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Pathogenic fungus contributes to amphibian losses in the Pacific Northwest
Abstract
Worldwide declines in amphibian populations have been the subject of numerous recent reports, and numerous hypotheses have been constructed to address the causes. There is no evidence for a single cause for the declines. We identify and describe the spread of a pathogenic fungus that appears to be largely responsible for egg mortality in one population of western toad Bufo boreas. This is the first study documenting contemporary mortality in an amphibian population with identification of the attributed pathogenic species. The fungus we identify is circumglobally distributed and we suggest that this fungal infection could also be a major contributor to other amphibian populations declines.
... It is not consensual in the literature whether Saprolegnia sp. is a "primary" or "opportunistic" pathogen since it is difficult to define whether the infection occurs before or after the death of the host; however, it can, in fact, act as both [43,48]. For example, S. australis is capable of infecting living and apparently healthy Pelophylax perezi tadpoles (personal observation). ...
... Other works reported that zoospores of S. diclina and S. ferax are capable of infecting both dead and living healthy eggs. Blaustein et al. [43] and Fernández-Benéitez et al. [48] reported healthy embryos of R. pipiens and of B. terrestris infected by S. ferax and S. diclina, respectively. In line with this, the Saprolegnia genus consists of opportunistic biotrophic or parasitic pathogens of various aquatic life stages of amphibians and of fully aquatic amphibian species. ...
... The most-reported effects focus mainly on amphibian eggs, pointing to high mortality levels, which are dependent on environmental factors and on the health conditions (or viability) of the eggs (please see Section 5.2). In addition, water molds typically infect dead or non-fertilized eggs and then start to spread, compromising all the spawn, and increasing the eggs' mortality [43]. In infected eggs, one of the signs of infection is the presence a thin layer of white fuzz over the surface of the jelly. ...
Amphibians constitute the class of vertebrates with the highest proportion of threatened species, with infectious diseases being considered among the greatest causes for their worldwide decline. Aquatic oomycetes, known as “water molds,” are fungus-like microorganisms that are ubiquitous in freshwater ecosystems and are capable of causing disease in a broad range of amphibian hosts. Various species of Achlya sp., Leptolegnia sp., Aphanomyces sp., and mainly, Saprolegnia sp., are responsible for mass die-offs in the early developmental stages of a wide range of amphibian populations through a disease known as saprolegniosis, aka, molding or a “Saprolegnia-like infection.” In this context, the main objective of the present review was to bring together updated information about saprolegniosis in amphibians to integrate existing knowledge, identify current knowledge gaps, and suggest future directions within the saprolegniosis–amphibian research field. Based on the available literature and data, an integrated and critical interpretation of the results is discussed. Furthermore, the occurrence of saprolegniosis in natural and laboratory contexts and the factors that influence both pathogen incidence and host susceptibility are also addressed. The focus of this work was the species Saprolegnia sp., due to its ecological importance on amphibian population dynamics and due to the fact that this is the most reported genera to be associated with saprolegniosis in amphibians. In addition, integrated emerging therapies, and their potential application to treat saprolegniosis in amphibians, were evaluated, and future actions are suggested.
... Lastly, S. delica was the second most isolated Saprolegnia species in water samples, and S. ferax was also occasionally captured by hempseed baits, while these two species were rarely obtained from tissue samples. Both species have previously been associated with embryonic mortality of fish and amphibians (Blaustein et al., 1994;Cao et al., 2012;Fregeneda-Grandes et al., 2007;Kiesecker et al., 2001) and were also often isolated from water (Rezinciuc et al., 2014;Sarowar et al., 2013). Our results are similar to a recent study done in Chilean salmonid farms, where S. ferax and S. delica were found both on adult and embryonic stages of salmonid fish without a clear preference for any particular developmental stage . ...
... salmonicida and other pathogens (Andreou et al., 2012;Garant et al., 2003;Johansen et al., 2011;Munday et al., 2002;Raynard et al., 2001;Thorstad and Finstad, 2018;Wallace et al., 2008). Our study illustrates this effect also for trout farms and Saprolegnia pathogens, which is relevant since saprolegniosis causes high annual economic losses in salmonid aquaculture (Hussein and Hatai, 2002;Phillips et al., 2008;van den Berg et al., 2013;van West, 2006) and has a negative impact on wild populations of salmonids and other freshwater fish, as well as other aquatic animals (Blaustein et al., 1994;Fregeneda Grandes et al., 2000;Kiesecker et al., 2001;Neitzel et al., 2004;Pickering and Willoughby, 1982;van West, 2006). For instance, Saprolegnia spp. ...
... can infect and kill crayfish specimens and it can be pathogenic towards amphibians (adult salamander and frog eggs) (Dieguez-Uribeondo et al., 1994;Gil-Turnes et al., 1989;Hirsch et al., 2008;Kiesecker and Blaustein, 1995;Kozubíková-Balcarová et al., 2013;Krugner-Higby et al., 2010;Lefcort et al., 1997). Saprolegnia species that have been introduced to the natural environment via fish restocking caused amphibian mortality (Blaustein et al., 1994;Kiesecker et al., 2001). In the last two decades, many diseases have increased in prevalence and distribution (emerging infectious diseases) (Fisher et al., 2012;Gozlan et al., 2014;van den Berg et al., 2013). ...
Oomycetes from the genus Saprolegnia are opportunistic pathogens that cause significant losses in salmonid aquaculture. Despite this, studies reporting dominant Saprolegnia species in different fish farming facilities, as well as analyses of their spreading to natural environments, are still scarce. In this study, we have for the first time identified oomycete species present in four different trout farms in Croatia. We have collected 220 oomycete isolates, both from affected tissue (46 in total: adult trout - 28, eggs - 13, and alevins - 5) and from water (174 in total: in the fish farm – 78, upstream – 50, and downstream - 46). We have used Bayesian inference to reconstruct phylogenetic relationship among the internal transcribed spacer (ITS) sequences of the collected isolates and referent strains, and determined that the isolates belonged to three different oomycete genera: Saprolegnia (64% of isolates), Pythium (35%), and Leptolegnia (1%). Saprolegnia isolates were classified into four species: S. parasitica with 53 isolates, S. australis - 52, S. delica – 25, and S. ferax – 11. Pythium and Leptolegnia isolates couldn't be identified to the species level and probably belong to so far undescribed species since their sequences didn't group with previously described species. Next, isolates from the affected tissue were mostly S. parasitica (32), while S. australis, S. delica, and S. ferax were less common (≤ 4 isolates per species). Furthermore, we used hempseed baits to capture oomycetes from water and positioned them inside the fish farms, as well as upstream (between 55 and 155 m) and downstream (between 95 and 140 m) of the fish farms. According to correspondence analysis, Saprolegnia species showed a strong association with fish farms and downstream locations, while upstream locations were associated with Pythium species, highlighting a possible role of trout farms as a source of spreading Saprolegnia species into the environment.
... Fungal and water moulds impose different levels of health risk on organisms that colonize water bodies, and have been recognized as important pathogens of amphibians since the midtwentieth century (e.g., from Bragg and Bragg 1958 to Ghirardi et al. 2018). These infections have been identified as the cause of massive mortality in amphibians, principally affecting the immobile and more susceptible stages of the amphibian cycle such as eggs and embryos (Blaustein et al. 1994). Infection by the water mould genus Saprolegnia Nees (Oomycota, Saprolegniales, Saprolegniaceae) has been associated with the massive death of eggs and embryos of the Western Toad (Anaxyrus boreas (Baird and Girard, 1852)), Natterjack Toad (Epidalea calamita (Laurenti, 1768)), Cascades Frog (Rana cascadae Slater, 1939), and Common Frog (Rana temporaria Linnaeus, 1758) (Banks and Beebee 1988;Beattie et al. 1991;Blaustein et al. 1994), and increased mortality of Menwig Frog (Physalaemus albonotatus (Steindachner, 1864)) embryos (Ghirardi et al. 2018). ...
