25 research outputs found
Seasonal and Spatial Effects of Wastewater Effluent on Growth, Survival, and Accumulation of Microbial Contaminants by Oysters in Mobile Bay, Alabama
We measured seasonal effects of wastewater treatment plant (WTP) effluent on growth, survival, and accumulation of microbes in oysters near a major WTP in Mobile Bay, AL. Despite higher nutrients near the WTP, seasonal conditions rather than distance affected chlorophyll a concentration and oyster growth. In summer and fall, when oyster growth was higher, δ15N‰ in oysters near the WTP changed through time to reflect δ15N‰ in effluent (approx. −4‰). Microbial indicators (male-specific coliphage, fecal coliforms) were highest in oysters near the WTP in all seasons and correlated with δ15N‰ in fall and summer. Increased riverine discharge and slower acquisition of δ15N‰ likely confounded correlations in winter/spring. Although we did not detect gross ecological effects of wastewater exposure for oysters, data indicated waste water derived particles entered the local food web and accumulated in oysters. These data highlight the importance of using multiple indicators of wastewater exposure and considering both seasonal and spatial effects when defining wastewater influence on a system or species
Short-Term Exposure to Warm Microhabitats Could Explain Amphibian Persistence with Batrachochytrium dendrobatidis
Environmental conditions can alter the outcomes of symbiotic interactions. Many amphibian species have declined due to chytridiomycosis, caused by the pathogenic fungus Batrachochytrium dendrobatidis (Bd), but many others persist despite high Bd infection prevalence. This indicates that Bd's virulence is lower, or it may even be a commensal, in some hosts. In the Australian Wet Tropics, chytridiomycosis extirpated Litoria nannotis from high-elevation rain forests in the early 1990 s. Although the species is recolonizing many sites, no population has fully recovered. Litoria lorica disappeared from all known sites in the early 1990 s and was thought globally extinct, but a new population was discovered in 2008, in an upland dry forest habitat it shares with L. nannotis. All frogs of both species observed during three population censuses were apparently healthy, but most carried Bd. Frogs perch on sun-warmed rocks in dry forest streams, possibly keeping Bd infections below the lethal threshold attained in cooler rain forests. We tested whether short-term elevated temperatures can hamper Bd growth in vitro over one generation (four days). Simulating the temperatures available to frogs on strongly and moderately warmed rocks in dry forests, by incubating cultures at 33°C for one hour daily, reduced Bd growth below that of Bd held at 15°C constantly (representing rain forest habitats). Even small decreases in the exponential growth rate of Bd on hosts may contribute to the survival of frogs in dry forests
Antifungal isolates database of amphibian skin-associated bacteria and function against emerging fungal pathogens
Microbial symbionts of vertebrate skin have an important function in defense of the host against pathogens. In particular, the emerging chytrid fungus Batrachochytrium
dendrobatidis, causes widespread disease in amphibians but can be inhibited via secondary metabolites produced by many different skin-associated bacteria. Similarly, the fungal
pathogens of terrestrial salamander eggs Mariannaea elegans and Rhizomucor variabilis are also inhibited by a variety of skin-associated bacteria. Indeed, probiotic therapy against fungal diseases is a recent approach in conservation medicine with growing experimental support. We
present a comprehensive Antifungal Isolates Database of amphibian skin-associated bacteria that have been cultured, isolated, and tested for antifungal properties. At the start, this database includes nearly 2000 cultured bacterial isolates from 37 amphibian host species
across 18 studies on five continents: Africa, Oceania, Europe, and North and South America.
As the research community gathers information on additional isolates, the database will be updated periodically. The resulting database can serve as a conservation tool for amphibians and other organisms, and provides empirical data for comparative and bioinformatic studies.
