Different Responses of Congeneric Consumers to an Exotic Food Resource: Who Gets the Novel Resource Prize?
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Biol Invasions (2014) 16:1757–1767 DOI 10.1007/s10530-013-0625-6 ORIGINAL PAPER Different responses of congeneric consumers to an exotic food resource: who gets the novel resource prize? Yvette K. Ortega • Leigh F. Greenwood • Ragan M. Callaway • Dean E. Pearson Received: 12 April 2013 / Accepted: 16 December 2013 / Published online: 22 December 2013 Ó Springer Science+Business Media Dordrecht(outside the USA) 2013 Abstract Exotic species can provide abundant food congeners did, particularly when foraging away from resources for native consumers, but predicting which cover. Via this hovering technique, birds were able to native species will respond positively remains a chal- gather knapweed seedheads from erect plants rather lenge. We studied the foraging behavior of black- than searching for seedheads on the ground. These shifts capped (Poecile atricapillus) and mountain (P. gambeli) in foraging behavior allowed black-capped chickadees chickadees in western Montana to compare the degree to to exploit Urophora larvae to a much greater degree than which these congeric and syntopic consumers exploited their congeners while minimizing exposure to a high- larvae of Urophora, an exotic biological control insect risk habitat, an outcome with potentially important living within the seedheads of the invasive forb, spotted community-wide consequences. Behavioral flexibility knapweed (Centaurea stoebe). Chickadees typically has been used to predict the success of invading species. forage within tree or shrub cover, whereas knapweed We suggest that behavioral flexibility may also be used and hence Urophora larvae thrive in open grassland to predict how native species will respond to invasions, away from cover. We found that black-capped chick- particularly the availability of exotic food resources. adees were much more likely than mountain chickadees to forage for Urophora. Black-capped chickadees Keywords Behavioral plasticity Á Biological strategically minimized time spent in open habitats by control agent Á Food subsidy Á Foraging behavior Á flying out from cover to retrieve knapweed seedheads Urophora and immediately returning to cover to extract the larvae. Black-capped chickadees also employed an atypical hovering technique nearly twice as often as their Introduction Y. K. Ortega (&) Á D. E. Pearson Exotic species can have strong negative effects on Rocky Mountain Research Station, USDA Forest Service, native species through competition, consumption, and 800 E. Beckwith Ave., Missoula, MT 59801, USA parasitism (Levine et al. 2003; Salo et al. 2007; Pysek e-mail: [email protected] et al. 2012), but less appreciated is the fact that such L. F. Greenwood Á D. E. Pearson invaders can also have strong positive effects on native Division of Biological Sciences, University of Montana, species (Rodriguez 2006). Notably, exotic organisms Missoula, MT 59812, USA can provide novel food resources for native consumers (Barber et al. 2008; McCusker et al. 2010; Tablado R. M. Callaway Division of Biological Sciences, Institute on Ecosystems, et al. 2010). Moreover, because exotic organisms often University of Montana, Missoula, MT 59812, USA become highly abundant, they can provide enormous 123 1758 Y. K. Ortega et al. subsidies for native consumers and potentially trigger Whether exotic or native, behavioral flexibility may community-wide effects (Roemer et al. 2002; Noon- confer advantages on organisms faced with novel burg and Byers 2005; Pearson and Callaway 2003). To conditions (Greenberg 1990; Sih et al. 2010, 2011). better understand the net effects of biological inva- Hence, understanding such flexibility may help to sions on native communities, we need to address the predict which native species will successfully exploit full range of native species responses to invaders, from exotic resources and which will not. negative to neutral and positive. One notable exotic resource in western North Many studies have documented consumption of America is supplied by the gall flies Urophora affinis exotic food resources by native species (Rodriguez and U. quadrifasciata, which were introduced for the 2006), but predicting which native species will success- biological control of the Eurasian forb spotted knap- fully exploit such resources remains a challenge (Sih weed (Centaurea stoebe) in the 1970s (Story et al. et al. 2010). Few studies have compared the responses of 1987). These flies oviposit in knapweed seedheads, and multiple native consumers to exotic food resources, and their larvae overwinter in galls and feed on their host fewer still have examined the mechanisms that underlie plant’s tissues (Story et al. 1987). Because Urophora the variation in native