... These infections have been identified as the cause of massive mortality in amphibians, principally affecting the immobile and more susceptible stages of the amphibian cycle such as eggs and embryos (Blaustein et al. 1994). Infection by the water mould genus Saprolegnia Nees (Oomycota, Saprolegniales, Saprolegniaceae) has been associated with the massive death of eggs and embryos of the Western Toad (Anaxyrus boreas (Baird and Girard, 1852)), Natterjack Toad (Epidalea calamita (Laurenti, 1768)), Cascades Frog (Rana cascadae Slater, 1939), and Common Frog (Rana temporaria Linnaeus, 1758) (Banks and Beebee 1988;Beattie et al. 1991;Blaustein et al. 1994), and increased mortality of Menwig Frog (Physalaemus albonotatus (Steindachner, 1864)) embryos (Ghirardi et al. 2018). It has also been related to a reduction in hatching time (a mechanism of evading the infection risk of immobile and more susceptible stages) and, consequently, to a variation in hatching morphology (Bragg and Bragg 1958;Blaustein et al. 1994;Fernández-Benéitez et al. 2008;Perotti et al. 2013). ...
... Infection by the water mould genus Saprolegnia Nees (Oomycota, Saprolegniales, Saprolegniaceae) has been associated with the massive death of eggs and embryos of the Western Toad (Anaxyrus boreas (Baird and Girard, 1852)), Natterjack Toad (Epidalea calamita (Laurenti, 1768)), Cascades Frog (Rana cascadae Slater, 1939), and Common Frog (Rana temporaria Linnaeus, 1758) (Banks and Beebee 1988;Beattie et al. 1991;Blaustein et al. 1994), and increased mortality of Menwig Frog (Physalaemus albonotatus (Steindachner, 1864)) embryos (Ghirardi et al. 2018). It has also been related to a reduction in hatching time (a mechanism of evading the infection risk of immobile and more susceptible stages) and, consequently, to a variation in hatching morphology (Bragg and Bragg 1958;Blaustein et al. 1994;Fernández-Benéitez et al. 2008;Perotti et al. 2013). ...
Water moulds are pathogens of amphibian eggs and embryos. However, little is known about oxidant or antioxidant status of amphibians in response to stress caused by water moulds. We exposed embryo stages of two-coloured oval frogs Elachistocleis bicolor (Guérin-Méneville, 1838) to Saprolegnia -like sp. water mould in order to explore homeostatic adjustments by the shifting of oxidative stress markers. We also tested whether water mould infection affected survivorship and hatching time and morphology of hatching embryos. We found that Saprolegnia -like sp. is a genuine stressor and substantially altered the physiological state of E. bicolor embryos. Among antioxidant defences, superoxide dismutase (SOD) and glutathione S-transferase (GST) activity increased in embryos exposed to Saprolegnia -like sp. However, no difference in lipid peroxidation levels was found between treatments, which might indicate that SOD and GST activation could be enough to prevent oxidative damage. Finally, we found higher mortality and number of malformations in the water mould treatment. We showed the stressful effect of water moulds on amphibian embryos, evidenced by the activation of their antioxidant system, and reveal the importance of considering physiological stress markers as key information when studying the potential consequences of disease outbreaks in the ecology and conservation of amphibians.
... Members of the genus Saprolegnia (hereafter collectively referred to as Saprolegnia), an oomycete, are one of the pathogens implicated in massive amphibian mortality events (Banks & Beebee 1988, Beattie et al. 1991, Blaustein et al. 1994, Kiesecker & Blaustein 1995. Saprolegnia is known to kill larvae of Rana aurora (Romansic et al. 2006) and newly metamorphosed R. cascadae (Romansic et al. 2007) and has helped drive local extirpations of R. pipiens and Anaxyrus terrestris in North America (Bragg & Bragg 1958, Bragg 1962. ...
... Beattie et al. 1991, Kiesecker & Blaustein 1995, Kiesecker et al. 2001a. For example, UV-B radiation may weaken the defense system of am phibians, resulting in increased vulnerability to pathogens such as Saprolegnia (Blaustein et al. 1994, Kiesecker & Blaustein 1995. Amphibian vulnerability to pathogens may also increase with water temperature, given the positive relationship between water temperature and the growth of Saprolegnia on anuran eggs (e.g. ...
... Our results showed that the prevalence of an undescribed strain of the pathogenic oomycete species Saprolegnia ferax was associated with an increased mortality in Bufo gargarizans eggs, as documented in other amphibians (Bragg & Bragg 1958, Bragg 1962, Blaustein et al. 1994, Kiesecker & Blaustein 1995, Perotti et al. 2013. While Saprolegnia presence in 2016 had a significant impact on the breeding activity of the subsequent year, no impact on the breeding activity of 2018 was found, and we cannot conclude on the impact of Saprolegnia on the subsequent breeding season of B. gargarizans at a site. ...
Pathogenic water molds have significant impacts on many species, especially amphibians. Saprolegnia is a pathogenic oomycete restricted to aquatic and moist habitats, and its presence is strongly linked to the abundance of amphibians and fishes. We investigated the influence of Saprolegnia presence on egg mortality and egg occurrence under varying environmental conditions in the Asiatic toad (Bufo gargarizans) at 27 breeding sites in the Republic of Korea. We then assessed the impact of Saprolegnia on the presence of B. gargarizans at the 27 sites surveyed weekly during B. gargarizans’ breeding season for three consecutive years. Water molds were identified as belonging to an undescribed Saprolegnia ferax strain with molecular tools. We demonstrated that the presence of Saprolegnia was positively associated with higher water conductivity and ponds. In addition, while Saprolegnia prevalence was associated with a reduction in B. gargarizans breeding activity and breeding success, we could not determine the impact of Saprolegnia presence on the subsequent breeding seasons. Our study highlights the potential negative effects of Saprolegnia on amphibian reproduction, although additional research is necessary to determine the relationship between Saprolegnia, its hosts, and the impacts of habitat loss on amphibians.
... Fish may be both co petitors and predators of amphibians, depending on life cycle stage (Bristow, 1991). T ey have been implicated in declines of western amphibians both as predators (Bradford, 1989) and as disease vectors (Blaustein et al., 1994b). Stocking of predatory fishes in p nds previously free of fish undoubtedly leads to a change in the amphibian community b cause many amphibians are defenseless against fish predators. ...
... A pathogenic fungus has been implicated rece dy in the decline and disappearance of Bufo boreas in the western United States (Blaustein et ., 1994b). The fungus (Saprolegnia [erax) is circumglobal in distribution and commonly on fish. ...
... However, fish are not native to the high mountain habitats occupied by B. orear, and the pathogen is thought to have been introduced when trout and salmon were tocked in high mountain streams and lakes. The same fungus has extirpated other frog pop ations in the U.S. and Europe (for a review of this topic see Blaustein et al., 1994b). Althou the extent of amphibian fungal infections is unknown in the Southeast, every egg mass ( na sp.) ...
... In oviparous amphibians, the use of an external jelly coating to surround their embryos functions as a protective barrier to reduce disease, desiccation and to a limited ex tent, predation. Despite this, a range of pathogens have been documented in both captive and wild am phi bian embryos (Green & Converse 2005) including viruses (Tweedell & Granoff 1968, McKinnell 1973, bacteria (Bishop et al. 2021, Khalifa et al. 2021, ciliates (Gilbert 1942), protists (Schuetz et al. 1978, Holz et al. 2015, algae (Gilbert 1942, Bachmann et al. 1986, Kim et al. 2014) and fungi (Forester 1979, Villa 1979, Blaustein et al. 1994, Gomez-Mestre et al. 2006, Banning et al. 2008. Although representative across pathogen taxa, this list is likely an underrepresentation of the true number of pathogenic microorganisms that impact amphibian embryos. ...
... In diseased embryos, fungal infections are often considered secondary invasions, rather than the primary cause of mortality (Blaustein et al. 1994). It is possible that developmental errors may weaken the defence system of an embryo (e.g. ...