The database consists of a FASTA file containing 16S rRNA gene sequences of the bacterial isolates, and a metadata file containing information on the host species, life-stage, geographic region, and antifungal capacity and taxonomic identity of the isolate
Chytridiomycosis and symbiosis: context-dependency in amphibian disease and conservation
Symbioses, long-term direct relationships between individuals of multiple species, are well known from many taxa and biomes. Although they are often thought of as static, symbioses are frequently dependent on environmental or ecological context. While there is a substantial amount of information on context-dependence in many symbioses, there little is known of how symbioses important to wildlife disease and conservation vary.\ud
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One disease of conservation importance that may be strongly affected by contextdependent symbioses is chytridiomycosis. This amphibian disease is caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) and has caused population declines and extinctions on several continents. Bd's growth rate depends on environmental context, as evidenced by its distinct in vitro thermal optimum (17-25°C). The majority of Bd-driven declines have occurred in relatively cool climates (at high-elevation and during winter in tropical regions), demonstrating that environmental context affects disease outcome. However, many cool weather declines have occurred at temperatures well below Bd's thermal optimum, where chytridiomycosis might be expected to be less severe. Two possible explanations for this pattern are that Bd in natural environments may adapt to low temperatures by increasing fecundity, or that production of anti-Bd skin peptides, a component of many amphibians' innate immunity, may be down-regulated in cool environments. Still a third possible explanation for the high incidence of Bd-driven declines at temperatures below the fungus's in vitro thermal optimum is that symbiotic bacteria that also inhabit amphibian skin and that can reduce the severity of chytridiomycosis may have severely reduced activity or density at cooler temperatures. However, no information exists on how the composition or antifungal activity of amphibians' anti-Bd bacterial assemblages respond to environmental contexts.\ud
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Eventually, antifungal bacterial symbiont populations may be augmented on amphibians' skin for management of chytridiomycosis. Currently, there is no broadly effective treatment or preventative available for wild amphibians at risk of chytridiomycosis, but supplementing amphibians' natural protective microflora, to enhance the protective effect they lend (termed "bioaugmentation,") is being explored. If these bacteria's anti-Bd activity varies with environmental and ecological context, bioaugmentation will require careful selection of robustly antifungal bacteria.\ud
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I identified 16 bacterial species previously not known to act as anti-Bd symbionts on the rainforest tree frogs Litoria serrata and L. nannotis. On average, in vitro anti-Bd activity of symbionts (both newly identified and previously known) from all bacterial classes was reduced at cooler temperatures characteristic of areas where declines driven by chytridiomycosis have been most severe. Such context-dependency in anti-Bd activity of amphibian symbionts may partially explain the association of past Bd-driven declines with cool temperatures, especially below the fungus's thermal optimum. It could also affect selection of bacteria for bioaugmentation and disease management.\ud
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Bd is a member of the little-studied and phylogenetically-basal Chytridiomycota, which are only distantly related to the better-studied higher fungi. Little is known of chytrids' interactions with bacteria. However, many higher fungi induce or inhibit the antifungal activity of antagonistic bacteria, altering the outcome of microbial symbioses and affecting agricultural biocontrol schemes. If Bd has mechanisms to defend against antifungal bacteria, they might adversely affect the success of bioaugmentation in natural amphibian populations. I found that Bd metabolites can affect the anti-Bd activity of antifungal bacterial symbionts isolated from Litoria serrata, L. rheocola, and L. nannotis. The activity of most symbionts was not affected, suggesting that although bacteria that are candidates for bioaugmentation will need to be screened for responses to Bd metabolites, most will not be affected. Activity of Bd metabolites should therefore not pose a severe problem for the management of chytridiomycosis by bioaugmentation, although Bd may still harbor non-chemical defense mechanisms not yet detected or evaluated.\ud
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While many amphibian species have declined due to Bd, some populations persist in an apparent commensal relationship with Bd. For example, in the Australian Wet Tropics, Litoria nannotis declined sharply at high elevation rain forest sites due to Bd in the early 1990s, and has not recovered. However L. nannotis, and one population of L. lorica, the latter previously believed extinct due to Bd, were recently found in high elevation dry forests, apparently healthy, but infected with Bd at high prevalence. One explanation previously suggested for persistence with Bd in dry forests is that exposure to sun-warmed rocks frogs perch on in these habitats may be keeping Bd infections below the lethal threshold attained at cooler rain forest sites. I tested whether short-term exposure to elevated temperatures can hamper in vitro Bd growth. One hour daily at 33°C, but not at 28°C (representing exposure to heavily and more moderately warmed rocks in dry forests, respectively) reduced in vitro Bd growth below that in a constant 15°C regime (representing cool rain forest habitats). The reduction in Bd growth over the fungus's first generation after inoculation was small but may translate into maintenance of Bd infection intensities below a lethal threshold in natural settings over multiple generations of Bd growth.\ud
