Evaluating unintended consequences of intentional species introductions and eradications for improved conservation management

Increasingly intensive strategies to maintain biodiversity and ecosystem function are being deployed in response to global anthropogenic threats, including intentionally introducing and eradicating species via assisted migration, rewilding, biological control, invasive species eradications, and gene drives. These actions are highly contentious because of their potential for unintended consequences. We conducted a global literature review of these conservation actions to quantify how often unintended outcomes occur and to elucidate their underlying causes. To evaluate conservation outcomes, we developed a community assessment framework for systematically mapping the range of possible interaction types for 111 case studies. Applying this tool, we quantified the number of interaction types considered in each study and documented the nature and strength of intended and unintended outcomes. Intended outcomes were reported in 51% of cases, a combination of intended outcomes and unintended outcomes in 26%, and strictly unintended outcomes in 10%. Hence, unintended outcomes were reported in 36% of all cases evaluated. In evaluating overall conservations outcomes (weighing intended vs. unintended effects), some unintended effects were fairly innocuous relative to the conservation objective, whereas others resulted in serious unintended consequences in recipient communities. Studies that assessed a greater number of community interactions with the target species reported unintended outcomes more often, suggesting that unintended consequences may be underreported due to insufficient vetting. Most reported unintended outcomes arose from direct effects (68%) or simple density-mediated or indirect effects (25%) linked to the target species. Only a few documented cases arose from more complex interaction pathways (7%). Therefore, most unintended outcomes involved simple interactions that could be predicted and mitigated through more formal vetting. Our community assessment framework provides a tool for screening future conservation actions by mapping the recipient community interaction web to identify and mitigate unintended outcomes from intentional species introductions and eradications for conservation.     

A field experiment characterizing variable detection rates during plant surveys

Surveys aimed at finding threatened and invasive species can be challenging due to individual rarity and low and variable individual detection rates. Detection rate in plant surveys typically varies due to differences among observers, among the individual plants being surveyed (targets), and across background environments. Interactions among these 3 components may occur but are rarely estimated due to limited replication and control during data collection. We conducted an experiment to investigate sources of variation in detection of 2 Pilosella species that are invasive and sparsely distributed in the Alpine National Park, Australia. These species are superficially similar in appearance to other yellow-flowered plants occurring in this landscape. We controlled the presence and color of flowers on target Pilosella plants and controlled their placement in plots, which were selected for their variation in cover of non-target yellow flowers and dominant vegetation type. Observers mimicked Pilosella surveys in the plots and reported 1 categorical and 4 quantitative indicators of their survey experience level. We applied survival analysis to detection data to model the influence of both controlled and uncontrolled variables on detection rate. Orange- and yellow-flowering Pilosella in grass- and heath-dominated vegetation were detected at a higher rate than nonflowering Pilosella. However, this detection gain diminished as the cover of other co-occurring yellow-flowering species increased. Recent experience with Pilosella surveys improved detection rate. Detection experiments are a direct and accessible means of understanding detection processes and interpreting survey data for threatened and invasive species. Our detection findings have been used for survey planning and can inform progress toward eradication. Interaction of target and background characteristics determined detection rate, which enhanced predictions in the Pilosella eradication program and demonstrated the difficulty of transferring detection findings into untested environments.     

Spatially explicit modeling of overstory manipulations in young forests: Effects on stand structure and light

Young forests can be manipulated in diverse ways to enhance their ecological values. We used stem maps from two dense, second-growth stands in western Washington and a spatially explicit light model (tRAYci) to simulate effects of five silvicultural manipulations on diameter distribution, species composition, spatial patterning, and light availability. Each treatment removed 30% of the basal area, but differed in how trees were selected for removal. Three primary treatments were thin from below (removing the smallest trees), random thin (removing trees randomly), and gap creation (removing all trees in circles ∼1 tree height in diameter). Two additional treatments combined elements of these approaches: random ecological thin (a mixture of thin from below and random thin) and structured ecological thin (a mixture of thin from below and gap creation).     