The Critically Endangered southern corroboree frog Pseudophryne corroboree is dependent upon captive assurance colonies for its continued survival. Although the captive breeding programme for this species has largely been successful, embryonic mortality remains high (40-90% per year). This study aimed to investigate the causes of mortality in P. corroboree embryos in the captive collection at Melbourne Zoo. During the 2021 breeding season, we investigated 108 abnormal embryos to determine the impact of infections and anatomical deformities on survival and used culture and molecular methods to identify microbes. Overall, 100% of abnormal embryos had fungal infections, and of these, 41.6% also had anatomical deformities. The mortality rate in abnormal embryos was 89.8%; however, we detected no difference in survival in any of the 3 observed fungal growth patterns or between deformed and non-deformed embryos. Sanger sequencing of the ITS region identified fungal isolates belonging to the genus Ilyonectria, the first record in a vertebrate host, and another as a Plectosphaerella sp., which is the first record of infection in an embryo. Dominant bacteria identified were of the genera Herbaspirillum and Flavobacterium; however, their role in the mortality is unknown. Fungal infection and deformities have a significant impact on embryo survival in captive-bred P. corroboree. In a species which relies on captive breeding, identifying and reducing the impacts of embryonic mortality can inform conservation efforts and improve reintroduction outcomes.
... Water molds infecting amphibians and functioning as naturally occurring stressors include many facultative pathogens such as species of the genera Achlya, Leptolegnia, Aphanomyces, and Saprolegnia (Gleason et al. 2014), all of which have been recognized as important pathogens of amphibians since the mid-20 th Century (e.g., from Bragg 1958to Bovo et al. 2016. Infection by Saprolegnia spp. is associated with reduced hatching time and higher mortality rates of many amphibian embryos (Bragg 1958(Bragg , 1962Blaustein et al. 1994;Fernández-Benéitez et al. 2011;Perotti et al. 2013). Decreased hatching time shortens the developmental period of embryos and reduces mass at metamorphosis, both of which have important implications for anuran population dynamics Uller et al. 2009;Perotti et al. 2013). ...
... To date, several studies have demonstrated the effects of infection by water molds (Oomycetes) on survival and development in amphibians (Blaustein et al. 1994;Fernández-Benéitez et al. 2008Ruthig 2009;Perotti et al. 2013), linking fungal-like infections with mortality or shortening of hatching time Touchon et al. 2006;Perotti et al. 2013). However, no studies have determined whether or not amphibian embryos under the risk of Oomycetes infection trigger antioxidant activation. ...
Infections by water molds of the genus Saprolegnia (Oomycetes) have been associated with the death of eggs and embryos in many anuran species; however, how water molds induce physiological responses in early and susceptible developmental stages of anurans is poorly known. To assess whether or not embryos of Physalaemus albonotatus (immobile and susceptible life stages) respond to Oomycetes infection, we performed a 4-d experiment exposing early stage embryos to the water mold Saprolegnia-like sp. We assessed mortality, hatching time, and oxidative stress (antioxidant enzyme activities and lipid peroxidation levels). Presence of water molds in infected embryos was not evident to the naked eye until 1 to 1.5 d after inoculation. Mortality was significantly higher in the water mold treatment than in the control treatment. Embryos exposed to Saprolegnia-like sp. hatched 24 h earlier than those in control treatment. Among enzymatic activities, only catalase enzyme showed a significant depletion in embryos exposed to water molds compared to control groups. These results emphasize the need to explore oxidative stress markers along with embryonic development at key stages, focusing on those early stages where hatching is induced by water molds infection.
... Abiotic stresses affect the timing of hatching as predicted (reviewed in Martin 1999), and variation in hatching stage in response to egg and larval predators has recently been discovered (Sih and Moore 1993, Warkentin 1995. Pathogens also cause substantial mortality of eggs and larvae (e.g., Banks and Beebee 1988, Blaustein et al. 1994, Williamson and Bull 1994; however, their effects on the timing of hatching have not been examined. Pathogens have important effects on host life history, behavior, and population dynamics (Dobson and Hudson 1986, Minchella and Scott 1991, Dobson and Crawley 1994, Poulin 1994. ...
... Pathogens, including several species of fungi and water molds, can pose a substantial risk to amphibian embryos (Blaustein et al. 1994, Czeczuga et al. 1998). In many natural amphibian populations, fungal infections of eggs impose moderate levels of mortality (e.g., Forester 1979, Simon 1983, Kam et al. 1996. ...
Pathogens can cause substantial mortality of amphibian eggs. If the timing of hatching is phenotypically plastic, embryos could escape from otherwise lethal infections by hatching early. We tested this with the arboreal eggs of red-eyed treefrogs, Agalychnis callidryas. A filamentous ascomycete (Dothideales: Phaeosphaeriaceae) was present on ∼7% of egg clutches collected from a pond in the rain forest in Panama and, when present, killed 40% of the eggs, on average. Inoculation experiments confirmed that the fungus attacked and killed healthy embryos, establishing that this fungus is a pathogen of A. callidryas eggs. As predicted from life history theory, embryos hatched earlier from both naturally infected and inoculated clutches than from fungus-free control clutches. Within infected clutches, live embryos in contact with fungal hyphae hatched before those embryos not in contact with the fungus. Accelerated hatching allowed embryos to survive that otherwise would have been killed, and tadpoles hatched from infected clutches were themselves uninfected. Red-eyed treefrog embryos also hatch early if attacked by predators, apparently in response to vibratory cues. Because fungal infection provides no vibratory stimuli, embryos must respond to different cues in fungus-induced hatching than in predator-induced hatching. The behavioral decision of when to hatch is complex and merits further investigation. Our study indicates that pathogens can influence the timing of life history transitions, as do other stage-specific risks.
Pathogens can cause substantial mortality of amphibian eggs. If the timing of hatching is phenotypically plastic, embryos could escape from otherwise lethal infections by hatching early. We tested this with the arboreal eggs of red-eyed treefrogs, Agalychnis callidryas. A filamentous ascomycete (Dothideales: Phaeosphaeriaceae) was present on ∼7% of egg clutches collected from a pond in the rain forest in Panama and, when present, killed 40% of the eggs, on average. Inoculation experiments confirmed that the fungus attacked and killed healthy embryos, establishing that this fungus is a pathogen of A. callidryas eggs. As predicted from life history theory, embryos hatched earlier from both naturally infected and inoculated clutches than from fungus-free control clutches. Within infected clutches, live embryos in contact with fungal hyphae hatched before those embryos not in contact with the fungus. Accelerated hatching allowed embryos to survive that otherwise would have been killed, and tadpoles hatched from infected clutches were themselves uninfected. Red-eyed treefrog embryos also hatch early if attacked by predators, apparently in response to vibratory cues. Because fungal infection provides no vibratory stimuli, embryos must respond to different cues in fungus-induced hatching than in predator-induced hatching. The behavioral decision of when to hatch is complex and merits further investigation. Our study indicates that pathogens can influence the timing of life history transitions, as do other stage-specific risks.
... These organisms cause huge losses in aquaculture worldwide and are also considered responsible for the decline in populations of wild fish and amphibians (1)(2)(3)(4)(5). The host range of these organisms includes various fish species, amphibians, and crustaceans (6)(7)(8). The disease caused by this organism, known as Saprolegniasis, is characterized by white or gray cottonlike mycelial growth at the site of infection. ...
Saprolegniosis is one of the most catastrophic oomycete diseases of freshwater fish caused by the members of the genus Saprolegnia. The disease is responsible for huge economic losses in the aquaculture industry worldwide. Until 2002, Saprolegnia infections were effectively controlled by using malachite green. However, the drug has been banned for use in aquaculture due to its harmful effect. Therefore, it has become important to find an alternate and safe anti-oomycete agent that is effective against Saprolegnia. In this study, we investigated the anti-oomycete activity of chlorhexidine gluconate (CHG) against Saprolegnia. Before in vitro evaluation, molecular docking was carried out to explore the binding of CHG with vital proteins of Saprolegnia, such as S. parasitica host-targeting protein 1 (SpHtp1), plasma membrane ATPase, and TKL protein kinase. In silico studies revealed that CHG binds with these proteins via hydrogen bonds and hydrophobic interactions. In an in vitro study, the minimum inhibitory concentration (MIC) and minimum fungicidal concentration (MFC) of CHG against S. parasitica were found to be 50 mg/L. Further, it was tested against S. australis, another species of Saprolegnia, and the MIC and MFC were found to be 100 and 200 mg/L, respectively. At 500 mg/L of CHG, there was complete inhibition of the radial growth of Saprolegnia hyphae. In propidium iodide (PI) uptake assay, CHG treated hyphae had bright red fluorescence of PI indicating the disruption of the cell membrane. The results of the present study indicated that CHG could effectively inhibit Saprolegnia and hence can be used for controlling Saprolegniasis in cultured fish.
