp.) and C. W. Benkman (*) spruce (Picea spp.) forests of the Northern Hemisphere Department of Zoology and Physiology, Program in Ecology, (Newton 1972). Most of the variation among Red/Common University of Wyoming, “ ” Laramie, WY, USA Crossbills is categorized into call types that are distin- e-mail: [email protected] guished by differences in their vocalizations and in their bill 48 Evo Edu Outreach (2010) 3:47–53 Fig. 1 South Hills crossbills foraging on lodgepole pine cones. scales, the lower mandible is abducted laterally (b), spreading the Crossbills forage in a very stereotypic manner. a First, crossbills orient scales apart, and exposing the seeds at their base. After using their so that the vertical axis of the bill is aligned with the elongated tongue to reach into the gap between the scales to lift the seed out, surfaces of the cone scales, and then bite between adjacent and often crossbills secure the seed in a lateral groove in their palate. Their hard, woody scales. Their crossed and decurved mandibles are key lower mandible cracks the seed coat, and the tongue and lower because they enable crossbills to exert and withstand strong forces at mandible remove and discard the seed coat before the kernel is the mandible tips. Once the mandible tips reach between adjacent cone swallowed (photos: the author) and body sizes (Groth 1993; Benkman 1999; Summers et al. hemlock (Tsuga heterophylla), Douglas-fir (Pseudotsuga 2002, 2007; Edelaar et al. 2008); two call types in Eurasia, menziesii), Rocky Mountain lodgepole pine (Pinus contorta the Parrot Crossbill (Loxia pytyopsittacus) and Scottish latifolia), and Rocky Mountain ponderosa pine (Pinus Crossbill (Loxia scotica), are recognized as distinct species, ponderosa scopulorum). To test the hypothesis, I captured and most other call types likely represent subspecies, over 30 crossbills from the four call types and housed them species, or incipient species. in aviaries where I could conduct foraging experiments. The hypothesis I tested was whether each of the four Then I collected conifer cones and measured how fast common call types in western North America was adapted to a crossbills could remove seeds from average-sized cones different species of conifer whose seeds and cones are from each of the four conifers. I then solved for the optimal morphologically distinct from each other, and produce and bill depth for foraging on each of the conifers (Fig. 3). If hold seeds in their cones in a sufficiently reliable manner to each call type was adapted for foraging on a particular allow specialization by crossbills. I predicted the “key conifer, then the average bill depth of a given call type conifers,” which represent a small subset of all of the conifers should match the predicted optimum. in the crossbills’ ranges, by examining the forestry literature My experiments revealed that two of the call types that provided information on seed production and seed matched the predicted optima, whereas two others were retention. My four hypothesized key conifers were western smaller than predicted (Benkman 1993). That the bill sizes of two of the call types were smaller than predicted did not cause me to reject the hypothesis, in part because I was able to estimate the optimal width of the groove in the crossbill’s palate that is used to secure seeds while they are husked; groove width influences seed handling time, whereas bill depth is related to providing access to seeds in the cones (Fig. 3). In the case of the groove width, each call type matched or closely approximated the predicted optimum (Benkman 1993). Overall, the data were consistent with the hypothesis that each call type was adapted to a single species of conifer. Moreover, I could predict these conifers a priori based on their seed production and seed retention. Fig. 2 Crossbills vary greatly in bill and body size. This shows the Interestingly, I initially hypothesized a fifth key conifer, extremes in the variation in bill size, with the Parrot Crossbill (Loxia Sitka spruce (Picea sitchensis), and thus a fifth call type pytyopsittacus; top), the largest crossbill, and the Common Crossbill, (Benkman 1993). I had gathered foraging data on Sitka Loxia curvirostra himalayensis (bottom; sensu Edelaar 2008), from spruce cones, and I and my first graduate student, Bill the Himalayan Mountains the smallest. There are at least 12 distinct taxa of crossbills in the New World and probably up to 20 in the Old Holimon, searched throughout much of the range of Sitka World (photo: Pim Edelaar) spruce (rainforests of the Pacific Northwest) for a fifth call Evo Edu Outreach (2010) 3:47–53 49 a time foraging on Sitka spruce, it also has a palate structure that matched what I had predicted over 15 years ago! Cone Variation, Red Squirrels, and Crossbills As I read the literature on conifers, I began to appreciate the extent of geographic variation in the structure of cones. If crossbills evolved to exploit different conifers, then what were the conifers and their cones evolving in response to? b Geographic variation in cone structure was particularly interesting in Rocky Mountain lodgepole pine. Its cones were fairly uniform in size throughout the Rocky Mountains from the Yukon to Colorado, but much smaller than those in the isolated Cypress Hills (Wheeler and Guries 1982)nearly 300 kilometers east of the Rocky Mountains along the border of Alberta and Saskatchewan (Fig. 4a). This was especially intriguing because several years earlier, W. Earl Godfrey, the author of The Birds of Canada, had encouraged me to visit the Cypress Hills. In the late 1930s and early 1940s, Red Crossbills were common there, and they had large bills (Fig. 4a;Godfrey1950). Moreover, red squirrels Fig. 3 An optimum is usually a function that is minimized or (Tamiasciurus hudsonicus), widespread throughout the maximized given constraints. In the case of crossbills, the optimal bill Rocky Mountains, were absent from the Cypress Hills. The depth is the bill depth that minimizes the time necessary to meet daily latter observation was significant, because in our conversa- energy demands. Individuals that can meet their energy requirements more rapidly will have a competitive advantage when food is scarce, tion, I had told Godfrey of my ideas of how the absence of minimizing the risk of starvation and allowing them to do other things red squirrels from Newfoundland was critical to the like find and court a mate. First, we need to consider the relationship evolution of a massive-billed crossbill on Newfoundland between bill depth and time needed to remove seeds from the cones. (Fig. 4b;Benkman1989). An example is shown for 27 Red Crossbills timed foraging on Douglas-fir cones (Benkman 1993), where the bill depth minimizing Nine thousand years ago, black spruce (Picea mariana) the time to extract a seed is approximately 9.4 millimeters (Fig.
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