Weed-biocontrol insects reduce native-plant recruitment through second-order apparent competition

Small-mammal seed predation is an important force structuring native-plant communities that may also influence exotic-plant invasions. In the intermountain West, deer mice (Peromyscus maniculatus) are prominent predators of native-plant seeds, but they avoid consuming seeds of certain widespread invasives like spotted knapweed (Centaurea maculosa). These mice also consume the biological-control insects Urophora spp. introduced to control C. maculosa, and this food resource substantially increases deer mouse populations. Thus, mice may play an important role in the invasion and management of C. maculosa through food-web interactions. We examined deer mouse seed predation and its effects on seedling emergence and establishment of a dominant native grass, Pseudoroegneria spicata, and forb, Balsamorhiza sagittata, in C. maculosa-invaded grasslands that were treated with herbicide to suppress C. maculosa or left untreated as controls. Deer mice readily took seeds of both native plants but removed 2-20 times more of the larger B. sagittata seeds than the smaller P. spicata seeds. Seed predation reduced emergence and establishment of both species but had greater impacts on B. sagittata. The intensity of seed predation corresponded with annual and seasonal changes in deer mouse abundance, suggesting that abundance largely determined mouse impacts on native-plant seeds. Accordingly, herbicide treatments that reduced mouse abundance by suppressing C. maculosa and its associated biocontrol food subsidies to mice also reduced seed predation and decreased the impact of deer mice on B. sagittata establishment. These results provide evidence that Urophora biocontrol agents may exacerbate the negative effects of C. maculosa on native plants through a form of second-order apparent competition-a biocontrol indirect effect that has not been previously documented. Herbicide suppressed C. maculosa and Urophora, reducing mouse populations and moderating seed predation on native plants, but the herbicide's direct negative effects on native forb seedlings overwhelmed the indirect positive effect of reducing deer mouse seed predation. By manipulating this four-level food chain, we illustrate that host-specific biological control agents may impact nontarget plant species through food-web interactions, and herbicides may influence management outcomes through indirect trophic interactions in addition to their direct effects on plants.     

Tropical coastal habitats as surrogates of fish community structure, grazing, and fisheries value

Habitat maps are frequently invoked as surrogates of biodiversity to aid the design of networks of marine reserves. Maps are used to maximize habitat heterogeneity in reserves because this is likely to maximize the number of species protected. However, the technique's efficacy is limited by intra-habitat variability in the species present and their abundances. Although communities are expected to vary among patches of the same habitat, this variability is poorly documented and rarely incorporated into reserve planning. To examine intra-habitat variability in coral-reef fishes, we generated a data set from eight tropical coastal habitats and six islands in the Bahamian archipelago using underwater visual censuses. Firstly, we provide further support for habitat heterogeneity as a surrogate of biodiversity as each predefined habitat type supported a distinct assemblage of fishes. Intra-habitat variability in fish community structure at scales of hundreds of kilometers (among islands) was significant in at least 75% of the habitats studied, depending on whether presence/absence, density, or biomass data were used. Intra-habitat variability was positively correlated with the mean number of species in that habitat when density and biomass data were used. Such relationships provide a proxy for the assessment of intra-habitat variability when detailed quantitative data are scarce. Intra-habitat variability was examined in more detail for one habitat (forereefs visually dominated by Montastraea corals). Variability in community structure among islands was driven by small, demersal families (e.g., territorial pomacentrid and labrid fishes). Finally, we examined the ecological and economic significance of intra-habitat variability in fish assemblages on Montastraea reefs by identifying how this variability affects the composition and abundances of fishes in different functional groups, the key ecosystem process of parrotfish grazing, and the ecosystem service of value of commercially important finfish. There were significant differences in a range of functional groups and grazing, but not fisheries value. Variability at the scale of tens of kilometers (among reefs around an island) was less than that among islands. Caribbean marine reserves should be replicated at scales of hundreds of kilometers, particularly for species-rich habitats, to capture important intra-habitat variability in community structure, function, and an ecosystem process.     

Are leaves that fall from imidacloprid-treated maple trees to control Asian longhorned beetles toxic to non-target decomposer organisms?

The systemic insecticide imidacloprid may be applied to deciduous trees for control of the Asian longhorned beetle, an invasive wood-boring insect. Senescent leaves falling from systemically treated trees contain imidacloprid concentrations that could pose a risk to natural decomposer organisms. We examined the effects of foliar imidacloprid concentrations on decomposer organisms by adding leaves from imidacloprid-treated sugar maple trees to aquatic and terrestrial microcosms under controlled laboratory conditions. Imidacloprid in maple leaves at realistic field concentrations (3-11 mg kg(-1)) did not affect survival of aquatic leaf-shredding insects or litter-dwelling earthworms. However, adverse sublethal effects at these concentrations were detected. Feeding rates by aquatic insects and earthworms were reduced, leaf decomposition (mass loss) was decreased, measurable weight losses occurred among earthworms, and aquatic and terrestrial microbial decomposition activity was significantly inhibited. Results of this study suggest that sugar maple trees systemically treated with imidacloprid to control Asian longhorned beetles may yield senescent leaves with residue levels sufficient to reduce natural decomposition processes in aquatic and terrestrial environments through adverse effects on non-target decomposer organisms.     