... Infections or other stresses may also make amphibians more susceptible to other pathogens. For example, a common water mold (Saprolegnia ferax) that is known to attack fish is responsible for mortality of up to 95 per cent of boreal toad embryos in Oregon (Blaustein et al. 1994b). ...
... Recent studies have also shown that one of the most important amphibian pathogens, the chytrid fungus Batrachochytrium dendrobatidis that has caused dramatic amphibian declines globally (Fisher and Garner 2020) is mitigated by the presence of micro-eukaryotes predating on its zoospores (Schmeller et al. 2014). Protozoan micro-predators (Yassin and El-Said 2011) and probiotic bacteria (Chauhan and Singh 2019) have also proven effective in reducing the growth of Saprolegnia water molds that are known to cause extended mortality of amphibian eggs (Blaustein et al. 1994;Gomez-Mestre et al. 2006). Recently, Jurga et al. (2020) used a DNA metabarcoding approach to demonstrate that fluid from the capsular chambers of A. maculatum clutches contained communities of micro-eukaryotes that represented a subset of the aquatic taxa present in free water at the respective sampling sites. ...
Amphibian clutches are colonized by diverse but poorly studied communities of micro-organisms. One of the most noted ones is the unicellular green alga, Oophila amblystomatis , but the occurrence and role of other micro-organisms in the capsular chamber surrounding amphibian clutches have remained largely unstudied. Here, we undertook a multi-marker DNA metabarcoding study to characterize the community of algae and other micro-eukaryotes associated with agile frog ( Rana dalmatina ) clutches. Samplings were performed at three small ponds in Germany, from four substrates: water, sediment, tree leaves from the bottom of the pond, and R. dalmatina clutches. Sampling substrate strongly determined the community compositions of algae and other micro-eukaryotes. Therefore, as expected, the frog clutch-associated communities formed clearly distinct clusters. Clutch-associated communities in our study were structured by a plethora of not only green algae, but also diatoms and other ochrophytes. The most abundant operational taxonomic units (OTUs) in clutch samples were taxa from Chlamydomonas , Oophila , but also from Nitzschia and other ochrophytes. Sequences of Oophila “Clade B” were found exclusively in clutches. Based on additional phylogenetic analyses of 18S rDNA and of a matrix of 18 nuclear genes derived from transcriptomes, we confirmed in our samples the existence of two distinct clades of green algae assigned to Oophila in past studies. We hypothesize that “Clade B” algae correspond to the true Oophila , whereas “Clade A” algae are a series of Chlorococcum species that, along with other green algae, ochrophytes and protists, colonize amphibian clutches opportunistically and are often cultured from clutch samples due to their robust growth performance. The clutch-associated communities were subject to filtering by sampling location, suggesting that the taxa colonizing amphibian clutches can drastically differ depending on environmental conditions.
... In contrast, in discrete individuals such as adult fish, hyphal spread is more likely to increase the extent of infection on a single individual, and so may cause only a partial reduction in fitness. The consequences from a population perspective may be profound because spread between caddisfly eggs directly increases mortality, as is also seen with infections in fish and amphibian eggs (Blaustein et al., 1994;Thoen et al., 2011;van den Berg et al., 2013). ...
• Disease can be a powerful driver of population and community dynamics, as well as evolutionary processes. Disease is also emerging at increasing rates, resulting in massive impacts on populations, communities, and ecosystems. However, assessing these impacts requires foundational knowledge of disease agents and hosts, which is often lacking, particularly in aquatic insects.
• We describe a recent disease outbreak in caddisflies, suggesting potential consequences for population and community dynamics of the host. We use a series of complementary studies to develop a cohesive foundation of information about this disease, including identification using genomic methods, observational prevalence studies, laboratory experiments to establish transmissibility and fitness consequences, and laboratory and field investigations to infer transmission mechanisms.
• We identified the infection as being caused by the oomycete Saprolegnia—the first time this parasite has been noted in insect eggs. Prevalence surveys found high prevalence (up to 36%) with variation across space, time, and host species. We demonstrated increasing egg mortality with increasing infection within an egg mass (every 10% increase in infection rate doubles odds of mortality), thereby confirming disease. We established transmissibility and show that transmission occurs through both direct contact with infected egg masses and from background sources, which probably interact to create complex patterns of disease.
• Taken together, our findings show that conditions necessary for population and community consequences are present. Specifically, increased mortality rates almost certainly occurred during the outbreak, yielding lower larval numbers and potentially altering community interactions. Transmission by contact between egg masses combined with observed species‐specific prevalence suggest shifts in the relative performance of different species because of interactions between host and parasite life histories.
• Outside extreme examples such as chytrid fungus, disease has traditionally received less interest than resource competition or predation in community ecology, although disease ecology is advancing rapidly. One major hurdle is a lack of foundational knowledge characterising disease processes in natural communities, particularly in aquatic insects. Our findings highlight the importance of investigating diseases in insect eggs and provide the foundation for further investigations of how these processes play out at the population and community scale.
... In fact, similar to what occurs in other vertebrate classes, some of the bacteria found in frog's skin act as symbionts, enhancing hosts tolerance to pathogens [3,[14][15][16][17][18][19][20][21]. In the context 2 of 13 of the global amphibians' crisis, pathogens are one of the major threats to their natural populations [22][23][24][25][26]. The effectiveness of skin bacteria in protecting against pathogens has already been proved by both in vitro and in vivo studies [15,16,27,28]. ...
(Diogo Neves Proença and Emanuele Fasola contributed equally to this work).
Microorganisms that live in association with amphibian skin can play important roles in protecting their host. Within the scenarios of global change, it is important to understand how environmental disturbances, namely, metal pollution, can affect this microbiota. The aim of this study is to recognize core bacteria in the skin cultivable microbiota of the Perez frog (Pelophylax perezi) that are preserved regardless of the environmental conditions in which the frogs live. The characterization of these isolates revealed characteristics that can support their contributions to the ability of frogs to use metal impacted environments. Frog’s skin swabs were collected from P. perezi populations that inhabit a metal-polluted site and three reference (non-metal polluted) sites. Bacterial strains were isolated, identified, and subjected to an acid mine drainage tolerance (AMD) test, collected upstream from a site heavily contaminated with metals, and tested to produce extracellular polymeric substances (exopolysaccharide, EPS). All frog populations had Acinetobacter in their cutaneous cultivable microbiota. Significant growth inhibition was observed in all bacterial isolates exposed to 75% of AMD. EPS production was considered a characteristic of several isolates. The data obtained is a preliminary step but crucial to sustain that the cultivable microbiota is a mechanism for protecting frogs against environmental contamination.
... Numerous genera of water molds contain species known to be pathogenic to amphibians: Saprolegnia, Leptolegnia, Achlya, Aphanomyces and Pythium (Ault et al. 2012;Ruthig and Provost-Javier 2012). Infections by common species of Saprolegnia such as S. ferax, S. parasitica and S. diclina across North America, Europe and Asia are particularly detrimental to the survival of amphibians at early life stages (Lefcort et al. 1997;Robinson, Griffiths and Jeffries 2003;Fernández-Benéitez et al. 2008;Romansic et al. 2009;Ruthig 2009;Groffen et al. 2019) and have been implicated as possibly contributing to declining numbers of some species (Blaustein et al. 1994;Green 1999). ...
Amphibian embryos often suffer increased mortality and altered hatching when exposed to road deicing salt runoff or pathogens such as water molds. However, the combined effects of such contaminants on embryos remains understudied. To test how pond salinization interacts with water mold (Saprolegnia sp.) to influence hatching timing and survival, we first measured pond water conductivity and temperature and quantified the prevalence and abundance of water mold in nature. Second, we experimentally placed wood frog (Rana sylvatica) embryos in the presence or absence of water mold, crossed with environmentally realistic salt concentrations (100 μS, 300 μS, or 600 μS). Lastly, we quantified growth and colonization of water mold in this range of salinities. Our results demonstrate that salt had synergistic effects with water mold exposure that affected hatching time, though water mold had less of an effect at higher salinities. Water mold significantly reduced egg survival whereas salt did not. Higher salinities also increased water mold growth and colonization on new substrates. These results indicate that road salt runoff may enhance colonization of amphibian eggs by water molds increasing mortality and premature hatching of surviving embryos, which may in turn have detrimental effects on amphibian communities.