species responses (e.g., Waring successfully established but failed to reduce popula- et al. 1993;Schummeretal.2008; Tablado et al. 2010). tions of their very abundant host, they occur at Morphology and physiology determine whether or not a extremely high densities (Story et al. 1995). Further- native organism has the capacity to respond to a novel more, Urophora larvae serve as a winter food subsidy resource. However, given the physical capacity, behav- that can double or triple native deer mouse (Peromys- ior can provide the flexibility that may be necessary to cus maniculatus) populations (Ortega et al. 2004; exploit such novelty (e.g., Greenberg 1990; Lefebvre Pearson and Fletcher 2008), leading to a variety of et al. 1997). Hence, this flexibility may be key to complex indirect food-web effects (Pearson and Call- understanding much of the variation in native species away 2003, 2006, 2008). Native songbirds may be responses to exotic food resources (Sih et al. 2010, similarly affected. Several songbird species consume 2011). Comparative studies of closely related consum- Urophora larvae during winter (Story et al. 1995; ers exhibiting differing responses to exotic food Pearson et al. 2000), and food availability can have resources would provide insight into how behavior strong effects on songbird populations by influencing influences such variation. overwinter survival (Brittingham and Temple 1988; A number of studies have documented the impor- Desrochers et al. 1988; Mccallum et al. 1999) and the tance of behavioral flexibility and associated behav- onset of breeding (Boutin 1990; Marshall et al. 2002; ioral traits in mediating the success of invasive species Ortega et al. 2006). Thus, Urophora has great potential in new ranges (Holway and Suarez 1999; Sol et al. to provide a critical resource for some native bird 2008; Pintor et al. 2009). However, the role that these species. However, we have not examined how utiliza- behavioral attributes have in determining the response tion of this exotic resource varies among taxa, or the of native species to invasions has received relatively role behavioral flexibility might play in this variation. little attention. This information gap likely arises from In western Montana, black-capped chickadees an emphasis on the negative impacts that invaders (Poecile atricapillus) prey heavily on Urophora larvae have on native species (Rodriguez 2006). Yet, if in the winter (Story et al. 1995). This native songbird behavioral flexibility allows some invaders to thrive in typically forages for arthropods, seeds, and fruit within the novel conditions of a new range, it may also allow the cover of trees (Hill and Lein 1988; Foote et al. some natives to thrive in the novel conditions created 2010). However, knapweed and hence Urophora by species invasions. Avian species vary greatly in the larvae are much more abundant in open grassland flexibility of their foraging behavior (Greenberg 1990; away from the cover of trees (Metlen et al. 2012), Lefebvre et al. 1997), and associated traits such as forcing the birds to venture into open microhabitats to neophobia (avoidance of novel objects or situations) exploit the exotic food source (Story et al. 1995). and innovation propensity (solving novel food prob- Mountain chickadees (Poecile gambeli) generally lems) correlate with the success of species introduced breed at higher elevations than black-capped chicka- into new ranges and ecosystems (Sol et al. 2002, dees, but some overwinter with their congeners in 2005a; Martin and Fitzgerald 2005; Møller 2009). mixed-species flocks within low-elevation woodlands 123 Novel resource prize 1759 typically invaded by knapweed. Mountain chickadees (elevation 945 m, 46°50008.1900N 114°5058.20W, have been observed consuming Urophora larvae but 46°49052.02N 114°5052.68W) were dominated by seemingly take less advantage of this novel resource ponderosa pine (Pinus ponderosa), while the third than black-capped chickadees (L. Greenwood, pers. site in Marshall Canyon 10 km northwest of Missoula obs.). Mountain chickadees are the closest relative of was a dry upland habitat (elevation 1,220 m, black-capped chickadees, and these species are very 46°54021.5600N 113°55028.12W) consisting primarily similar in morphology and physiology (Mccallum of ponderosa pine and Douglas-fir (Pseudotsuga et al. 1999; Foote et al. 2010). Like black-capped menziesii). Forest cover was intermixed with the chickadees, mountain chickadees tend to forage for native shrubs red-osier dogwood (Cornus stolonifera) arthropods and seeds within tree cover (Hill and Lein and ninebark (Physocarpus malvaceus). Open areas 1988; Mccallum et al. 1999). Therefore, like their contained native grassland species including blue- congeners, mountain chickadees would have to leave bunch wheatgrass (Psuedoroegnaria spicata), Idaho their typical