Jonah Piovia-Scott

Preventing horticultural introductions of invasive plants: potential efficacy of voluntary initiatives

Although prevention is the most cost-effective way to avoid the enormous expenses associated with plant invasions, invasive plants continue to be imported as trade commodities for horticultural use. With very little government regulation of horticultural imports of invasive plants, efforts have turned toward fostering voluntary initiatives to encourage self-regulation by the horticulture trade. Our study takes the first step toward evaluating the potential success of these voluntary initiatives. We conducted a survey of nursery professionals to gauge their perceptions of invasive species, the role of the horticulture trade in invasive plant introductions, and their participation—potential and actual—in preventive measures outlined in the St Louis Voluntary Codes of Conduct for nursery professionals. We found nursery professionals to be highly aware of invasive plants and to accept responsibility as a trade for horticultural introductions. Although only 7% of respondents had heard of the St Louis Voluntary Codes of Conduct, the majority (57%) reported having participated in at least two of seven preventive measures, and most (78%) reported willingness to engage in the majority of preventive measures. We found that several factors significantly predict increased participation in preventive measures, particularly awareness of invasive plants and involvement in trade associations. We also identified incentives and obstacles to participating in preventive behaviors, including “concern for the environment” and “lack of information,” respectively. Our results suggest that participation in voluntary initiatives will improve through increased outreach, and we provide specific recommendations for improving participation in voluntary programs in the horticulture trade.

Tackling aquatic invasions: risks and opportunities for the aquarium fish industry

The aquarium trade is an important and rapidly growing vector for introduced species in the United States. We examined this vector by surveying pet stores in the San Francisco Bay–Delta region to compile a list of aquarium fish species commonly stocked. We identified which of these species might be able to survive in the Bay–Delta, and investigated store representatives’ knowledge and attitudes about biological invasions. A restrictive analysis using conservative estimates of fish temperature tolerances and environmental conditions found that the local aquarium trade includes 5 fish species that can survive in a temperate system such as the Bay–Delta. Under more inclusive parameters, up to 27 fish species met the criteria for survival in the Bay–Delta. We further explored these results by comparing potential invader incidence between different types of stores. In the more restrictive analysis, three national retail chains stocked significantly more potentially invasive species than independent aquarium stores, but there was no difference in the more inclusive analysis. A significantly higher percentage of fish taxa were easily identifiable and well-labeled in chain stores than in independent stores. Most aquarium store representatives indicated willingness to take action to reduce the threat of trade-related introductions, although chain store employees were more willing to assign responsibility for reducing this threat to the aquarium industry than were independent store employees. Management efforts for this vector should focus on (a) improving labeling and identification of fish species in stores, (b) expanding the often spotty data on fish physiological tolerances, especially for saltwater species, (c) educating customers and store employees about the risks posed by pet release, and (d) providing better options for responsible disposal of unwanted fish.

Correlates of virulence in a frog-killing fungal pathogen: evidence from a California amphibian decline

The fungal pathogen Batrachochytrium dendrobatidis (Bd) has caused declines and extinctions in amphibians worldwide, and there is increasing evidence that some strains of this pathogen are more virulent than others. While a number of putative virulence factors have been identified, few studies link these factors to specific epizootic events. We documented a dramatic decline in juvenile frogs in a Bd-infected population of Cascades frogs (Rana cascadae) in the mountains of northern California and used a laboratory experiment to show that Bd isolated in the midst of this decline induced higher mortality than Bd isolated from a more stable population of the same species of frog. This highly virulent Bd isolate was more toxic to immune cells and attained higher density in liquid culture than comparable isolates. Genomic analyses revealed that this isolate is nested within the global panzootic lineage and exhibited unusual genomic patterns, including increased copy numbers of many chromosomal segments. This study integrates data from multiple sources to suggest specific phenotypic and genomic characteristics of the pathogen that may be linked to disease-related declines.

Effects of Experimental Seaweed Deposition on Lizard and Ant Predation in an Island Food Web

In a simple island ecosystem, a rare pulse of resource input alters the interaction between predator species. The effect of environmental change on ecosystems is mediated by species interactions. Environmental change may remove or add species and shift life-history events, altering which species interact at a given time. However, environmental change may also reconfigure multispecies interactions when both species composition and phenology remain intact. In a Caribbean island system, a major manifestation of environmental change is seaweed deposition, which has been linked to eutrophication, overfishing, and hurricanes. Here, we show in a whole-island field experiment that without seaweed two predators—lizards and ants—had a substantially greater-than-additive effect on herbivory. When seaweed was added to mimic deposition by hurricanes, no interactive predator effect occurred. Thus environmental change can substantially restructure food-web interactions, complicating efforts to predict anthropogenic changes in ecosystem processes.