... Seasonal and spatial variation may raise questions about increased exposure to UV-B as a cause of amphibian declines, but are there other consequences to variation in the timing of breeding? Extreme temperatures can be lethal to amphibian embryos, and temperature stress is as plausible a hypothesis as increased UV-B to explain episodes of high mortality of B. boreas observed in Oregon (Blaustein et al. 1994, Kiesecker et al. 2001. Mean temperatures did not differ among the treatments at different depths in the Oregon experiment, but temperature ranges were not reported (Kiesecker et al. 2001). ...
... Most species from the oomycete genus Saprolegnia are opportunistic parasites (Plumb, 1999) that cause the disease saprolegniasis in various fish species (van West, 2006), amphibians (Blaustein et al., 1994), crustaceans (Diéguez-Uribeondo et al., 1994), and other aquatic animals (Fernandez-Beneitez et al., 2011). The virulent strains of Saprolegnia parasitica infect eggs, juvenile, and adult fish, leading to important losses in fish farms worldwide (van West, 2006). ...
Many Stramenopile species belonging to oomycetes from the genus Saprolegnia infect fish, amphibians, and crustaceans in aquaculture farms and natural ecosystems. Saprolegnia parasitica is one of the most severe fish pathogens, responsible for high losses in the aquaculture industry worldwide. Most of the molecules reported to date for the control of Saprolegnia infections either are inefficient or have negative impacts on the health of the fish hosts or the environment resulting in substantial economic losses. Until now, the whole proteome of S. parasitica has not been explored for a systematic screening of novel inhibitors against the pathogen. The present study was designed to develop a consensus computational framework for the identification of potential target proteins and their inhibitors and subsequent experimental validation of selected compounds. Comparative analysis between the proteomes of Saprolegnia, humans and fish species identified proteins that are specific and essential for the survival of the pathogen. The DrugBank database was exploited to select food and drug administration (FDA)-approved inhibitors whose high binding affinity to their respective protein targets was confirmed by computational modeling. At least six of the identified compounds significantly inhibited the growth of S. parasitica in vitro. Triclosan was found to be most effective with a minimum inhibitory concentration (MIC100) of 4 μg/ml. Optical microscopy showed that the inhibitors affect the morphology of hyphal cells, with hyper-branching being commonly observed. The inhibitory effects of the compounds identified in this study on Saprolegnia’s mycelial growth indicate that they are potentially usable for disease control against this class of oomycete pathogens. Similar approaches can be easily adopted for the identification of potential inhibitors against other plant and animal pathogenic oomycete infections.
... The loose arrangement of branched fibres is consistent with the morphology of fungal hyphae [16][17][18] , and the varying length and the fixed diameter (around 10μm) also fits the characteristics of hyphae ( Fig. 4B and C). Fungal infections (such as water moulds) can occur on modern amphibian eggs and affect the hatching rate [17][18][19][20][21] . The condition in the amber specimen is similar to that observed in infected modern samples 17,20 . ...
The eggs of fish, amphibians, and many invertebrates are soft, delicate structures that are only rarely preserved in the fossil record. Here we report egg masses preserved as inclusions in mid-Cretaceous amber deposits of Myanmar. Of five specimens recovered, three of the egg masses probably pertain to insects, but the other two appear different. One mass is composed of relatively stiff eggs that retain their shape throughout the mass and may be linked by mucoid strands. This morphology resembles that of some terrestrial molluscs. The second mass is composed of softer eggs that have compressed one another so that their shapes are strongly distorted within the mass. These eggs most closely resemble those of amphibians. Given the forest environment reconstructed for the amber locality, the eggs were presumably attached on or close to the resin producing tree.
... Stressors can interact by imposing additional energetic demands on individuals (Van Der Veen 2005;Warne et al. 2011;Matzelle et al. 2015) and leading to deteriorating condition of the individual and interference with important physiological pathways (Relyea and Mills 2001;Relyea 2003;Relyea and Edwards 2010), or by necessitating incompatible adaptive responses (Van Der Veen 2005;Lakowitz et al. 2008;Kelly et al. 2016). These interactions can substantially influence productivity or mortality (Teplitsky and Laurila 2007;Steinberg 2012), potentially fuelling population declines (Blaustein et al. 1994;Relyea and Edwards 2010). Importantly, when multiple stressors interact, complex and often unpredictable consequences that deviate substantially from individual effects may arise (Relyea 2003;Relyea and Edwards 2010;Marino and Werner 2013). ...
There is increasing interest in how animals respond to multiple stressors, including potential synergistic or antagonistic interaction between pathogens and perceived predation risk (PPR). For prey that exhibit phenotypic plasticity, it is unclear whether infection and PPR affect behaviour and morphology independently, or in an antagonistic or synergistic manner. Using a 2 × 2 factorial experiment involving green frog (Lithobates clamitans) tadpoles exposed to ranavirus (FV3) and larval dragonflies (Anax spp.), we assessed whether anti-predator responses were affected by infection. We found that activity and feeding were reduced additively by both stressors. Body mass of tadpoles from FV3-exposed tanks was lighter relative to control and PPR-only tanks, while metabolism was comparable across treatments. We found that FV3 exposure compromised morphometric responses to PPR in an antagonistic manner: tadpoles exposed to both treatments had restricted changes in tail depth compared to those receiving singular treatment. We conclude that multiple stressors can have complex and substantive effects on organisms, and that interactions between stressors may yield a range of responses depending on the level of exposure and sensitivity of the organism. Additional work should more fully determine mechanisms underlying the complex interplay between infection and predation risk, across a range of environmental conditions.
... Offspring mortality caused by water mould infection (family Saprolegniaceae) is a serious issue in numerous aquatic organisms including pond-and stream-breeding amphibians including A. japonicus (Smith, 1907;Suzuki, 1984;Blaustein, Hokit & O'Hara, 1994;Sarowar et al., 2013). Some amphibians possess unique ways to protect their offspring from water mould infection. ...
Parental care in salamanders is thought to be simple and typically limited to female egg attendance. No elaborate preoviposition parental care had been described from salamanders. Recent studies revealed complex care behaviours by male Japanese giant salamanders (Andrias japonicus), a fully aquatic, secretive species with external fertilization. These studies emphasize behavioural convergence in paternal care between some of the fish species and the giant salamanders. The fish examples further imply the possibility that males of A. japonicus provide preoviposition parental care in the form of nest cleaning and building. We tested this possibility and also predicted that cleaning effort by a male salamander, if exists, would increase as it approaches the spawning event. Prior to the breeding season, large males (i.e. den masters) of A. japonicus occupy and guard suitable burrows well-hidden along the stream bank. In the falls of 2012, 2013 and 2015, we videotaped and examined a single den master's pre- and postoviposition behaviours at Asa Zoological Park in Hiroshima, Japan. The den master repeatedly exhibited vigorous movements of front and hind limbs in a paddling motion at the bottom of the nest every day for the three separate years. The cleaning effort by the den master lineally increased as the spawning event approached, after which the den master completely ceased cleaning. With the cleaning behaviour, the den master made the den filled with debris including leaves and twigs buried in the sand. The floating debris was subsequently removed by the water current flowing through the nest. Water mould infection is a major cause of offspring mortality of aquatic amphibians including A. japonicus. By reducing the amount of organic matter that provides food sources for water mould, the nest cleaning likely reduces the risk of water mould infection among the offspring, serving as an important preoviposition parental care.
... Captive harbor seals (Phoca vitulina) fed fish from the polluted waters of the Baltic Sea developed impaired T-cell mediated immune function accompanied by suggestions of increased bacterial infection (74). Similarly, Blaustein et al. (75) suggest that amphibians may be especially susceptible to infection by Saprolignia, a circumglobally distributed pathogenic fungus, when under stress from competitive situations or adverse environmental conditions including pollution, loss of habitat, acidification, or increased levels of ultraviolet-B (UV-B) radiation. ...
