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Evaluation of ecological risk to populations of a threatened plant from an invasive biocontrol insect

Controversy exists over estimation of ecological risk in biological control. At present, the risk to the rare, federally listed Pitcher's thistle ( Cirsium pitcheri ) in North America from Rhinocyllus conicus , a biological control weevil now feeding on many native thistles, is unknown. We hypothesized that quantification of host specificity and potential phenological overlap between insect and plant would improve assessment of the magnitude of risk. In laboratory host specificity tests, we found no significant difference in R. conicus feeding or oviposition preference between the rare C. pitcheri and the targeted exotic weed ( Carduus nutans ) or between C. pitcheri and Platte thistle ( C. canescens ), a closely related native North American species known to be affected by R. conicus . In a garden environment, R. conicus spontaneously found, oviposited, and developed completely on C. pitcheri . Taller plants with more flower heads were significantly more vulnerable, suggesting that the greatest impact is likely to be on individuals that generally contribute the most to recruitment and population persistence. For eight sites in two national parks over three years, the calculated period of expected R. conicus activity overlapped 99% and 78% of the flower heads initiated by C. pitcheri in the southern and the northern park, respectively. A demographic model suggests that population growth rate (λ) of C. pitcheri will decrease from 0.9897 to 0.8686, while time to halve the population will decrease from 66.9 to 4.9 years, under the conservative assumption that oviposition by R. conicus on C. pitcheri will occur at the same rate as on the related C. canescens . Calculated decreases in λ and t 0.5 are larger if the rate of oviposition actually observed in the laboratory tests is used. These results indicate that the weevil poses a serious quantitative, demographic risk to the threatened C. pitcheri . The study supports the suggestion that ecological data can be used to improve the quantification of risk to native nontarget plant populations within the potential physiological host range of a biological control insect.

Ecological Applications

A habitat overlap analysis derived from maxent for tamarisk and the south-western willow flycatcher

Biologic control of the introduced and invasive, woody plant tamarisk ( Tamarix spp, saltcedar) in south-western states is controversial because it affects habitat of the federally endangered South-western Willow Flycatcher ( Empidonax traillii extimus ). These songbirds sometimes nest in tamarisk where floodplain-level invasion replaces native habitats. Biologic control, with the saltcedar leaf beetle ( Diorhabda elongate ), began along the Virgin River, Utah, in 2006, enhancing the need for comprehensive understanding of the tamarisk-flycatcher relationship. We used maximum entropy (Maxent) modeling to separately quantify the current extent of dense tamarisk habitat (>50% cover) and the potential extent of habitat available for E. traillii extimus within the studied watersheds. We used transformations of 2008 Landsat Thematic Mapper images and a digital elevation model as environmental input variables. Maxent models performed well for the flycatcher and tamarisk with Area Under the ROC Curve (AUC) values of 0.960 and 0.982, respectively. Classification of thresholds and comparison of the two Maxent outputs indicated moderate spatial overlap between predicted suitable habitat for E. traillii extimus and predicted locations with dense tamarisk stands, where flycatcher habitat will potentially change flycatcher habitats. Dense tamarisk habitat comprised 500 km 2 within the study area, of which 11.4% was also modeled as potential habitat for E. traillii extimus . Potential habitat modeled for the flycatcher constituted 190 km 2 , of which 30.7% also contained dense tamarisk habitat. Results showed that both native vegetation and dense tamarisk habitats exist in the study area and that most tamarisk infestations do not contain characteristics that satisfy the habitat requirements of E. traillii extimus . Based on this study, effective biologic control of Tamarix spp. may, in the short term, reduce suitable habitat available to E. traillii extimus , but also has the potential in the long term to increase suitable habitat if appropriate mixes of native woody vegetation replace tamarisk in biocontrol areas.

Frontiers of Earth Science

How well can fishes prey on zebra mussels in eastern North America?