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My work provides early evidence of the role context-dependency may play in determining the outcome of the amphibian-Bd-bacteria symbiosis. If observed reductions in the anti-Bd activity of amphibians' bacterial symbionts at cool temperatures in vitro translate to wild frogs' symbionts, then corresponding losses in amphibian protection from Bd could account for the relatively frequent occurrence of amphibian declines at cool temperatures below Bd’s thermal optimum. In what was, to my knowledge, the first study of a chytrid fungus's effects on antagonistic bacteria, I found that metabolites of Bd were not active against the majority of Litoria spp. bacterial symbionts tested, suggesting that most antagonistic bacteria are not affected by any defenses involving metabolites. In future work based on the present study, chemical methods could be used to measure in situ concentrations of antifungal compounds on amphibian skin, and to identify the composition of Bd's metabolites. Future studies should also clarify the roles of warm microhabitats, amphibian immunity, and animal behavior in driving the apparent commensal nature of the amphibian-Bd symbiosis in tropical Australia’s upland dry forests and elsewhere
Incidence and impacts of war-driven mammal declines in African ecosystems
Warfare has been common in Africa, and the civilian and military movements, artillery use, lawlessness, poverty, and changes in conservation investment that accompany armed conflict can affect wildlife either positively or negatively. I provide the first quantitative synthesis of war’s impact on wildlife, and consider the aftermath of war-driven mammal declines for ecological communities.
In Chapter One I evaluate war’s impact on Africa’s large mammals. I pair literature-based density estimates for 36 species from 126 protected areas and 19 countries with conflict locations, and nine other ecological and socio-economic predictors which might explain mammal declines. For 1946–2010 (and 1989–2010) mammals declined more often where conflict was more frequent, and conflict frequency was the best predictor of mammal population trajectories.
In Chapter Two, I measure the impacts of war-driven mammal declines on vegetation structure in Mozambique’s Gorongosa National Park. Using historical (1977) and modern satellite (2012) satellite imagery, I document a one-third increase in tree cover across the 3670 km2 park following the near-extirpation of large herbivores during the country’s civil war. The results accord with those from smaller-scale experiments showing that the effect of eliminating grazers (fewer trees) is trumped by that of removing browsers (more trees).
Chapter Three is a global meta-analysis that finds the strength of large mammalian herbivore impacts (through competition, facilitation, and habitat modification) on other animals are stronger in areas of lower net primary productivity; there plants are slower to recover from direct effects of herbivory, which mediate herbivore impacts on animals. We can expect mammal declines (war-driven and otherwise) to have their greatest community-wide impacts in these low-productivity habitats.
Finally, in Chapter Four, I consider habitat selection in Gorongosa’s post-war, recovering populations of three congeneric antelope: bushbuck, nyala, and kudu. Understanding species’ habitat preferences allows ecosystem management for their benefit. Using hourly antelope movement data and GIS-based habitat classifications, I show that all three species preferred areas closer to termite mounds, plus certain fire regimes and vegetation structure. The strength of selection for each of these factors scaled with species’ body size, making this a rare demonstration of landscape-scale consequences of allometry
Data from: Does primary productivity modulate the indirect effects of large herbivores? A global meta-analysis
1. Indirect effects of large mammalian herbivores (LMH), while much less studied than those of apex predators, are increasingly recognized to exert powerful influences on communities and ecosystems. The strength of these effects is spatiotemporally variable, and several sets of authors have suggested that they are governed in part by primary productivity. However, prior theoretical and field studies have generated conflicting results and predictions, underscoring the need for a synthetic global analysis.
2. We conducted a meta-analysis of the direction and magnitude of large mammalian herbivore-initiated indirect interactions using 67 published studies comprising 456 individual responses. We georeferenced 41 of these studies (comprising 253 responses from 33 locations on 5 continents) to a satellite-derived map of primary productivity. Because predator assemblages might also influence the impact of large herbivores, we conducted a similar analysis using a global map of large-carnivore species richness.
3. In general, LMH reduced the abundance of other consumer species and also tended to reduce consumer richness, although the latter effect was only marginally significant.