... However, the observations that Bufo eggs develop fungal infections following handling (C Carey, unpublished observation) suggest that eggs and embryos are protected until hatching by one or more defense mechanisms in intact and undisturbed jelly. Recent observations show that fungal infections (Saprolegniaferax) of eggs resulted in almost complete reproductive failure of one population of boreal toads (Bufo boreas boreas) in the Cascades of Oregon (19). It is unclear whether such infections result from recent introduction of fish carrying the fungus into breeding areas of these toads, or whether environmental factors are reducing protective qualities of the jelly capsule against such pathogens. ...
... Una vez en contacto con la puesta, este protozoario afecta la membrana vitelina y posteriormente el embrión o larva del anfibio en periodo de organogénesis, retrasando su desarrollo, induciendo la eclosión temprana y finalmente matándolo en la mayoría de los casos. Algunos anfibios afectados por este organismo son Anaxyrus boreas, Pleurodema thaul, Rana cascadae, Rana aurora y Pseudacris regilla (Blaustein et al., 1994;Kiesecker y Blaustein, 1999;Romansic et al., 2009;Perotti et al., 2013). ...
This is a review paper that addresses the issue of macroscopic anomalies in anuran amphibian larvae. Currently, the cause of many anomalies in amphibians is known totally or partially, such as those caused by genetic factors (mutations, albinism and cauda bifida), by infectious agents (viruses, bacteria, fungi, protozoa and helminth parasites), by environmental factors (ultraviolet radiation, magnetism, temperature and predation) and by exposure to pollutants (endocrine disruptors and heavy metals), however, there are also anomalies whose cause remains unknown (p anomaly and weak limbs syndrome). Among the macroscopic anomalies mentioned in this article are the curvature of the spine, abnormalities in extremities, edema, skin and pigmentation problems, eye abnormalities and delayed growth. In the larval stage, the spectrum of anomalies is greater than in the adult stage, because in this stage the anuran amphibians are more vulnerable to different environmental and anthropogenic factors, and many of them will not reach the adult stage. The presence of macroscopic anomalies in larvae of anuran amphibians can give us information about the health status of a population or species, finding out the cause of these anomalies could help to generate conservation strategies for this biological group and minimize the loss of its biodiversity.
... The presence of a reservoir host like R. catesbeiana (or others [75]) could lead to local population declines due to disease, even well beyond the initial emergence of Bd [60]. High risk areas include many watersheds in the Cascade Range in the Pacific Northwest, the California coastal ranges, and the Sierra Nevada Mountains, all areas where native amphibians have declined [15,[76][77][78]. ...
Batrachochytrium dendrobatidis (Bd), a causal agent of the amphibian fungal skin disease chytridiomycosis, has been implicated in the decline and extinction of over 200 species worldwide since the 1970s. Despite almost two decades of research, the history of Bd and its global spread is not well understood. However, the spread of the Global Panzootic Lineage of Bd (Bd-GPL), the lineage associated with amphibian die-offs, has been linked with the American bullfrog (Rana [Aqurana] catesbeiana) and global trade. Interestingly, R. catesbeiana is native to the eastern U.S., where no Bd-related declines have been observed despite Bd’s presence since the late 1800s. In contrast Bd has been found to have emerged in California and Mexico in the 1960s and 1970s, after which epizootics (i.e., epidemics in wildlife) ensued. We hypothesize that Bd-GPL spread from the eastern U.S. with the introduction of R. catesbeiana into the western US, resulting in epizootics and declines of native host species. Using museum records, we investigated the historical relationship between R. catesbeiana and Bd invasion in the western US and found that R. catesbeiana arrived in the same year or prior to Bd in most western watersheds that had data for both species, suggesting that Bd-GPL may have originated in the eastern US and R. catesbeiana may have facilitated Bd invasion in the western US. To predict areas with greatest suitability for Bd, we created a suitability model by integrating habitat suitability and host availability. When we incorporated invasion history with high Bd suitability, we found that watersheds with non-native R. catesbeiana in the mountain ranges of the West Coast have the highest disease risk. These findings shed light on the invasion history and disease dynamics of Bd in North America. Targeted historical surveys using archived specimens in natural history collections and present-day field surveys along with more localized, community-level studies, monitoring, and surveillance are needed to further test this hypothesis and grow our understanding of the disease ecology and host-pathogen dynamics of Bd.
... Saprolegnia parasitica causes saprolegniosis on various fish species. In addition to fish, species of amphibians [79], crustaceans [80] and aquatic insects [81] are also highly susceptible to saprolegniosis. There is conclusive evidence that Saprolegnia species are major killers of populations of amphibians globally, threatening some already highly endangered species [82][83][84]. ...
... Such infections are widespread in all stages of the life cycle of fish, from the egg to the adult stage. Members of the family Saprolegniaceae, in particular, Saprolegnia spp., Achlya spp., and Aphanomyces spp., are the causative agents of these infections (Scott and Warren 1964;Willoughby 1970Willoughby , 1978Willoughby , 1998Neish and Hughes 1980;Hoshiai 1992a, 1992b;Blausteine et al. 1994;Kitancharoen et al. 1995;Hussein and Hatai 1999). ...
This study was conducted to investigate the antimycotic activities of eugenol, a major essential oil of clove, against some fish pathogenic species of Saprolegniaceae as well as to determine the toxicity of eugenol to selected cultured fish. Two eugenol solutions were used in this study, a 10% v/v (volume: volume) solution in dimethyl sulfoxide (DMSO) and FA 100, which contains 10% v/v eugenol. The fungal species investigated were Saprolegnia parasitica, S. diclina, S. ferax, S. salmonis, Achlya klebsiana, and Aphanomyces piscicida. The minimum inhibitory concentrations (MICs) of eugenol in DMSO against Saprolegnia spp., A. klebsiana, and A. piscicida were 500, 250, and 125 mg/mL, respectively, and the fungicidal concentrations (for complete killing) were 1,000, 500, and 250 mg/mL, respectively. In contrast, the MICs of FA 100 against S. parasitica, other Saprolegnia spp., A. klebsiana, and A. piscicida were 250, 125, 250, and 63 mg/mL, respectively, and the fungicidal concentrations were 1,000, 1,000, 1,000, and 63 mg/mL, respectively. Zoospores of the Saprolegnia spp. tested and of A. klebsiana could not germinate in the presence of a concentration of 250 mg/ mL of either eugenol solution, while those of A. piscicida were killed by a concentration of 125 mg/mL of either eugenol solution. Eugenol was highly toxic to salmonids but less toxic to cyprinids.
... While L. catesbeiana may not be a competent reservoir species because it does not retain infection under laboratory conditions, it is likely important in driving disease dynamics in many parts of its native and invasive range. One of the most robust examples of a reservoir host is the Pacific chorus frog, Pseudacris regilla, which has high Bd prevalence in the wild (Fellers et al., 2011), and can maintain a high and stable infection in the lab without signs of disease (Blaustein et al., 1994;Reeder, Pessier & Vredenburg, 2012;Gervasi et al., 2013a). Maintaining a high and stable infection over time is important for a competent reservoir host because it can be the driver of infection within a community of co-occurring susceptible species. ...
... In the United States, 31.7 % of amphibian species are in decline (Adams et al. 2013) and 26% of rare endemics are listed as threatened (IUCN 2015). In the western United States, populations of B. boreas have experienced declines across their large geographic range (Blaustein & Wake 1990;Blaustein et al. 1994;Bull & Carey 2008;Pilliod et al. 2010). Within the Great Basin, B. boreas occupancy is declining because of habitat loss (Wente et al. 2005), and all three endemics are threatened (IUCN 2015). ...
We describe a new species of toad from the Great Basin region of northern Nevada belonging to the Bufo (Anaxyrus) boreas species complex. This cryptic species was detected through genetic analyses of toad populations sampled throughout the Great Basin and the morphological evidence was quantified through extensive sampling of live toads within the region. The new species has the smallest body size in the species complex, and can be further diagnosed from other species in the complex by its large tibial glands and unique coloration. The known distribution of the new species is restricted to an area less than 6 km2 in Dixie Valley, Churchill Co., Nevada. The Great Basin is an arid region where aquatic resources are both rare and widely scattered, making habitat suitable for anuran populations highly vulnerable to anthropogenic change. The habitat occupied by this newly described species is threatened by the incipient installation of geothermal and solar power development projects that require the water that defines its habitat.