Literature on mollusk-eating fishes was reviewed to determine the potential for different species of fish to control zebra mussels in eastern North America. At least six species are potential predators of zebra mussels because they possess (1) both upper and lower pharyngeal teeth or (2) lower pharyngeal teeth and chewing pads located on the dorsal roof for crushing mollusk shells. Freshwater drum ( Aplodinotus grunniens ) and two centrarchids, redear sunfish ( Lepomis microlophus ) and pumpkinseed ( L. gibbosus ), possess both upper and lower pharyngeal teeth and are likely to consume more zebra mussels than fishes with only lower pharyngeal teeth. Only two catostomid species, copper and river redhorses ( Moxostoma hubbsi and M. carinatum ), have chewing pads that enable them to crush mollusks. The exotic omnivorous common carp ( Cyprinus carpio ), possessing lower teeth and a chewing pad, may prey on zebra mussels when aquatic insect larvae, its preferred food, become rare. Managing populations of drum, sunfishes and redhorses to reduce exploitation of large individuals and improve their habitats are suggested as means to intensify biological control of zebra mussels in eastern North America. Other Eurasian molluscivores, the roach ( Rutilus rutilus ) and the black carp ( Mylopharyngodon piceus ) should not be introduced into North America because research has shown repeatedly that an introduced biological controller usually does not forage for unwanted pests or reside only in preferred habitats of pests. Drum, sunfishes and redhorses should be preferred over these exotics as biological controllers of zebra mussels in North America because these native fishes will likely occupy newly established habitats of zebra mussels.

Fisheries

Differential parasitism of seed-feeding Cydia (Lepidoptera: Tortricidae) by native and alien wasp species relative to elevation in subalpine Sophora (Fabaceae) forests on Mauna Kea, Hawaii

Alien parasitic wasps, including accidental introductions and purposefully released biological control agents, have been implicated in the decline of native Hawaiian Lepidoptera. Understanding the potential impacts of alien wasps requires knowledge of ecological parameters that influence parasitism rates for species in their new environment. Sophora seed-feeding Cydia spp. (Lepidoptera: Tortricidae) were surveyed for larval parasitoids to determine how native and alien wasps are partitioned over an elevation gradient (2200-2800 m) on Hawaii Island, Hawaii. Parasitism rate of native Euderus metallicus (Eulophidae) increased with increased elevation, while parasitism rate by immigrant Calliephialtes grapholithae (Ichneumonidae) decreased. Parasitism by Pristomerus hawaiiensis (Ichneumonidae), origins uncertain, also decreased with increased elevation. Two other species, Diadegma blackburni (Ichneumonidae), origins uncertain, and Brasema cushmani (Eupelmidae), a purposefully introduced biological control agent for pepper weevil, did not vary significantly with elevation. Results are contrasted with a previous study of this system with implications for the conservation of an endangered bird species that feed on Cydia larvae. Interpretation of results is hindered by lack of knowledge of autecology of moths and wasps, origins, phylogeny, systematics, competitive ability, and physiological limitations of each wasp species. These factors should be incorporated into risk analysis for biological control introductions and invasive species programs. ?? 2004 Kluwer Academic Publishers.

Journal of Insect Conservation

Modeling the compensatory response of an invasive tree to specialist insect herbivory

The severity of the effects of herbivory on plant fitness can be moderated by the ability of plants to compensate for biomass loss. Compensation is an important component of the ecological fitness in many plants, and has been shown to reduce the effects of pests on agricultural plant yields. It can also reduce the effectiveness of biocontrol through introduced herbivores in controlling weedy invasive plants. This study used a modeling approach to predict the effect of different levels of foliage herbivory by biological control agents introduced to control the invasive tree Melaleuca quinquennervia (melaleuca) in Florida. It is assumed in the model that melaleuca can optimally change its carbon and nitrogen allocation strategies in order to compensate for the effects of herbivory. The model includes reallocation of more resources to production and maintenance of photosynthetic tissues at the expense of roots. This compensation is shown to buffer the severity of the defoliation effect, but the model predicts a limit on the maximum herbivory that melaleuca can tolerate and survive. The model also shows that the level of available limiting nutrient (e.g., soil nitrogen) may play an important role in a melaleuca’s ability to compensate for herbivory. This study has management implications for the best ways to maximize the level of damage using biological control or other means of defoliation.

Florida

Detection of tamarisk defoliation by the northern tamarisk beetle based on multitemporal Landsat 5 thematic mapper imagery.

