Reduced herbivore resistance in introduced smooth cordgrass ( Spartina alterniflora ) after a century of herbivore-free growth

Abstract

We compared resistance to insect herbivory in two introduced populations of smooth cordgrass (Spartina alterniflora) differing in their history of herbivory. One population in Willapa Bay, Washington, has spread in the absence of herbivory for more than a century, while another population in San Francisco, California, was introduced 20 years ago and is fed upon by the Spartina-specialist planthopper, Prokelisia marginata. The planthopper is a sap-feeder common on the Atlantic and Gulf coasts of North America, where smooth cordgrass is native. Smooth cordgrass plants from Willapa Bay (WB), San Francisco Bay (SFB), and Maryland (the source of the SFB introduction) were exposed to P. marginata herbivory over two consecutive summers in a common greenhouse environment, and their growth was compared with that of control plants that were grown herbivore-free. The planthoppers had relatively little effect on the growth of SFB plants, with plants exposed to herbivores averaging 77% and 83% of the aboveground biomass of herbivore-free controls after the first and second season of herbivory, respectively. The growth of plants from Maryland was similarly little-affected by the planthoppers, with the plants exposed to herbivores averaging near 100% of the biomass of herbivore-free controls after two seasons. In contrast, the growth of the WB plants was greatly reduced by the planthopper, with the plants exposed to planthopper herbivory averaging only 30% and 12% of the aboveground biomass of herbivore-free controls after the first and second seasons of herbivory, respectively. By the end of the second season of herbivory, 37% of the WB plants exposed to herbivory had died, while none of the SFB plants exposed to herbivores had died. Among WB clones, there was variation in resistance; one WB clone suffered 0% mortality while another suffered 100% mortality when exposed to herbivores. Short-term herbivory experiments with the putative founder clone for the WB population suggested that the WB founder was similar to the more resistant WB clones in its susceptibility to planthopper herbivory. Nitrogen analyses of green leaf tissue indicated that WB plants, including the WB founder clone, averaged 70% more total leaf nitrogen than SFB and Maryland plants. In a planthopper choice experiment, more planthoppers were observed on WB plants than SFB plants after 95 days of exposure to herbivory. Planthopper preference for WB plants may have contributed to the lower resistance of WB plants to herbivory; however, even before planthoppers had become more abundant on the WB plants, the proportion of leaves with 50% or more dead tissue averaged significantly greater on the WB plants, suggesting a difference between populations in tolerance to herbivory as well. Multiple factors, including a founder effect, further loss of herbivore tolerance, and herbivore preference for WB plants, appear to account for the reduced planthopper resistance in the WB population.

Potential for Self‐defeating Biological Control? Variation in Herbivore Vulnerability Among Invasive Spartina Genotypes

“…The relative shoot survival of one genotype from San Francisco was Ͼ1, which would indicate that the planthopper somehow caused an increase in shoot survival of this genotype. We have observed other genotypes of S. alterniflora from Virginia to have higher biomass when supporting low densities of moderate densities of P. marginata (Daehler and Strong 1997;D. Garcia-Rossi, personal observation).…”

“…is Bodega Bay, California. S. alterniflora was introduced to Willapa Bay 900 km to the north ϳ100 years ago, without P. marginata or other specialized herbivores (Daehler and Strong 1997). Thus, the cordgrass populations in this study that have been long-separated from herbivory are S. anglica and S. alterniflora from Willapa Bay.…”

“…Prokelisia marginata were collected from San Francisco Bay (Daehler and Strong 1997). Mean greenhouse temperature during March-August was 23ЊC by day and 12ЊC by night.…”

Selection for chemical trait remixing in an invasive weed after reassociation with a coevolved specialist

“…Reassociation with a specialized coevolved enemy in an area of nonindigeneity is likely to have a profound and more predictable effect on host-plant chemistry. Although little quantitative and ecologically relevant information is available on phytochemical changes in plants that occur after introduction into a nonindigenous area and release from interactions with longtime insect associates (7)(8)(9)(10), even less information is available on phytochemical changes that ensue when coevolved enemies that are demonstrated reciprocal selective agents resume interacting with a host plant in an area of invasion. Such changes should be more predictable because the decoupling of defense and herbivory that has been observed in interactions between invasive plants and indigenous herbivores (11) is less likely to occur upon reassociation with a coevolved specialist.…”

Insect‐plant interactions on a planet of weeds

“…Plants from a population of Smooth cordgrass (Spartina alterniflora) at Willapa Bay, Washington had been free from herbivory by the plant hopper Prokelisia marginata for more than a century. In a greenhouse study these plants were found far more susceptible than those from two areas (San Francisco Bay and Maryland) where the insect and the plant coexist (Daehler & Strong, 1997). The low frequency of genotypes resistant to P. marginata herbivory in the Willapa Bay population encouraged investigators to release the plant hopper for biological control in Washington State.…”