... This is particularly true in the Pacific Northwest, USA, which is a region where Saprolegnia has been identified as a potential pathogen on amphibians that have experienced local declines (Kiesecker and Blaustein 1995). For example Blaustein et al (1994) suggested Saprolegnia ferax was responsible for mortality of nearly 95% of western toad (Bufo boreas) eggs at one site in Oregon. Despite these claims that S. ferax is a pathogenic water mold of amphibian eggs, no studies have attempted to document which species of oomycetes occur on the eggs of North American amphibians and whether egg mortality is uniquely associated with S. ferax. ...
We assessed the diversity and phylogeny of Saprolegniaceae on amphibian eggs from the Pacific Northwest, with particular focus on Saprolegnia ferax, a species implicated in high egg mortality. We identified isolates from eggs of six amphibians with the internal transcribed spacer (ITS) and 5.8S gene regions and BLAST of the GenBank database. We identified 68 sequences as Saprolegniaceae and 43 sequences as true fungi from at least nine genera. Our phylogenetic analysis of the Saprolegniaceae included isolates within the genera Saprolegnia, Achlya and Leptolegnia. Our phylogeny grouped S. semihypogyna with Achlya rather than with the Saprolegnia reference sequences. We found only one isolate that grouped closely with S. ferax, and this came from a hatchery-raised salmon (Idaho) that we sampled opportunistically. We had representatives of 7–12 species and three genera of Saprolegniaceae on our amphibian eggs. Further work on the ecological roles of different species of Saprolegniaceae is needed to clarify their potential importance in amphibian egg mortality and potential links to population declines.
... Artificial agitation markedly increases hatching success of A. japonicas in captivity (Suzuki, 1981(Suzuki, , 1984 presumably because it prevents yolk adhesions and developmental anomalies (Nussbaum, 1985). Lastly, water mould infection presents a serious threat to aquatic eggs of various amphibians (Blaustein et al., 1994;Gomez-Mestre, Touchon & Warkentin, 2006) including A. japonicas (Suzuki, 1984). Hygienic filial cannibalism is likely to be important in preventing water mould infection from spreading over the entire clutch. ...
Parental care is remarkably diverse in its modes both within and across taxa. Within amphibians, various pre- and post-hatching care behaviours have been described in frogs. In contrast, the current knowledge about salamander parental care is largely limited to pre-hatching attendance by females. In particular, post-hatching parental care by male salamanders have never been described and analysed in detail. A recent study revealed various modes of pre-hatching care provided by male Japanese giant salamanders (Andrias japonicus). Their hatched larvae are known to stay in the nest with the father (i.e. den master) for several months before dispersal, which led to the hypothesis that den masters continue providing care for hatchlings. To test this hypothesis, we videotaped and analysed post-hatching behaviours of two male A. japonicus that remained in the nests with hatchlings in situ. We also developed and tested several predictions regarding the post-hatching care behaviours in comparison to the pre-hatching behaviours. While one male abandoned the nest, the other male remained in the nest and provided care until the larvae dispersed in the following spring. The comparative analyses on three parental care behaviours (tail fanning, agitating/checking and hygienic filial cannibalism) between pre- and post-hatching care suggest their flexible and condition-dependent nature. Furthermore, the comparison in larval mortality and potential predators between the attended and abandoned nest revealed the crucial role of a den master in improving offspring survivorship. Our observations also disclosed the possibility of leech infection posing a serious threat to larval giant salamanders. The life-history traits associated with the evolution of such prolonged post-hatching paternal care in salamanders are fully aquatic life cycle, external fertilization and stream habitat. The rare combination of these traits is unique to the family Cryptobranchidae which consists of the three imperiled and secretive giant salamanders.
... Saprolegnia parasitica causes saprolegniosis on various fish species. In addition to fish, species of amphibians [79], crustaceans [80] and aquatic insects [81] are also highly susceptible to saprolegniosis. There is conclusive evidence that Saprolegnia species are major killers of populations of amphibians globally, threatening some already highly endangered species [82][83][84]. ...
Oomycetes, or water moulds, are fungal-like organisms phylogenetically related to algae. They cause devastating diseases in both plants and animals. Here, we describe seven oomycete species that are emerging or re-emerging threats to agriculture, horticulture, aquaculture and natural ecosystems. They include the plant pathogens Phytophthora infestans , Phytophthora palmivora , Phytophthora ramorum , Plasmopara obducens , and the animal pathogens Aphanomyces invadans , Saprolegnia parasitica and Halioticida noduliformans . For each species, we describe its pathology, importance and impact, discuss why it is an emerging threat and briefly review current research activities.
This article is part of the themed issue ‘Tackling emerging fungal threats to animal health, food security and ecosystem resilience’.
Ambystoma altamirani is a microendemic amphibian limited to central Mexico, speci cally the Bosque de Agua region in the Trans-Mexican Volcanic Belt, renowned for its endemic amphibian species. Anthropogenic activities such as land use change, water pollution, and the introduction of exotic species such as rainbow trout (Oncorhynchus mykiss) have substantially transformed its habitat, creating barriers that fragment it and impeding the mobility of the species and connectivity with other populations. This fragmentation poses challenges, including emerging diseases, inbreeding, limited gene ow, and a loss of genetic diversity, placing Ambystoma altamirani in national and international risk categories. The present study utilized the ENMeval and biomod2 models for environmental niche modeling (ENM) to assess the potential distribution of Ambystoma altamirani in the Bosque de Agua region. The key supporting variables include rivers, lakes, altitude, and a combination of Abies and Pinus forests, while the detrimental factors include urbanization and agriculture. Employing circuit theory (CT) and least-cost path (LCP) methodologies, this research explored structural connectivity, identifying core areas in the central region of Bosque de Agua. As migration distance decreases, the number of corridors facilitating population ow decreases. In the concluding phase, an analysis assessed the coincidence of state and federal Mexican Natural Protected Areas with core areas, revealing a lack of protection. The results of this study could lead to improved knowledge about Ambystoma altamirani, providing valuable tools for helping stakeholders formulate comprehensive strategies for species conservation.
The introduction of exotic species is one of the main leading factors in the decline and extinction of amphibian populations worldwide. Reductions in the abundance and local extinctions of amphibians due to the introduction of exotic fishes in rivers or lakes have been reported worldwide. To help prevent further extinctions, studies are needed in order to make appropriate conservation decisions. In the present study, environmental niche modeling (ENM) was used to identify the environmental niche overlap and land-use and vegetation cover variables that favor the presence of the invasive species Rainbow trout (Oncorhynchus mykiss) and its amphibian prey, including the Mountain stream salamander (Ambystoma altamirani), Mountain tree frog (Dryophytes eximius), and Ridged tree frog (Dryophytes plicatus) in central Mexico. We found that the potential distributions and environmental niches of O. mykiss and its amphibian prey are similar, which may affect the amphibian populations in several ways, including the displacement of these species from their distribution area in the long term. The information generated in this study is critical for proposing better conservation strategies for these amphibian species as well as management solutions for the invasive O. mykiss hatcheries.
Description
Original research discusses the protocols and approaches to studying the effects of multiple environmental stressors on amphibian populations and gives new perspectives on this complicated subject. This new publication integrates a variety of stressors that can act in concert and may ultimately cause a decline in amphibian populations.
Sixteen peer-reviewed papers cover:
Toxicity Assessment examines methods, which range from long-established laboratory approaches for evaluating adverse chemical effects to amphibians, to methods that link chemicals in surface waters, sediments, and soils with adverse effects observed among amphibians in the field.
Field and Laboratory Studies illustrates studies in the evaluation of multiple stressor effects that may lead to declining amphibian populations. A range of laboratory and field studies of chemicals, such as herbicides, insecticides, chlorinated organic compounds, metals, and complex mixtures are also included.
Causal Analysis demonstrates the range of tools currently available for evaluating "cause-effect" relationships between environmental stressors and declining amphibian populations.
Audience: This new publication is a must-have for scientists and resource management professionals from diverse fields, including ecotoxicology, chemistry, ecology, field biology, conservation biology, and natural resource management.