The spread of tamarisk ( Tamarix spp., also known as saltcedar) is a significant ecological disturbance in western North America and has long been targeted for control, leading to the importation of the northern tamarisk beetle ( Diorhabda carinulata ) as a biological control agent. Following its initial release along the Colorado River near Moab, Utah in 2004, the beetle has successfully established and defoliated tamarisk across much of the upper Colorado River Basin. However, the spatial distribution and seasonal timing of defoliation are complex and difficult to quantify over large areas. To address this challenge, we tested and compared two remote sensing approaches to mapping tamarisk defoliation: Disturbance Index (DI) and a decision tree method called Random Forest (RF). Based on multitemporal Landsat 5 TM imagery for 2006-2010, changes in DI and defoliation probability from RF were calculated to detect tamarisk defoliation along the banks of Green, Colorado, Dolores and San Juan rivers within the Colorado Plateau area. Defoliation mapping accuracy was assessed based on field surveys partitioned into 10 km sections of river and on regions of interest created for continuous riparian vegetation. The DI method detected 3711 ha of defoliated area in 2007, 7350 ha in 2008, 10,457 ha in 2009 and 5898 ha in 2010. The RF method detected much smaller areas of defoliation but proved to have higher accuracy, as demonstrated by accuracy assessment and sensitivity analysis, with 784 ha in 2007, 960 ha in 2008, 934 ha in 2009, and 1008 ha in 2010. Results indicate that remote sensing approaches are likely to be useful for studying spatiotemporal patterns of tamarisk defoliation as the tamarisk leaf beetle spreads throughout the western United States.

Arizona, Colorado, New Mexico, Utah, Wyoming

Plant invasions in protected areas of tropical pacific islands, with special reference to Hawaii

Isolated tropical islands are notoriously vulnerable to plant invasions. Serious management for protection of native biodiversity in Hawaii began in the 1970s, arguably at Hawaii Volcanoes National Park. Concerted alien plant management began there in the 1980s and has in a sense become a model for protected areas throughout Hawaii and Pacific Island countries and territories. We review the relative successes of their strategies and touch upon how their experience has been applied elsewhere. Protected areas in Hawaii are fortunate in having relatively good resources for addressing plant invasions, but many invasions remain intractable, and invasions from outside the boundaries continue from a highly globalised society with a penchant for horticultural novelty. There are likely few efforts in most Pacific Islands to combat alien plant invasions in protected areas, but such areas may often have fewer plant invasions as a result of their relative remoteness and/or socio-economic development status. The greatest current needs for protected areas in this region may be for establishment of yet more protected areas, for better resources to combat invasions in Pacific Island countries and territories, for more effective control methods including biological control programme to contain intractable species, and for meaningful efforts to address prevention and early detection of potential new invaders.

Hawaii

Short-term disruption of a leafy spurge (Euphorbia esula) biocontrol program following herbicide application

Integrated pest management (IPM) for invasive plant species is being advocated by researchers and implemented by land managers, but few studies have evaluated the success of IPM programs in natural areas. We assessed the relative effects of components of an IPM program for leafy spurge (Euphorbia esula), an invasive plant, at Theodore Roosevelt National Park, North Dakota. Effects of herbicides on leafy spurge abundance and on dynamics of flea beetles (Aphthona spp.) used to control leafy spurge were evaluated over three field seasons following herbicide application. We monitored leafy spurge-infested plots with established flea beetle populations that had received picloram plus 2,4-D in September 1997 or 1998, imazapic in September 1998, versus those with no chemical treatment. Mature stem counts did not differ significantly between treated and untreated plots in 2001, suggesting that leafy spurge stands had recovered from herbicide treatment. Flea beetles were less abundant on plots with a history of herbicide treatment. Structural equation models indicated that in 2000 negative correlations between relative abundances of the two flea beetle species were greater on plots that had received herbicide treatments than on those that had not, but by 2001 no differences were apparent between treated and untreated plots. These results suggest that the most effective component of IPM for leafy spurge at this site is biological control. All herbicide effects we observed were short-lived, but the increased negative correlation between flea beetle relative abundances during 2000 implies that herbicide application may have temporarily disrupted an effective biological control program at this site. ?? 2006 Elsevier Inc. All rights reserved.