Bacterial flora on Cascades frogs in the Klamath mountains of California

Amphibians are experiencing global declines due in part to the infectious disease chytridiomycosis. Some symbiotic bacteria residents on frog skin have been shown to inhibit the growth of Batrachochytrium dendrobatitis (Bd) but few studies have attempted to fully describe the resident bacterial flora of frog skin. We cultured and sequenced 130 bacterial isolates from frogs collected from the California Klamath Range, recovering predominantly Gram-negative bacteria from 20 higher order taxa and 31 genera. There were also a large number of unclassifiable isolates. Forty-three isolates were assessed for their ability to inhibit the growth of Bd in vitro; of these, two had strong and three had slight anti-Bd activity. We suggest that many bacterial species may play a secondary role in Bd resistance, acting synergistically with inhibitory species. Future research is required in order to characterize these interactions. Understanding the relationships between bacterial strains may be important in predicting and managing the effects of future anti-Bd treatments such as antimicrobial compounds or probiotic bacteria.

The effect of disturbance on an ant-plant mutualism.

Protective ant–plant mutualisms—where plants provide food or shelter to ants and ants protect the plants from herbivores—are a common feature in many ecological communities, but few studies have examined the effect of disturbance on these interactions. Disturbance may affect the relationship between plants and their associated ant mutualists by increasing the plants’ susceptibility to herbivores, changing the amount of reward provided for the ants, and altering the abundance of ants and other predators. Pruning was used to simulate the damage to buttonwood mangrove (Conocarpus erectus) caused by hurricanes. Pruned plants grew faster than unpruned plants, produced lower levels of physical anti-herbivore defenses (trichomes, toughness), and higher levels of chemical defenses (tannins) and extrafloral nectaries. Thus, simulated hurricane damage increased plant growth and the amount of reward provided to ant mutualists, but did not have consistent effects on other anti-herbivore defenses. Both herbivores and ants increased in abundance on pruned plants, indicating that the effects of simulated hurricane damage on plant traits were propagated to higher trophic levels. Ant-exclusion led to higher leaf damage on both pruned and upruned plants. The effect of ant-exclusion did not differ between pruned and unpruned plants, despite the fact that pruned plants had higher ant and herbivore densities, produced more extrafloral nectaries, and had fewer physical defenses. Another common predator, clubionid spiders, increased in abundance on pruned plants from which ants had been excluded. I suggest that compensatory predation by these spiders diminished the effect of ant-exclusion on pruned plants.

Lizards on newly created islands independently and rapidly adapt in morphology and diet

Significance We report for island populations of the termite-eating common gecko species Gymnodactylus amarali rapid parallel morphological and ecological change in response to human-caused environmental disturbance. The islands were formerly part of an extensive terrestrial ecosystem; in 1997, the area was flooded to construct a reservoir, fragmenting the higher portions into separate islands. Populations on all five islands studied have proportionally larger heads than populations at five nearby mainland sites. The new island morphology is accompanied by an increase in dietary niche breadth, mainly via expansion toward larger prey. This expansion is likely due to the greater availability of such prey on the newly formed islands after the extinction there of four larger lizard species that typically also included termites in their diets. Rapid adaptive changes can result from the drastic alterations humans impose on ecosystems. For example, flooding large areas for hydroelectric dams converts mountaintops into islands and leaves surviving populations in a new environment. We report differences in morphology and diet of the termite-eating gecko Gymnodactylus amarali between five such newly created islands and five nearby mainland sites located in the Brazilian Cerrado, a biodiversity hotspot. Mean prey size and dietary prey-size breadth were larger on islands than mainlands, expected because four larger lizard species that also consume termites, but presumably prefer larger prey, went extinct on the islands. In addition, island populations had larger heads relative to their body length than mainland populations; larger heads are more suited to the larger prey taken, and disproportionately larger heads allow that functional advantage without an increase in energetic requirements resulting from larger body size. Parallel morphological evolution is strongly suggested, because there are indications that, before flooding, relative head size did not differ between future island and future mainland sites. Females and males showed the same trend of relatively larger heads on islands, so the difference between island and mainland sites is unlikely to be due to greater male–male competition for mates on islands. We thus discovered a very fast (at most 15 y) case of independent parallel adaptive change in response to catastrophic human disturbance.