4. There was a pronounced reduction in the strength of negative (i.e., suppressive, due e.g. to competition) indirect effects of LMH on consumer abundance in more productive ecosystems. In contrast, positive (facilitative) indirect effects were not significantly correlated with productivity, likely because these comprised a more heterogeneous array of mechanisms. We found no effect of carnivore species richness on herbivore-initiated indirect effect strength.
5. Our findings help to resolve the fundamental problem of ecological contingency as it pertains to the strength of an under-studied class of multi-trophic interactions. Moreover, these results will aid in predicting the indirect effects of anthropogenic wildlife declines and irruptions, and how these effects might be mediated by climatically driven shifts in resource availability. To the extent that intact ungulate guilds help to suppress populations of small animals that act as agricultural pests and disease reservoirs, the negative impacts of large-mammal declines on human well-being may be relatively stronger in low-productivity areas
Data from: Ecological legacies of civil war: 35-year increase in savanna tree cover following wholesale large-mammal declines
1. Large mammalian herbivores (LMH) exert strong effects on plants in tropical savannas, and many wild LMH populations are declining. However, predicting the impacts of these declines on vegetation structure remains challenging. 2. Experiments suggest that tree cover can increase rapidly following LMH exclusion. Yet it is unclear whether these results scale up to predict ecosystem-level impacts of LMH declines, which often alter fire regimes, trigger compensatory responses of other herbivores, and accompany anthropogenic land-use changes. Moreover, theory predicts that grazers and browsers should have opposing effects on tree cover, further complicating efforts to forecast the outcomes of community-wide declines. 3. We used the near-extirpation of grazing and browsing LMH from Gorongosa National Park during the Mozambican Civil War (1977-1992) as a natural experiment to test whether megafaunal collapse increased tree cover. We classified herbaceous and tree cover in satellite images taken (a) at the onset of war in 1977 and (b) in 2012, two decades after hostilities ceased. 4. Throughout the 3620-km2 park, proportional tree cover increased by 34% (from 0.29 to 0.39)—an addition of 362 km2. Four of the park's five major habitat zones (including miombo woodland, Acacia-Combretum-palm savanna, and floodplain grassland) showed even greater increases in tree cover (51–134%), with an average increase of 94% in ecologically critical Rift Valley habitats. Only in the eastern Cheringoma Plateau, which had historically low wildlife densities, did tree cover decrease (by 5%). 5. The most parsimonious explanation for these results is that reduced browsing pressure enhanced tree growth, survival, and/or recruitment; we found no directional trends in rainfall or fire that could explain increased tree cover. 6. Synthesis: Catastrophic large-herbivore die-offs in Mozambique's flagship national park were followed by 35 years of woodland expansion, most severely in areas where pre-war wildlife biomass was greatest. These findings suggest that browsing release supersedes grazer-grass-fire feedbacks in governing ecosystem-level tree cover, consistent with smaller-scale experimental results, although the potentially complementary effect of CO2 fertilization cannot be definitively ruled out. Future work in Gorongosa will reveal whether recovering LMH populations reverse this trend, or alternatively whether woody encroachment hinders ongoing restoration efforts
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Ecological legacies of civil war: 35-year increase in savanna tree cover following wholesale large-mammal declines
1. Large mammalian herbivores (LMH) exert strong effects on plants in tropical savannas, and many wild LMH populations are declining. However, predicting the impacts of these declines on vegetation structure remains challenging. 2. Experiments suggest that tree cover can increase rapidly following LMH exclusion. Yet it is unclear whether these results scale up to predict ecosystem-level impacts of LMH declines, which often alter fire regimes, trigger compensatory responses of other herbivores and accompany anthropogenic land-use changes. Moreover, theory predicts that grazers and browsers should have opposing effects on tree cover, further complicating efforts to forecast the outcomes of community-wide declines. 3. We used the near-extirpation of grazing and browsing LMH from Gorongosa National Park during the Mozambican Civil War (1977–1992) as a natural experiment to test whether megafaunal collapse increased tree cover. We classified herbaceous and tree cover in satellite images taken (a) at the onset of war in 1977 and (b) in 2012, two decades after hostilities ceased. 