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  1. Abstract

    Batrachochytrium dendrobatidis(Bd) has been associated with massive amphibian population declines worldwide. Wildlife vaccination campaigns have proven effective for mitigating damage from other pathogens, and there is evidence that adult frogs can acquire resistance to Bd when exposed to killed Bd zoospores and the metabolites they produced.

    Here, we investigated whether Cuban treefrogs tadpolesOsteopilus septentrionaliscan gain protection from Bd through exposure to a prophylaxis treatment composed of killed zoospores or soluble Bd metabolites. We used a 2 × 2 factorial design, crossing the presence or absence of killed zoospores with the presence or absence of Bd metabolites. All hosts were subsequently exposed to live Bd to evaluate susceptibility.

    Exposure to killed zoospores did not induce a protective response. However, tadpoles exposed to Bd metabolites had significantly lower Bd intensity and prevalence than tadpoles that were not exposed to metabolites.

    The metabolites Bd produce pose no risk of Bd infection and therefore make an epidemiologically safe prophylaxis treatment, protecting tadpoles against Bd. This work provides a promising potential for protecting amphibians in the wild as a disease management strategy for controlling Bd‐associated declines.

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  2. Abstract

    Agricultural expansion is predicted to increase agrochemical use two to fivefold by 2050 to meet food demand. Experimental evidence suggests that agrochemical pollution could increase snails that transmit schistosomiasis, a disease impacting 250 million people, yet most agrochemicals remain unexamined.

    Here we experimentally created >100 natural wetland communities to quantify the relative effects of fertilizer, six insecticides (chlorpyrifos, terbufos, malathion, λ‐cyhalothrin, permethrin and esfenvalerate), and six herbicides (acetochlor, alachlor, metolachlor, atrazine, propazine and simazine) on two snail genera responsible for 90% of global schistosomiasis cases.

    We identified four of six insecticides (terbufos, permethrin, chlorpyrifos and esfenvalerate) as high risk for increasing snail biomass by reducing snail predators. Hence, malathion and λ‐cyhalothrin might be useful for improving food production without increasing schistosomiasis. This top‐down effect of insecticides on predators was so strong that the effects of herbicides on schistosomiasis risk were masked in the presence of predators because there were so few snails. In the absence of snail predators, herbicide effects on snails were generally negative by reducing submerged vegetationHydrilla verticillata. The exception was that atrazine and acetochlor significantly increased the biomass of infected snails and total snails respectively.

    Like insecticides, fertilizer had strong positive effects on snail populations. Fertilizer increased both snail habitat (submerged vegetation) and snail food (periphyton), but of these two pathways, the increases in snail habitat resulted in greater snail population growth. Total snail biomass was positively associated with both infected snail biomass and parasite production and thus human infection risk.

    Synthesis and applications. Our findings suggest that fertilizers and insecticides generally have consistently higher chances of increasing human schistosomiasis than herbicides in natural communities. Furthermore, our results highlight the need to identify other low risk insecticides, which might help reduce crop pests without increasing snails and thus risk of schistosomiasis.

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  3. <sc>A</sc>bstract

    Freshwater systems are critical to life on earth, yet they are threatened by the increasing rate of synthetic chemical pollution. Current predictions of the effects of synthetic chemicals on freshwater ecosystems are hampered by the sheer number of chemical contaminants entering aquatic systems, the diversity of organisms inhabiting these systems, the myriad possible direct and indirect effects resulting from these combinations, and uncertainties concerning how contaminants might alter ecosystem metabolism via changes in biodiversity. To address these knowledge gaps, we conducted a mesocosm experiment that elucidated the responses of ponds composed of phytoplankton and zooplankton to standardized concentrations of 12 pesticides, nested within four pesticide classes, and two pesticide types. We show that the effects of the pesticides on algae were consistent within herbicides and insecticides and that responses of over 70 phytoplankton species and genera were consistent within broad taxonomic groups. Insecticides generated top‐down effects on phytoplankton community composition and abundance, which were associated with persistent increases in ecosystem respiration. Insecticides had direct toxic effects on cladocerans, which led to competitive release of copepods. These changes in the zooplankton community led to a decrease in green algae and a modest increase in diatoms. Herbicides did not change phytoplankton composition but reduced total phytoplankton abundance. This reduction in phytoplankton led to short‐term decreases in ecosystem respiration. Given that ponds release atmospheric carbon and that worldwide pesticide pollution continues to increase exponentially, scientists and policy makers should pay more attention to the ways pesticides alter the carbon cycle in ponds via changes in communities, as demonstrated by our results. Our results show that these predictions can be simplified by grouping pesticides into types and species into functional groups. Adopting this approach provides an opportunity to improve the efficiency of risk assessment and mitigation responses to global change.