Itraconazole treatment reduces Batrachochytrium dendrobatidis prevalence and increases overwinter field survival in juvenile Cascades frogs.

The global spread of the fungal pathogen Batrachochytrium dendrobatidis (Bd) has led to widespread extirpation of amphibian populations. During an intervention aimed at stabilizing at-risk populations, we treated wild-caught Cascades frogs Rana cascadae with the antifungal drug itraconazole. In fall 2012, we collected 60 recently metamorphosed R. cascadae from 1 of the 11 remnant populations in the Cascades Mountains (CA, USA). Of these, 30 randomly selected frogs were treated with itraconazole and the other 30 frogs served as experimental controls; all were released at the capture site. Bd prevalence was low at the time of treatment and did not differ between treated frogs and controls immediately following treatment. Following release, Bd prevalence gradually increased in controls but not in treated frogs, with noticeable (but still non-significant) differences 3 wk after treatment (27% [4/15] vs. 0% [0/13]) and strong differences 5 wk after treatment (67% [8/12] vs. 13% [1/8]). We did not detect any differences in Bd prevalence and load between experimental controls and untreated wild frogs during this time period. In spring 2013, we recaptured 7 treated frogs but none of the experimental control frogs, suggesting that over-winter survival was higher for treated frogs. The itraconazole treatment did appear to reduce growth rates: treated frogs weighed 22% less than control frogs 3 wk after treatment (0.7 vs. 0.9 g) and were 9% shorter than control frogs 5 wk after treatment (18.4 vs. 20.2 mm). However, for critically small populations, increased survival of the most at-risk life stage could prevent or delay extinction. Our results show that itraconazole treatment can be effective against Bd infection in wild amphibians, and therefore the beneficial effects on survivorship may outweigh the detrimental effects on growth.

The effect of chronic seaweed subsidies on herbivory: plant-mediated fertilization pathway overshadows lizard-mediated predator pathways

Flows of energy and materials link ecosystems worldwide and have important consequences for the structure of ecological communities. While these resource subsidies typically enter recipient food webs through multiple channels, most previous studies focussed on a single pathway of resource input. We used path analysis to evaluate multiple pathways connecting chronic marine resource inputs (in the form of seaweed deposits) and herbivory in a shoreline terrestrial ecosystem. We found statistical support for a fertilization effect (seaweed increased foliar nitrogen content, leading to greater herbivory) and a lizard numerical response effect (seaweed increased lizard densities, leading to reduced herbivory), but not for a lizard diet-shift effect (seaweed increased the proportion of marine-derived prey in lizard diets, but lizard diet was not strongly associated with herbivory). Greater seaweed abundance was associated with greater herbivory, and the fertilization effect was larger than the combined lizard effects. Thus, the bottom-up, plant-mediated effect of fertilization on herbivory overshadowed the top-down effects of lizard predators. These results, from unmanipulated shoreline plots with persistent differences in chronic seaweed deposition, differ from those of a previous experimental study of the short-term effects of a pulse of seaweed deposition: while the increase in herbivory in response to chronic seaweed deposition was due to the fertilization effect, the short-term increase in herbivory in response to a pulse of seaweed deposition was due to the lizard diet-shift effect. This contrast highlights the importance of the temporal pattern of resource inputs in determining the mechanism of community response to resource subsidies.

Recent Emergence of a Chytrid Fungal Pathogen in California Cascades Frogs (Rana cascadae)

The pathogenic fungus Batrachochytrium dendrobatidis (Bd) has been associated with global amphibian declines, but it is often difficult to discern the relative importance of Bd as a causal agent in declines that have already occurred. Retrospective analyses of museum specimens have allowed researchers to associate the timing of Bd arrival with the timing of past amphibian declines. Cascades frogs (Rana cascadae) have experienced dramatic declines in northern California, but it is not clear whether the onset of these declines corresponds to the arrival of Bd. We used quantitative real-time PCR assays of samples collected from museum specimens to determine historical Bd prevalence in the northern California range of Cascades frogs. We detected Bd in 13 of 364 (3.5%) Cascades frog specimens collected between 1907 and 2003, with the first positive result from 1978. A Bayesian analysis suggested that Bd arrived in the region between 1973 and 1978, which corresponds well with the first observations of declines in the 1980s.