4. Throughout the 3620-km2 park, proportional tree cover increased by 34% (from 0.29 to 0.39) – an addition of 362 km2 . Four of the park’s five major habitat zones (including miombo woodland, Acacia–Combretum–palm savanna, and floodplain grassland) showed even greater increases in tree cover (51–134%), with an average increase of 94% in ecologically critical Rift Valley habitats. Only in the eastern Cheringoma Plateau, which had historically low wildlife densities, did tree cover decrease (by 5%). 5. The most parsimonious explanation for these results is that reduced browsing pressure enhanced tree growth, survival and/or recruitment; we found no directional trends in rainfall or fire that could explain increased tree cover. 6. Synthesis. Catastrophic large-herbivore die-offs in Mozambique’s flagship national park were followed by 35 years of woodland expansion, most severely in areas where pre-war wildlife biomass was greatest. These findings suggest that browsing release supersedes grazer–grass–fire feedbacks in governing ecosystem-level tree cover, consistent with smaller-scale experimental results, although the potentially complementary effect of CO2 fertilization cannot be definitively ruled out. Future work in Gorongosa will reveal whether recovering LMH populations reverse this trend, or alternatively whether woody encroachment hinders ongoing restoration efforts
Crassostrea virginica shells record local variation\ud in wastewater inputs to a coastal estuary
We measured δ15N values in the acid-insoluble organic portion of shells from Crassostrea virginica transplanted at increasing distance from a major wastewater treatment plant in Mobile Bay, Alabama. To determine whether δ15N in shell material recorded local spatial variation in\ud
wastewater influence, we compared δ15N in newly deposited oyster shell to δ15N values in wastewater effluent and in suspended particulate matter in receiving waters. We compared δ15N values in shell to δ15N in adductor muscle and whole tissues to determine the isotopic relationships between shell and soft tissues for this previously untested species. δ15N values in oyster shell reflected differences\ud
in wastewater influence relative to distance from the wastewater treatment plant within 38 d of transplanting. δ15N values in shell were enriched by 2.4‰ compared to available foods, consistent with a trophic shift from food source to consumer. δ15N values in shell also were significantly correlated with δ15N values in soft tissues, but were enriched by 1.9‰ compared to whole tissues and 0.8‰\ud
compared to adductor muscle. Overall, δ15N values in oyster shell were a better proxy for adductor muscle than whole tissues. If applied with care, oyster shells provide an ecologically and commercially meaningful wastewater detection tool that may be effective over relatively short spatial and temporal scales. δ15N values in shell material may be particularly useful to enable anthropogenic\ud
source tracing and refine food web reconstructions in areas with remnant shells where oysters or other bivalves have been severely depleted or already lost
Cool temperatures reduce antifungal activity of symbiotic bacteria of threatened amphibians: implications for disease management and patterns of decline
Chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), is a widespread disease of amphibians responsible for population declines and extinctions. Some bacteria from amphibians' skins produce antimicrobial substances active against Bd. Supplementing populations of these cutaneous antifungal bacteria might help manage chytridiomycosis in wild amphibians. However, the activity of protective bacteria may depend upon environmental conditions. Biocontrol of Bd in nature thus requires knowledge of how environmental conditions affect their anti-Bd activity. For example, Bd-driven amphibian declines have often occurred at temperatures below Bd's optimum range. It is possible these declines occurred due to reduced anti-Bd activity of bacterial symbionts at cool temperatures. Better understanding of the effects of temperature on chytridiomycosis development could also improve risk evaluation for amphibian populations yet to encounter Bd. We characterized, at a range of temperatures approximating natural seasonal variation, the anti-Bd activity of bacterial symbionts from the skins of three species of rainforest tree frogs (Litoria nannotis, Litoria rheocola, and Litoria serrata). All three species declined during chytridiomycosis outbreaks in the late 1980s and early 1990s and have subsequently recovered to differing extents. We collected anti-Bd bacterial symbionts from frogs and cultured the bacteria at constant temperatures from 8°C to 33°C. Using a spectrophotometric assay, we monitored Bd growth in cell-free supernatants (CFSs) from each temperature treatment. CFSs from 11 of 24 bacteria showed reduced anti-Bd activity in vitro when they were produced at cool temperatures similar to those encountered by the host species during population declines. Reduced anti-Bd activity of metabolites produced at low temperatures may, therefore, partially explain the association between Bd-driven declines and cool temperatures. We show that to avoid inconsistent antifungal activity, bacteria evaluated for use in chytridiomycosis biocontrol should be tested over a range of environmental temperatures spanning those likely to be encountered in the field