Biological Control

A river system to watch: documenting the effects of saltcedar ( Tamarix spp.) biocontrol in the Virgin River valley

Throughout riparian areas of the southwestern United States, non-native saltcedar (also known as tamarisk; Tamarix spp.) can form dense, monotypic stands and is often reported to have detrimental effects on native plants and habitat quality (Everitt 1980; Shafroth et al. 2005). Natural resource managers of these riparian areas spend considerable time and resources controlling saltcedar using a variety of techniques, including chemical (Duncan and McDaniel 1998), mechanical, and burning methods (Shafroth et al. 2005). Approximately one billion dollars are spent each year on river restoration projects nationally (Bernhardt et al. 2005), and a majority of these projects focus on invasive species control in the Southwest (Follstad Shah et al. 2007). A technique that has drawn much attention is the use of the saltcedar leaf beetle ( Diorhabda spp.), a specialist herbivore, as biological control of saltcedar (Lewis et al. 2003). Research testing was conducted with beetles housed in secure enclosures in six states in 1998 and 1999 (Dudley et al. 2001), followed by open release at some of those sites starting in 2001 (DeLoach et al. 2004). By 2005, full-scale saltcedar biocontrol was implemented in 13 states, led by the USDA Animal and Plant Health Inspection Service (APHIS), the agency that oversees biological control programs, and with the participation and support of the U.S. Fish and Wildlife Service (USFWS). Despite the widespread application of Diorhabda , however, only limited research has quantified the consequences (benefits and costs) on biotic communities and ecosystem services. Alterations to riparian areas caused by various non-native species control activities have the potential to affect a variety of habitat types used by wildlife (Bateman et al. 2008a); processes like water availability, fluvial deposition, and erosion; and the establishment of other non-native species (Carruthers and D'Antonio 2005, Shafroth et al. 2005, DeLoach et al. 2006). Similarly, biocontrol is expected to modify riparian ecosystems, and it is imperative to document and evaluate both the environmental benefits and the potential costs of this tamarisk management method.

Virgin River

Tamarisk biocontrol in the western United States: Ecological and societal implications

Tamarisk species (genus Tamarix), also commonly known as saltcedar, are among the most successful plant invaders in the western United States. At the same time, tamarisk has been cited as having enormous economic costs. Accordingly, local, state, and federal agencies have undertaken considerable efforts to eradicate this invasive plant and restore riparian habitats to pre-invasion status. Traditional eradication methods, including herbicide treatments, are now considered undesirable, because they are costly and often have unintended negative impacts on native species. A new biological control agent, the saltcedar leaf beetle (Diorhabda elongata), has been released along many watersheds in the western US, to reduce the extent of tamarisk cover in riparian areas. However, the use of this insect as a biological control agent may have unintended ecological, hydrological, and socioeconomic consequences that need to be anticipated by land managers and stakeholders undertaking restoration efforts. Here, we examine the possible ramifications of tamarisk control and offer recommendations to reduce potential negative impacts on valued riparian systems in the western US.

Frontiers in Ecology and the Environment

Influences of the Tamarisk Leaf Beetle ( Diorhabda carinulata ) on the diet of insectivorous birds along the Dolores River in Southwestern Colorado

We examined the effects of a biologic control agent, the tamarisk leaf beetle (Diorhabda carinulata), on native avifauna in southwestern Colorado, specifically, addressing whether and to what degree birds eat tamarisk leaf beetles. In 2010, we documented avian foraging behavior, characterized the arthropod community, sampled bird diets, and undertook an experiment to determine whether tamarisk leaf beetles are palatable to birds. We observed that tamarisk leaf beetles compose 24.0 percent (95-percent-confidence interval, 19.9-27.4 percent) and 35.4 percent (95-percent-confidence interval, 32.4-45.1 percent) of arthropod abundance and biomass in the study area, respectively. Birds ate few tamarisk leaf beetles, despite a superabundance of D. carinulata in the environment. The frequency of occurrence of tamarisk leaf beetles in bird diets was 2.1 percent (95-percent-confidence interval, 1.3- 2.9 percent) by abundance and 3.4 percent (95-percent-confidence interval, 2.6-4.2 percent) by biomass. Thus, tamarisk leaf beetles probably do not contribute significantly to the diets of birds in areas where biologic control of tamarisk is being applied.

