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Direct and Indirect Effects of Serpentine Soil on Florivores and Pollinators

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Direct and Indirect Effects of Serpentine Soil on Florivores and Pollinators Oecologia (2013) 173:1355–1366 DOI 10.1007/s00442-013-2711-y PLANT-MICROBE-ANIMAL INTERACTIONS - ORIGINAL RESEARCH Edaphic factors and plant–insect interactions: direct and indirect effects of serpentine soil on florivores and pollinators George A. Meindl · Daniel J. Bain · Tia‑Lynn Ashman Received: 31 January 2013 / Accepted: 6 June 2013 / Published online: 10 July 2013 © Springer-Verlag Berlin Heidelberg 2013 Abstract Edaphic factors can lead to differences in plant florivores relative to non-serpentine plants. In experimental morphology and tissue chemistry. However, whether these arrays, soil environment did not influence pollinator visita- differences result in altered plant–insect interactions for tion (though larger flowers were visited more frequently), soil-generalist plants is less understood. We present evi- but did alter florivore damage, with serpentine-grown plants dence that soil chemistry can alter plant–insect interactions receiving less damage. Our results demonstrate that the soil both directly, through chemical composition of plant tissue, environment can directly and indirectly affect plant–mutu- and indirectly, through plant morphology, for serpentine- alist and plant–antagonist interactions of serpentine-toler- tolerant Mimulus guttatus (Phrymaceae). First, we scored ant plants by altering flower chemistry and floral display. floral display (corolla width, number of open flowers per inflorescence, and inflorescence height), flower chemistry, Keywords Serpentine · Soil chemistry · Pollination · pollinator visitation and florivory of M. guttatus growing Florivory on natural serpentine and non-serpentine soil over 2 years. Second, we conducted a common garden reciprocal soil transplant experiment to isolate the effect of serpentine soil Introduction on floral display traits and flower chemistry.A nd last, we observed arrays of field-collected inflorescences and pot- Biotic interactions can be influenced by abiotic factors, thus ted plants to determine the effect of soil environment in the identical communities found in disparate environments (i.e., field on pollinator visitation and florivore damage, respec- with different resource availability) may differ in both the tively. For both natural and experimental plants, serpentine strength (Breitburg et al. 1997; Alonso 1999; Chalcraft and soil caused reductions in floral display and directly altered Andrews 1999) and direction (Pugnaire and Luque 2001) of flower tissue chemistry. Plants in natural serpentine popu- interactions. Abiotic conditions have been documented to lations received fewer pollinator visits and less damage by alter biotic interactions across a broad range of organisms, including effects of temperature and moisture on insect (Park 1954) and bivalve competition (Connell 1961). Plants, Communicated by Christina Caruso. in particular, are heavily dependent upon their abiotic envi- Electronic supplementary material The online version of this ronment for inorganic nutrient acquisition, and as a conse- article (doi:10.1007/s00442-013-2711-y) contains supplementary quence may be particularly susceptible to abiotic-mediated material, which is available to authorized users. variation (Klanderud and Totland 2005) in morphology and plant tissue chemistry, which in turn may affect how G. A. Meindl (*) · T.-L. Ashman Department of Biological Sciences, University of Pittsburgh, they interact with animals. Chemical and physical aspects Pittsburgh, PA 15260, USA of soils are extremely variable and this variation can alter e-mail: [email protected] both plant morphology and tissue chemistry (e.g., Cunning- ham et al. 1999; Murren et al. 2006; Burnett et al. 2008). D. J. Bain Department of Geology and Planetary Science, University For plants that occur in a variety of soil types, it is unclear of Pittsburgh, Pittsburgh, PA 15260, USA whether interactions with mutualists (e.g., pollinators) or 1 3 1356 Oecologia (2013) 173:1355–1366 antagonists (e.g., herbivores) are affected by soil context, interactions have only begun to be explored (Quinn et al. and whether soil could modify these interactions via direct 2011). Moreover, serpentine soils may generally influence effects on plant chemistry or indirect effects on morphol- plant–animal interactions (i.e., for non-hyperaccumulating ogy. However, such modification of biotic interactions could plants) through changes in tissue chemistry, as concentra- be instrumental in varying patterns of coevolution (i.e., the tions of metals in plant tissues far below hyperaccumulator geographic mosaic of coevolution; Thompson 1999). thresholds have been shown to be toxic to herbivores (Cole- The soil environment