Oecologia (2010) 162:71–80 DOI 10.1007/s00442-009-1424-8 PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER Diversity of floral visitors to sympatric Lithophragma species differing in floral morphology Mariana Cuautle Æ John N. Thompson Received: 30 March 2009 / Accepted: 14 July 2009 / Published online: 11 August 2009 Ó The Author(s) 2009. This article is published with open access at Springerlink.com Abstract Most coevolving relationships between pairs of were low, and the asymptotic number of visitor species was species are embedded in a broader multispecific interaction less than 20 species in all populations. Lithophragma network. The mutualistic interaction between Litho- species shared some of the visitors, with visitor assem- phragma parviflorum (Saxifragaceae) and its pollinating blages differing between sites more for L. heterophyllum floral parasite Greya politella (Lepidoptera, Prodoxidae) than for L. parviflorum. Pollination efficacy experiments occurs in some communities as a pairwise set apart from showed that most visitors were poor pollinators. Single most other interactions in those communities. In other visits to flowers by this assemblage of species resulted in communities, however, this pair of species occurs with significantly higher seed set in Lithophragma heterophyl- congeners and with other floral visitors to Lithophragma. lum (30.6 ± 3.9 SE) than in L. parviflorum (4.7 ± 3.4 SE). We analyzed local and geographic differences in the net- This difference was consistent between sites, suggesting work formed by interactions between Lithophragma plants that these visitors provide a better fit to the floral mor- and Greya moths in communities containing two Litho- phology of L. heterophyllum. Overall, none of the non- phragma species, two Greya species, and floral visitors Greya visitors appears to be either sufficiently common or other than Greya that visit Lithophragma flowers. Our goal efficient as a pollinator to impose strong selection on any of was to evaluate if non-Greya visitors were common, if these four Lithophragma populations in comparison with visitor assembly differs between Lithophragma species and Greya, which occurs within almost all populations of these populations and if these visitors act as effective pollinators. species throughout their geographic ranges. Sympatric populations of L. heterophyllum and L. parvi- florum differ in floral traits that may affect assemblies of Keywords California Á Geographic variation Á Greya Á floral visitors. Visitation rates by non-Greya floral visitors Pollinator efficacy Á Interaction network Communicated by Jeff Karron. Introduction M. Cuautle (&) Á J. N. Thompson Department of Ecology and Evolutionary Biology, As evidence of coevolution has accumulated, it has become University of California, A316 Earth and Marine clear that most coevolving relationships between pairs of Sciences Building, Santa Cruz, CA 95064, USA species are shaped by interactions with yet other taxa. Even e-mail: [email protected]; [email protected] the most commonly cited examples of extreme coevolution between pairs of species are known to be molded by a J. N. Thompson e-mail: [email protected] broader network of interactions. Examples include nematodes that attack pollinating fig wasps (Herre 1993), Present Address: co-pollinators that alter one-to-one mutualism between M. Cuautle particular pollinators and plants (Thompson and Cunningham Departamento de Ciencias Quı´mico-Biolo´gicas, Universidad de las Ame´ricas-Puebla, Cholula, 2002), and squirrels that can locally disrupt coevolution Puebla 72820, Mexico between lodgepole pines and crossbills (Benkman et al. 123 72 Oecologia (2010) 162:71–80 2001). The effect of other species on pairwise interactions often varies among populations, creating the potential for a multispecific geographic mosaic of coevolution in many interactions (Thompson 1994, 2005). In some interactions, such as pollination mutualisms, these geographically varying networks of species develop through a combination of diversification of closely related taxa and convergence of traits of unrelated species (e.g., ‘‘pollination syndromes’’). In fact, recent analyses of pollination and other mutualistic networks have shown that Fig. 1 Photographs of a Lithophragma parviflorum and b Litho- such mutualisms among free-living species often result in phragma heterophyllum, showing differences in floral morphology between species. In both species floral length from the top of the much less compartmentalization than occurs in antagonis- sepals to the base of the ovary is approximately 6 mm tic interactions such as those between predators and prey (Bascompte et al. 2003; Jordano et al. 2003; Guimara˜es et al. 2006; Lewinsohn et al. 2006). There is, however, the moths and the