Colorado;Utah

Global cycling and climate effects of aeolian dust controlled by biological soil crusts

Biological soil crusts (biocrusts) cover ~12% of the global land surface. They are formed by an intimate association between soil particles, photoautotrophic and heterotrophic organisms, and they effectively stabilize the soil surface of drylands. Quantitative information on the impact of biocrusts on the global cycling and climate effects of aeolian dust, however, is not available. Here, we combine the currently limited experimental data with a global climate model to investigate the effects of biocrusts on regional and global dust cycling under current and future conditions. We estimate that biocrusts reduce the global atmospheric dust emissions by ~60%, preventing the release of ~0.7 Pg dust per year. Until 2070, biocrust coverage is expected to be severely reduced by climate change and land-use intensification. The biocrust loss will cause an increased dust burden, leading to a reduction of the global radiation budget of around 0.12 to 0.22 W m−2, corresponding to about 50% of the total direct forcing of anthropogenic aerosols. This biocrust control on dust cycling and its climate impacts have important implications for human health, biogeochemical cycling and the functioning of the ecosystems, and thus should be considered in the modelling, mitigation and management of global change.

Nature Geoscience

Controls of biological soil crust cover and composition shift with succession in sagebrush shrub-steppe

Successional stage may determine strength and causal direction of interactions among abiotic and biotic factors; e.g., species that facilitate the establishment of other species may later compete with them. We evaluated multivariate hypotheses about abiotic and biotic factors shaping biological soil crusts (BSCs) in early and late successional stages. We surveyed vegetation and BSC in the shrub-steppe ecosystem of the Columbia Basin. We analyzed the relationships with bryophyte and lichen covers using structural equation models, and analyzed the relationships with BSC composition using Indicator Species Analysis and distance-based linear models. Cover, indicator species, and composition varied with successional stage. Increasing elevation and bryophyte cover had higher lichen cover early in succession; these relationships were negative in the later successional stage. Lichen cover did not appear to impede B. tectorum cover, but B. tectorum appeared to strongly negatively affect lichen cover in both stages. Biological soil crust composition varied with bunchgrass cover in the early successional stage, but with elevation and B. tectorum cover later in succession. Our findings support the hypotheses that as succession progresses, the strength and direction of certain community interactions shift, and B. tectorum leads to reductions in biological soil crust cover regardless of successional stage.

Journal of Arid Environments

Global assessment of schistosomiasis control over the past century shows targeting the snail intermediate host works best

Background Despite control efforts, human schistosomiasis remains prevalent throughout Africa, Asia, and South America. The global schistosomiasis burden has changed little since the new anthelmintic drug, praziquantel, promised widespread control. Methodology We evaluated large-scale schistosomiasis control attempts over the past century and across the globe by identifying factors that predict control program success: snail control (e.g., molluscicides or biological control), mass drug administrations (MDA) with praziquantel, or a combined strategy using both. For data, we compiled historical information on control tactics and their quantitative outcomes for all 83 countries and territories in which: (i) schistosomiasis was allegedly endemic during the 20 th century, and (ii) schistosomiasis remains endemic, or (iii) schistosomiasis has been "eliminated," or is "no longer endemic," or transmission has been interrupted. Principal Findings Widespread snail control reduced prevalence by 92 ± 5% (N = 19) vs. 37 ± 7% (N = 29) for programs using little or no snail control. In addition, ecological, economic, and political factors contributed to schistosomiasis elimination. For instance, snail control was most common and widespread in wealthier countries and when control began earlier in the 20 th century. Conclusions/Significance Snail control has been the most effective way to reduce schistosomiasis prevalence. Despite evidence that snail control leads to long-term disease reduction and elimination, most current schistosomiasis control efforts emphasize MDA using praziquantel over snail control. Combining drug-based control programs with affordable snail control seems the best strategy for eliminating schistosomiasis.

PLoS Neglected Tropical Diseases

Intended consequences statement

As the biodiversity crisis accelerates, the stakes are higher for threatened plants and animals. Rebuilding the health of our planet will require addressing underlying threats at many scales, including habitat loss and climate change. Conservation interventions such as habitat protection, management, restoration, predator control, translocation, genetic rescue, and biological control have the potential to help threatened or endangered species avert extinction. These existing, well-tested methods can be complemented and augmented by more frequent and faster adoption of new technologies, such as powerful new genetic tools. In addition, synthetic biology might offer solutions to currently intractable conservation problems. We believe that conservation needs to be bold and clear-eyed in this moment of great urgency.