can influence plant reproductive man et al. 2005). In addition, while studies of folivory are morphology, which can in turn affect both plant–florivore important, an understanding of how flower chemistry alters and plant–pollinator interactions. Macronutrients in the florivory is needed, as many insects supplement their diets soil, such as N, P, K, Ca, and Mg, have been shown to influ- with nutrient-rich flower tissue (Held and Potter 2004). In ence flower size and number (e.g., Nagy and Proctor 1997; fact, some studies suggest that florivory can be just as com- Murren et al. 2006; Burnett et al. 2008). In addition, toxic mon as leaf herbivory in natural populations (e.g., Zangerl elements, such as heavy metals, often result in stunting and Rutledge 1996; Wolfe 2002), with potentially negative of growth when present in high concentrations in the soil implications for plant reproductive success (Mothershead (Antonovics et al. 1971) and are also known to influence and Marquis 2000). Florivores can affect male and female flower size (Hladun et al. 2011) and flower number (Sai- fitness both directly, through consumption of gamete- kkonen et al. 1998). Soil-induced changes in floral mor- housing structures, and indirectly by altering floral traits phology can have consequences for plant reproduction, as important for biotic interactions (e.g., pollinator attraction; both pollinators (Mitchell et al. 2004; Ivey and Carr 2005) reviewed in McCall and Irwin 2006). Therefore, under- and herbivores (Juenger et al. 2005; Ashman and Penet standing how the soil environment alters plant–florivore 2007) generally favor plants with large floral displays.A s a interactions may be vital towards explaining plant adapta- result, soil chemistry may mediate the quantity and quality tion to unique soils. of plant interactions with florivores and pollinators. Many Serpentine soil is distinct from adjacent soils by having studies have documented the effects of environment on low Ca:Mg ratios, mineral nutrient deficiencies (e.g., P, K), plant reproductive morphology, yet few (e.g., Galen 2000; and relatively high concentrations of several metals (Co, Lau et al. 2008) have determined whether these morpho- Cr, Ni, Fe, Mg, and Zn; Brady et al. 2005; Safford et al. logical changes lead to altered plant–animal interactions 2005; Table S1). These soils provide an ideal model system across different environments. to test whether the soil environment alters plant–florivore Soil chemistry can also have effects on plant tissue and plant–pollinator interactions as they are (1) globally chemistry (Cunningham et al. 1999), although the conse- distributed, (2) host many species of tolerant plants, and quences for plant–animal interactions are less well under- (3) are chemically distinct from adjacent soil types (Brady stood. While plant–herbivore interactions are often studied et al. 2005; Harrison and Rajakaruna 2011). We address in the context of plant secondary compounds (reviewed in whether biotic interactions are soil-dependent by answering Mithöfer and Boland 2012), recent studies suggest that pri- the following questions with respect to a serpentine-toler- mary metabolites (e.g., N, P, K) may also greatly influence ant species, Mimulus guttatus: (1) Does growth on serpen- both herbivore preference (Alonso and Herrera 2003) and tine soil alter traits that mediate plant–animal interactions, fitness (Beanland et al. 2003; Perkins et al. 2004). In addi- i.e., flower size, flower number, and inflorescence height? tion, soils that contain toxic elements can alter plant–herbi- (2) Does serpentine soil directly influence floral chemistry, vore interactions. For instance, Streptanthus polygaloides, a specifically for minerals known to be enriched or deficient serpentine soil endemic, hyperaccumulates Ni (i.e., tissues in serpentine and/or known to influence plant–animal inter- >1,000 ppm Ni; Baker and Brooks 1989), which results actions (macronutrients: Ca, Mg, P, K; micronutrients: Fe, in less leaf damage by herbivores (Boyd and Moar 1999) Ni, Zn, B; or other beneficial nutrients:A l, Na; Marschner and pathogens (Boyd et al. 1994). The effect of metal 1986)? And (3) is (a) pollinator visitation rate, (b) pollina- accumulation on plant–pollinator interactions, however, tor diversity, and/or (c) florivore damage lower for plants is unclear. For example, interactions with pollinators may growing in serpentine versus non-serpentine soils? also be affected if metals are translocated to floral tissues and pollinator rewards (e.g., nectar and pollen). A recent study of a non-metal (Se) hyperaccumulator has shown Materials and methods that flower constituents, including nectar, can accumulate non-essential elements in high concentrations (Hladun Study system et al. 2011), though metal accumulators from serpentines have not been similarly studied, and the implications
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