plants ranges among habitats from always some compartmentalization in mutualistic net- mutualistic to commensalistic to antagonistic, depending works. Many of these networks include modules composed on the presence of co-pollinators. In parts of the Coast of a closely related group of species (e.g., two or more Ranges of California, the network structure of the inter- congeneric plant species) that interacts with another group action is more complex. Some ecosystems have two to of closely related species (e.g., two or more congeneric three co-occurring Lithophragma species that are visited by pollinator species). The number of species involved in Greya moths and occasionally by other floral-visiting taxa. these mutualistic modules often varies geographically, These co-occurring Lithophragma species are similar in ranging from a simple pairwise interaction in some com- many traits but differ in others, including the degree of munities to trios, quartets, or larger sets of interacting inferiority of the ovary within the flower, floral scent, and species in other communities. As these interactions con- width of the corolla opening (Fig. 1; Taylor 1965; Kuzoff tinue to diversify through speciation and secondary contact, et al. 1999). These differences in floral traits may con- they could either continue to coevolve as a tight mutualistic tribute to differential visitation by floral visitors and sub- network or change fundamentally in ways that allow sequent selection on the evolution of floral morphology. incorporation of other, unrelated species into the We assessed visitation patterns to Lithophragma species interaction. in two widely separated communities where L. hetero- Here, we evaluate if a pairwise pollination mutualism phyllum and L. parviflorum are sympatric. In both com- has diversified to incorporate unrelated species as the munities, Greya moths visit the flowers of both species and mutualistic pair has undergone speciation and then reas- then lay their eggs in the plant tissues. They spend much of sembled in local communities as small sets of coexisting their adult lives either nectaring, resting, or ovipositing on congeners. Specifically, we analyze local and geographic their hostplants. In the year of this study, 77–90% of differences in the floral visitor network formed by two L. parviflorum plants received Greya eggs and 16–21% species of woodland star, Lithophragma heterophyllum and of L. heterophyllum plants received eggs (K. Rich and L. parviflorum (Saxifragaceae), and their assemblages of J. N. Thompson, unpublished data). Our goal was to floral visitors. The two Lithophragma species differ in evaluate whether non-Greya floral visitors are also com- multiple floral traits, and they co-occur in communities that mon visitors to these plants, whether their visitation differ in overall floristic and faunistic composition, pro- patterns differ between the two Lithophragma species, viding an opportunity to evaluate how divergence in traits whether the patterns were similar in the two communities, and community context may have reshaped the role of and whether the most common of these visitors could act as co-pollinators in these interactions. effective pollinators as has been shown in some northern One of these species, L. parviflorum, has previously regions where only L. parviflorum occurs. been shown to have a strongly mutualistic relationship with a pollinating floral parasitic moth, Greya politella (Pro- doxidae), in some ecosystems in the North American Materials and methods Pacific Northwest where co-pollinators are uncommon and there are no co-occurring Lithophragma species that are Lithophragma (Saxifragaceae) is endemic to western North visited by Greya (Thompson and Pellmyr 1992; Pellmyr America, comprising seven to nine species (Taylor 1965; and Thompson 1996; Thompson and Cunningham 2002; Kuzoff et al. 1999). Lithophragma parviflorum, which is Thompson and Fernandez 2006). The interaction between the most derived species within the genus (Kuzoff et al. 123 Oecologia (2010) 162:71–80 73 1999), has the widest geographic distribution and encom- underground bulbils. The plants remain in this vegetative passes the ranges of most of the other Lithophragma state until the spring, when they flower again. species. It occurs in steppe, grasslands, savannas, and In both Lithophragma species, individual flowers remain woodlands from southern British Columbia to California open for only a few days. Unpollinated flowers soon wither and eastward into the Rocky Mountains. Several subspe- as the plant produces new flowers higher up on the floral cies have been recognized and these have sometimes been scape. considered as separated species, but molecular studies (Kuzoff et al. 1999) and crossing studies (S. Dwiggins and Study sites