Conservation Science and Practice

Quagga and zebra mussels: biology, impacts, and control

Quagga and Zebra Mussels: Biology, Impacts, and Control , Second Edition provides a broad view of the zebra/quagga mussel issue, offering a historic perspective and up-to-date information on mussel research. Comprising 48 chapters, this second edition includes reviews of mussel morphology, physiology, and behavior. It details mussel distribution and spread in Europe and across North America, and examines policy and regulatory responses, management strategies, and mitigation efforts. In addition, this book provides extensive coverage of the impact of invasive mussel species on freshwater ecosystems, including effects on water clarity, phytoplankton, water quality, food web changes, and consequences to other aquatic fauna. It also reviews and offers new insights on how zebra and quagga mussels respond and adapt to varying environmental conditions. This new edition includes seven video clips that complement chapter text and, through visual documentation, provide a greater understanding of mussel behavior and distribution.

Book

Egg parasitoids of Sophonia rufofascia (Homoptera: Cicadellidae) in Hawaii Volcanoes National Park

Parasitism of the leafhopper Sophonia rufofascia (Kuoh and Kuoh), a recent immigrant that has become a widespread pest in Hawaii, was examined in a 1-year survey in Hawaii Volcanoes National Park. Samples of young leaves of four plant species infested with eggs of S. rufofascia were collected at five sites ranging from 880 to 1190 m in elevation. Leafhopper eggs were parasitized principally by three species of Mymaridae (Hymenoptera): Polynema sp., Schizophragma sp. probably bicolor (Dozier), and Chaetomymar sp. Although parasitism by each species fluctuated at levels usually below 10%, all three were detected consistently across most host plants, sites, and sample periods. Total parasitism differed at a marginally significant level among host plants and sites, but not among sample periods. Total parasitism averaged 14.3% (maximum: 26.3%) on Dodonaea viscosa Jacquin, 10.6% (maximum: 17.5%) on Myrica faya Aiton, 8.7% (maximum: 29.5%) on Metrosideros polymorpha Gaudich-Beaupre, and 1.6% (maximum: 4.3%) on Vaccinium reticulatum Smith. Parasitism was generally higher at sites lower in elevation. Further monitoring is recommended to determine whether parasitism will increase to levels that can effectively suppress S. rufofascia populations. The efficacy of natural enemies already present in Hawaii is important because concern over nontarget impacts on endemic leafhoppers makes introduction of new biological control agents difficult. ?? 2001 Academic Press.

Biological Control

Bureau of Sport Fisheries and Wildlife Pesticide-Wildlife Review: 1959

Research findings of the Bureau of Sport Fisheries and Wildlife, State agencies and independent research workers in Ala., Ark., Fla., Ga., La., Mass., Mich., Mont., N. Dak., Tex., and Wis. are summarized in this report together with recommendations for reducing damage from pest control operations. Major topics discussed are: Scope of Pesticide-Wildlife Problem; Effects on Wildlife-General; Laboratory Studies and Toxicology; Direct and Indirect Effects of Pesticides on Wildlife; Recent Pesticide Legislation; Value of Wildlife; and Recommendations for Safeguarding Wildlife Values during Pest Control. To avoid undue hazards to wildlife, applications must not exceed the toxicity equivalent of the following concentrations of DDT to the respective forms of wildlife: 0.1 pounds of DDT/acre for crustaceans; 0.2 for fish; 1.0 for amphibians; 2.0 for reptiles and birds; and 5.0 for most mammals. Other suggestions are: 1) Chemical treatment should be used only when entomological research has proved it to be necessary; 2) Before pesticides are used, the effects on different kinds of animals and on animals living in different habitats should be known and carefully considered; 3) Only minimum quantities of chemicals necessary to achieve adequate control of pests should be applied; 4) Pesticides should not be applied to areas that are any larger than is necessary and the chemicals that are used should be the ones whose effects are no more long-lasting than necessary; 5) Whenever possible, chemicals should be applied at the seasons of the year when wildlife damage will be least; 6) Conscientious effort should be made to be sure that pesticides are applied at no more than the intended rates and that no areas receive double doses. Alternates to chemical control are suggested. Among these are biological control, modified agricultural practices, destruction of insect wintering quarters, and the manipulation of water levels.

Circular