Predicting Multi-trophic Consequences of an Emerging Disease

Author

Adam D. Chupp, Southern Illinois University CarbondaleFollow

Date of Award

5-1-2015

Degree Name

Doctor of Philosophy

Department

Plant Biology

First Advisor

Battaglia, Loretta

Abstract

There are numerous examples of how exotic insect pests and pathogens have altered the dominance of native tree species and the ecological processes and function related to those species. While targeted species may persist in a functionally altered state via vegetative sprouting, the widespread decimation of a species can have dramatic direct and indirect consequences for organisms in multiple trophic levels. Devastation due to alien insect herbivores poses the greatest threat to native insect larvae that specialize on the impacted host species. The loss of pollinators whose larvae feed on impacted species and provide services for native plants may also be a serious but yet undocumented indirect threat of these exotic invasions. The disruption of mutualistic relationships between native species will have negative consequences for those species and could potentially benefit exotic species. In the southeastern US, laurel wilt disease (LWD) is impacting numerous species in the Lauraceae family, with the majority of cases observed on Persea borbonia, a common sub-canopy tree found in many Coastal Plain habitats. This species is also known to be the primary larval host of the palamedes swallowtail (Papilio palamedes). While infection rates and crown dieback are catastrophically high (>90%), basal resprouting is a common response in P. borbonia. The exotic Cinnamomum camphora is the only Lauraceae species that has shown resistance to LWD and could benefit from opportunities to replace P. borbonia and other Lauraceae species threatened by LWD. The primary objectives of this study were four fold: 1) to quantify P. borbonia sprouting responses in the field and greenhouse and determine the effect of P. borbonia removal on the composition and abundance of woody and herbaceous plant species in the understory layer, 2) to test the relative suitability of C. camphora as an alternative larval host for P. palamedes, 3) to determine the reliance of the Platanthera ciliaris on P. palamedes for successful pollination and the relative availability of alternative long-tongued pollinators, and 4) to forecast how disease-induced shifts in the relative abundance of native (P. borbonia) and exotic (C. camphora) fruit may alter patterns of consumption and subsequent dispersal of C. camphora by birds. The field component (Grand Bay National Estuarine Research Reserve (GBNERR), Jackson County, MS) of chapter two involved the removal of P. borbonia main stems to mimic the impacts of LWD which resulted in a significant increase (~50%) in light transmission. All treated individuals produced sprouts and the size and number of sprouts was positively related to initial tree size. Following the removal of P. borbonia from treatment plots, Ilex vomitoria showed the greatest increase in basal area after two years. Both woody seedlings and herbaceous plants showed no significant trends in composition and/or abundance over time. In the greenhouse (Southern Illinois University, Carbondale, IL), the stem and leaf biomass of vegetative sprouts was significantly greater in a high-nutrient treatment. Light treatments had no effect on sprout production. Results from chapter two suggest that the loss of P. borbonia from the canopy layer may have little direct effect on plant community dynamics. In addition, I found that sprout production is vigorous in P. borbonia and the capacity to persist and tolerate future disturbances may be enhanced on more nutrient-rich sites. In chapter three, I used laboratory experiments and field observations to compare larval performance and adult female preference of P. palamedes between C. camphora and P. borbonia foliage. My results indicate moderate survivorship on C. camphora (46%) compared to P. borbonia (87%) and there were no differences in first and fourth instar growth rates between treatments. Fourth instars consumed less C. camphora foliage than P. borbonia, but metabolic efficiency did not differ between treatments. In the field and laboratory, I found no oviposition preference for C. camphora relative to P. borbonia. While females laid eggs on C. camphora during laboratory trials, the same number of eggs was also laid on inanimate objects. I conclude that C. camphora is suitable for larval development but host-switching to this species by P. palamedes will be primarily constrained by oviposition behaviors. In chapter four, I monitored pollinator visitation and measured nectar spur lengths of P. ciliaris flowers and proboscis lengths of its floral visitors (at GBNERR). Papilio palamedes was the primary visitor (44 visits) but Phoebis sennae was also observed (4 visits). There were no significant differences among P. ciliaris nectar spurlength and the proboscis lengths of P. palamedes and P. sennae. Fruit set was 55 ± 10.8% with access to pollinators and 0% on bagged inflorescences (pollinators excluded). Although I found a positive relationship between visitation and inflorescence size, there was no such pattern in fruit set, indicating that fruit set was not limited by pollinator visitation within the range of visitation rates I observed. Phoebis sennae may provide supplemental pollination service but is likely constrained by habitat preferences that do not always overlap with those of P. cilaris. Although additional observations are needed, my results suggest that expected LWD-induced declines of P. palamedes will threaten the reproductive success and persistence of P. ciliaris populations. In chapter five, I investigated redundancy between C. camphora and P. borbonia with respect to fruit characteristics (physical and chemical) and selectivity by frugivorous birds (at GBNERR). Across two winter survey periods I observed fruit removal from artificial infructescences. I manipulated background species upon which displays were hung (Myrica cerifera and Triadica sebifera) and the accessibility of the displays. Using motion-activated cameras I confirmed foraging bouts on both P. borbonia and C. camphora fruits by three bird species (Dumetella carolinensis, Turdus migratorius, and Catharus guttatus). There was no significant difference in selectivity between fruit types during year one of my surveys but there was a significant preference for C. camphora in year two, which coincided with significantly lower mean daily temperatures. Background tree species and accessibility had no apparent effect on fruit preference. Total polyphenols and pulp:seed ratio were significantly higher in C. camphora fruit. I conclude that the fruits of C. camphora and P. borbonia represent nearly substitutable resources for native birds. However, native species may prefer C. camphora fruit in times of energetic stress. The decline of P. borbonia will likely increase the consumption and dispersal of C. camphora fruits. Additional studies are required to determine if such changes could ultimately increase the distribution and abundance of this exotic species. Combined, the chapters of this dissertation present substantial empirical evidence for the potential multi-trophic level impacts of an exotic plant disease. While it remains unclear how dramatic these impacts will be, the approach used here is vital for understanding and mitigating the long-term ecological effects of species/disease invasions.