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  4. Abstract

    Introduced hosts are capable of introducing parasite species and altering the abundance of parasites that are already present in native hosts, but few studies have compared the tolerances of native and invasive hosts to introduced parasites or identified the traits of introduced hosts that make them supershedders of non‐native parasites.

    Here, we compare the effects of a nematodeAplectana hamatospiculathat is native to Cuba but appears to be introduced to Florida on the native Floridian treefrog,Hyla femoralis, and on the Cuban treefrog (CTF),Osteopilus septentrionalis. We were particularly interested in CTFs because their introduction to Florida has led to reported declines of native treefrogs.

    In the laboratory, infection withA. hamatospiculacaused a greater loss in body mass ofH. femoralisthan CTFs despiteH. femoralisshedding fewer total worms in their faeces than CTFs. Field collections of CTFs,H. femoralis, and another native Floridian treefrog,H.squirella(Squirrel treefrog) from Tampa, FL also showed that CTFs shed more larval worms in their faeces than both native frogs when controlling for body size. Hence, the non‐native CTF is a supershedder of this non‐native parasite that is spilling over to less tolerant native treefrogs.

    Any conservation intervention to reduce the effects of CTFs on native treefrogs would benefit from knowing the traits that contribute to the invasive host being a supershedder of this parasite. Hence, we conducted necropsies on 330 CTFs to determine how host sex and body size affect the abundance ofA. hamatospicula, and two other common parasites in this species (acuariid nematodes and trematode metacercariae).

    There was a significant linear increase inA. hamatospiculaand encysted acuariids with CTF body size, but there was no detectable relationship between host body size and the intensity of metacercariae. Female CTFs were bigger, lived longer and, on average, had moreA. hamatospiculathan male CTFs.

    Synthesis and applications. These results of the study suggest that there is parasite spillover from the invasive Cuban treefrog (CTF) to native treefrogs in Florida. Additionally, at least some of the adverse effects of CTFs on native treefrogs could be caused by the introduction and amplification of this introduced parasite, and female and larger CTFs seem to be amplifying these infections more than males and smaller CTFs, respectively, suggesting that management could benefit from targeting these individuals.

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  5. Abstract

    Heterogeneities in infections among host populations may arise through differences in environmental conditions through two mechanisms. First, environmental conditions may alter host exposure to pathogens via effects on survival. Second, environmental conditions may alter host susceptibility, making infection more or less likely if contact between a host and pathogen occurs. Further, host susceptibility might be altered through acquired resistance, which hosts can develop, in some systems, through exposure to dead or decaying pathogens and their metabolites. Environmental conditions may alter the rates of pathogen decomposition, influencing the likelihood of hosts developing acquired resistance.

    The present study primarily tests how environmental context influences the relative contributions of pathogen survival and per capita transmission on host infection prevalence using the amphibian chytrid fungus (Batrachochytrium dendrobatidis; Bd) as a model system. Secondarily, we evaluate how environmental context influences the decomposition of Bd because previous studies have shown that dead Bd and its metabolites can illicit acquired resistance in hosts. We conducted Bd survival and infection experiments and then fit models to discern how Bd mortality, decomposition and per capita transmission rates vary among water sources [e.g. artificial spring water (ASW) or water from three ponds].

    We found that infection prevalence differed among water sources, which was driven by differences in mortality rates of Bd, rather than differences in per capita transmission rates. Bd mortality rates varied among pond water treatments and were lower in ASW compared to pond water.

    These results suggest that variation in Bd infection dynamics could be a function of environmental factors in waterbodies that result in differences in exposure of hosts to live Bd. In contrast to the persistence of live Bd, we found that the rates of decomposition of dead Bd did not vary among water sources, which may suggest that exposure of hosts to dead Bd or its metabolites might not commonly vary among nearby sites. Ultimately, a mechanistic understanding of the environmental dependence of free‐living pathogens could lead to a deeper understanding of the patterns of outbreak heterogeneity, which could inform surveillance and management strategies.

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  6. Abstract

    Lethal and sublethal effects of pathogens should theoretically select for host avoidance of these pathogenic organisms. Some amphibians can learn to avoid the pathogenic fungusBatrachochytrium dendrobatidis(Bd) after one infection‐clearance event.

    Here, we investigated whether four taxonomically distinct amphibians, Cuban tree frogsOsteopilus septentrionalis, southern toadsAnaxyrus(Bufo)terrestris, greenhouse frogsEleutherodactylus planirostrisand pine woods tree frogsHyla femoralis, exhibited any innate or learned avoidance of Bd on a moist substrate and, if so, what cues they used to identify the fungus.

    Cuban tree frogs, pine woods tree frogs and greenhouse frogs did not appear to exhibit detectable innate or learned avoidance of Bd. However, southern toads learned to avoid Bd after only one exposure. Southern toads avoided any treatment containing Bd metabolites but did not avoid treatments that lacked Bd metabolites even when dead zoospores were present.