Mercury concentrations in wild mink (Mustela vison) and river otters (Lontra canadensis) collected from eastern and Atlantic Canada: relationship to age and parasitism

Total mercury (Hg) concentrations were measured in the fur, brain and liver of wild mink (Mustela vison) and river otters (Lontra canadensis) collected from eastern and Atlantic Canada. Total Hg concentrations in fur were strongly correlated with levels in the brain and liver. There was no difference in tissue concentrations between male and female mink; however, female otters had significantly higher fur, brain and liver Hg levels than males. Similarly, there was not a significant relationship between Hg concentration and age of mink, whereas in otters, Hg concentrations in all three tissues decreased significantly with age. In both species, only a very small percentage of the variability in Hg concentration was explained by age. After adjusting the data for site-to-site differences in Hg levels, Hg concentrations in the fur of mink infected by the parasite, Dioctophyma renale, were found to be significantly higher than Hg levels in uninfected mink.     

Level of contamination and impact of pesticides in cupped oyster, Crassostrea gigas, reared in a shellfish production area in Normandy (France)

Over the last decade, oysters in the Bay of Veys (Northwest France) have sporadically experienced significant summer mortality events which appear to be due to a combination of extrinsic and intrinsic factors. In the present work, the involvement of pesticides (as additional stressors) was investigated using both artificial exposure and field studies (at two sites). Six herbicides were detected in seawater following tests for a total of 15 herbicides. The most estuarine site was the most contaminated, showing relatively high values compared with those recorded in a neighboring river. No pesticides were detected in the flesh of oysters in the field but exposure experiments led to an accumulation of two substituted ureas (diuron and isoproturon, from 0.5 micro g/L and 1 micro gL(- 1) respectively). Some physiological effects were observed in terms of reproduction (partial spawning) and histopathology (atrophy of the digestive tubule epithelium) but results related to other tissue alterations and to neutral red retention (NRR) assays were not conclusive and require further investigation.     

Source to sink tracking of selected human pharmaceuticals from two Oslo city hospitals and a wastewater treatment works

The occurrence of twenty pharmaceutical compounds was quantitatively determined in effluents from two major Oslo city hospitals, Rikshospitalet and Ullev?l, along with influent, sludge and final effluent from the city's VEAS wastewater treatment works (WTW). Composite hospital effluents were collected over a twelve week period and were showed to contain paracetamol, metoprolol, diclofenac, ibuprofen, 17beta-Estradiol, estriol, estrone, oxytetracycline, tetracycline, doxycycline, chlorotetracycline, demeclocycline, trimethoprim, ciprofloxacin, sulfamethoxazole, cyclophosphamide and ifosfamide. Three pharmaceuticals were not detected above the limit of detection; cefuroxime, 17alpha-ethinylestradiol and meclocycline. Composite influent, sludge and effluent samples were collected from VEAS WTW over a seven week period. The influent into VEAS WTW contained all of the same selected substances detected in the hospital effluents, except for oxytetracycline, chlorotetracycline, demeclocycline, cyclophosphamide and ifosfamide. The percentage of pharmaceuticals entering the works from the hospitals was <10% for all of the selected compounds. VEAS sludge samples contained a different profile of substances reflecting their physico-chemical properties. Hydrophobic antibiotics, such as oxytetracycline, tetracycline and ciprofloxacin, were detected in all of the collected sludge samples. Their absence in the collected influent samples suggests that they enter the works bound to effluent particles, with the dissolved fraction observed in the hospital effluents partitioning onto particulate matter within the sewerage network. The final effluent from VEAS WTW contained reduced concentrations of many pharmaceuticals, including paracetamol, ibuprofen and sulfamethoxazole. For other compounds, such as metoprolol, diclofenac and trimethoprim, there were often higher concentrations in the effluent than the influent. These effluent concentrations represent median inputs varying from low g day(-1) (e.g. paracetamol and ibuprofen) to nearly 200 g day(-1) (e.g. metoprolol and trimethoprim) into Oslofjord. A simple risk assessment showed that the antibiotic ciprofloxacin may at times pose an acute risk to the Oslofjord aquatic environment.