    Bd metabolites appeared to be the cues that amphibians use to avoid Bd. These metabolites may have a distinct smell or may cause discomfort, which would be consistent with a classical or Pavlovian conditioning response.

    Synthesis and applications. Not all species of amphibians respond the same way to Bd exposure; some can learn to avoid Bd and the metabolites it produces, while others do not. These findings have important implications for both management practices and policy, and should be considered when developing disease models and conservation plans for amphibians.

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  7. Free, publicly-accessible full text available January 1, 2025
  8. Extreme weather events (EWEs; for example, heatwaves, cold spells, storms, floods and droughts) and non-native species invasions are two major threats to global biodiversity and are increasing in both frequency and consequences. Here we synthesize 443 studies and apply multilevel mixed-effects metaregression analyses to compare the responses of 187 non-native and 1,852 native animal species across terrestrial, freshwater and marine ecosystems to different types of EWE. Our results show that marine animals, regardless of whether they are non-native or native, are overall insensitive to EWEs, except for negative effects of heatwaves on native mollusks, corals and anemone. By contrast, terrestrial and freshwater non-native animals are only adversely affected by heatwaves and storms, respectively, whereas native animals negatively respond to heatwaves, cold spells and droughts in terrestrial ecosystems and are vulnerable to most EWEs except cold spells in freshwater ecosystems. On average, non-native animals displayed low abundance in terrestrial ecosystems, and decreased body condition and life history traits in freshwater ecosystems, whereas native animals displayed declines in body condition, life history traits, abundance, distribution and recovery in terrestrial ecosystems, and community structure in freshwater ecosystems. By identifying areas with high overlap between EWEs and EWE-tolerant non-native species, we also provide locations where native biodiversity might be adversely affected by their joint effects and where EWEs might facilitate the establishment and/or spread of non-native species under continuing global change. 
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    Free, publicly-accessible full text available December 1, 2024
  9. The pathogenic fungusBatrachochytrium dendrobatidis(Bd)is associated with drastic global amphibian declines. Prophylactic exposure to killed zoospores and the soluble chemicals they produce (Bdmetabolites) can induce acquired resistance toBdin adult Cuban treefrogsOsteopilus septentrionalis. Here, we exposed metamorphic frogs of a second species, the Pacific chorus frogPseudacris regilla, to one of 2 prophylactic treatments prior to liveBdexposures: killedBdzoospores with metabolites, killed zoospores alone, or a water control. Prior exposure to killedBdzoospores with metabolites reducedBdinfection intensity in metamorphic Pacific chorus frogs by 60.4% compared to control frogs. Interestingly,Bdintensity in metamorphs previously exposed to killed zoospores alone did not differ in magnitude relative to the control metamorphs, nor to those treated with killed zoospores plus metabolites. Previous work indicated thatBdmetabolites alone can induce acquired resistance in tadpoles, and so these findings together indicate that it is possible that the solubleBdmetabolites may contain immunomodulatory components that drive this resistance phenotype. Our results expand the generality of this prophylaxis work by identifying a second amphibian species (Pacific chorus frog) and an additional amphibian life stage (metamorphic frog) that can acquire resistance toBdafter metabolite exposure. This work increases hopes that aBd-metabolite prophylaxis might be widely effective across amphibian species and life stages.

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    Free, publicly-accessible full text available September 28, 2024
  10. Immunity changes through ontogeny and can mediate facilitative and inhibitory interactions among co-infecting parasite species. In amphibians, most immune memory is not carried through metamorphosis, leading to variation in the complexity of immune responses across life stages. To test if the ontogeny of host immunity might drive interactions among co-infecting parasites, we simultaneously exposed Cuban treefrogs ( Osteopilus septentrionalis ) to a fungus ( Batrachochytrium dendrobaditis , Bd) and a nematode ( Aplectana hamatospicula ) at tadpole, metamorphic and post-metamorphic life stages. We measured metrics of host immunity, host health and parasite abundance. We predicted facilitative interactions between co-infecting parasites as the different immune responses hosts mount to combat these infectious are energetically challenging to mount simultaneously. We found ontogenetic differences in IgY levels and cellular immunity but no evidence that metamorphic frogs were more immunosuppressed than tadpoles. There was also little evidence that these parasites facilitated one another and no evidence that A. hamatospicula infection altered host immunity or health. However, Bd, which is known to be immunosuppressive, decreased immunity in metamorphic frogs. This made metamorphic frogs both less resistant and less tolerant of Bd infection than the other life stages. These findings indicate that changes in immunity altered host responses to parasite exposures throughout ontogeny. This article is part of the theme issue ‘Amphibian immunity: stress, disease and ecoimmunology’. 
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    Free, publicly-accessible full text available July 31, 2024