Este Manual de Campo ha sido el producto de un esfuerzo colectivo, que ha involucrado profesionales de diferentes instituciones y países de los Andes tropicales y de especialistas de otros países en América y Europa. Su conocimiento, experiencia extensiva y compromiso en la conservación de los anfibios han sido claves para el desarrollo del mismo. Este compendio de experiencias llega en un momento en que los esfuerzos para la conservación de los anfibios son tan altamente necesarios como
críticos y urgen el incremento del trabajo de campo que permita disminuir los vacíos de conocimiento colectivo acerca de los anfibios andinos.
Este manual se desarrolló con estas prioridades en mente, ya que ha sido escrito como herramienta de apoyo para los biólogos especialistas o para aquellas personas profesionales o en curso de serlo, interesados en los anfibios, con el objeto de facilitarles la estructuración de proyectos de investigación en los Andes tropicales.
“Técnicas de inventario y monitoreo para los anfibios de la región tropical andina”
recoge el deseo de los autores de los capítulos en ofrecer el estado del arte sobre el conocimiento de los mecanismos, prácticas y metodologías sobre el inventario y monitoreo de los anfibios con la esperanza de motivar el reclutamiento de nuevos investigadores que, a través de su propia iniciativa o de los cursos que hasta ahora
han venido siendo adelantados por la Iniciativa Atelopus, puedan ampliar su formación académica en beneficio de la conservación de nuestra herencia natural.
Amphibians are declining globally, chemical contamination being one of the major factors driving this process. As a consequence of exposure to such environmental perturbation, natural population of amphibians may lose their genetic diversity, which may occur due to a decrease in: 1) fitness, 2) environmental plasticity capabilities and 3) tolerance mechanisms efficiency. Metal contamination is one of the most worldwide distributed contamination source, having a great impact in the Iberian Peninsula habitats, especially in the Iberian pyrite belt region. Therefore, is important to explore how tolerance mechanism, toward metal contamination, work in amphibians and how genetically determined tolerance mechanisms are inherited. In this work, these topics were addressed by assessing the inheritance to lethal tolerance to acid mine drainage and copper contamination in eggs of the Perez's frog Pelophylax perezi. Incomplete dominance was found to be the most likely inheritance mechanism of tolerance toward these two chemical stressors in the eggs of P. perezi. The results support the recessive (or incompletely dominant) tolerance inheritance (working-) hypothesis. Thus, the amphibians’ populations impacted by metal contamination can considerably lower their genetic diversity, even if allele fixation was excluded. The possibility of tadpoles, historically exposed to metal contamination, being able to acquire an increased tolerance to metal contamination, comparatively to tadpoles inhabiting reference sites, was also studied. Pelophylax perezi tadpoles, sampled at historically metal impacted mining sites, did not show higher oxidative stress or lethal tolerance comparatively to tadpoles inhabiting reference sites. However, the metal body burden proved metal contamination at the historically metal impacted sites and showed that mercury and lead ions are readily bioavailable for P. perezi tadpoles. Furthermore, tadpoles from metal contaminated sites seem to show higher constitutive levels of metallothioneins, which may suggest adaptation to metal contamination The last objective of this work, was to evaluate the influence, of metal contamination, on the composition and diversity of the P. perezi skin microbiome, and to explore its tolerance to acid mine drainage contamination. Amphibians’ skin microbial community has been shown to help its hosts tolerating infections. Because the increasing research on the important protective role of amphibians’ skin microbiome, its diversity and capacity to tolerate metal contamination was as well investigated. Obtained results showed that metal contamination influences the skin microbial community composition in frogs living at metal impacted sites; furthermore, an intense acid mine drainage concentration can inhibit the growth of almost all the isolated strains. This inhibition suggests that amphibians may lose an important part of their skin microbiome, affecting the protection of their skin, when exposed to metal contamination; which, in turn may lead to an increased sensitivity to metal contamination.
Emerging infectious diseases are major drivers of global and local amphibian biodiversity loss. Therefore, developing effective disinfection methods to manage the impact of diseases in wild and captive “ark” populations are an important goal in amphibian conservation. While chemical disinfectants have been used safely and effectively in larval and adult amphibians infected with pathogenic microbes, their applicability to amphibian egg masses has remained untested. To bridge this gap, we exposed embryos of the common toad (Bufo bufo) and agile frog (Rana dalmatina) experimentally to three widely used disinfectants: voriconazole, chloramphenicol and chlorogen‐sesquihydrate. For 3 days we exposed portions of egg masses to these disinfectants at 1×, 2×, 5× and 10× the concentration recommended for the disinfection of tadpoles and adults. Subsequently, we recorded embryonic and larval survival, as well as larval body mass and the incidence of abnormalities 12 days after hatching. Application of voriconazole had species‐ and concentration‐dependent negative impacts on survival and body mass, and caused marked malformations in the viscerocranial structure of B. bufo tadpoles. Exposure to chlorogen‐sesquihydrate also resulted in significant mortality in B. bufo embryos and negatively affected body mass of R. dalmatina larvae. Chloramphenicol had little negative effects on embryos or larvae in either species. Based on these results, the application of voriconazole and chlorogen‐sesquihydrate cannot be recommended for the disinfection of amphibian eggs, whereas treatment with chloramphenicol appears to be a safe method for eliminating potential pathogens from anuran egg masses and their immediate aquatic environment.
Saprolegnia ferax is isolated from polluted water sample collected from Mula River, Pune, Maharashtra, India. The isolated taxon is illustrated and compared with the morphotaxonomy based first record of Indian S. ferax isolated by Wani et al. (2017). The present study deals with the re-description of the isolated taxon S. ferax based on detail morphological features, sequence analysis and phylogeny of ITS and LSU regions of rDNA.
Saprolegnia ferax is isolated from polluted water sample collected from Mula River, Pune, Maharashtra, India. The isolated taxon is illustrated and compared with the morphotaxonomy based first record of Indian S. ferax isolated by Wani et al. (2017). The present study deals with the re-description of the isolated taxon S. ferax based on detail morphological features, sequence analysis and phylogeny of ITS and LSU regions of rDNA.
Como ha sido ampliamente divulgado en las revistas científicas y medios de comunicación del orbe, los anfibios enfrentan, en la actualidad, una grave amenaza para su conservación. Esta crisis mundial es el
resultado de una sinergia de muchas amenazas que están conspirando contra la supervivencia de uno de los grupos de vertebrados de una forma nunca observada en tiempos modernos. Con este conjunto de situaciones negativas como la creciente pérdida de hábitat, el inclemente uso de pesticidas, el aumento de la radiación ultravioleta, y la peligrosa expansión y patogenicidad de la chitridomicosis, los anfibios en general y muy seguramente otros grupos de especies de nuestra rica biodiversidad tendrán que enfrentar un futuro sombrío.
La buena noticia, si hay alguna, es que aún podemos hacer algo, pero requerimos dedicar esfuerzos a adquirir información reciente sobre la situación de conservación de las poblaciones, hacerles seguimiento y obtener de esta manera elementos de juicio para adelantar acciones novedosas y creativas que contrarresten esta crisis de conservación. Igualmente es importante resaltar que la investigación in situ y el trabajo mancomunado de muchos actores debe ser un componente central y clave para desarrollar este nuevo conocimiento. El reto es enorme, máxime si reconocemos y comprendemos que el estar en el epicentro de la biodiversidad convierte a los cinco países andinos en un escenario de máxima vulnerabilidad, pues los impactos de esa aún incomprendida sinergia de amenazas creciente, pueden ser desastrosos sobre nuestros recursos dado que siempre tendremos mucho que perder, pero también mucho que ganar en la medida que establezcamos un frente común para contenerlos. Al igual que el estatus de conservación de las especies de anfibios en
los Andes tropicales, nuestro conocimiento sobre la historia natural, niveles poblacionales y usos benéficos está en peligro. Y aunque los científicos lleven muchos años trabajando para incrementar el conocimiento sobre la diversidad de especies y se hayan adelantado los pasos necesarios para identificar algunas de las causas más importantes de la disminución de sus poblaciones, la realidad es que hay aún un enorme desconocimiento sobre aspectos relevantes de la historia natural en general y sobre la identidad de muchas de las especies que habitan en diversas regiones inexploradas o exploradas parcialmente. Todo ello conduce a pensar que el gran número de especies deficientes de datos (DD), casi amenazadas (NT) listadas en la última evaluación global de anfibios de 2004 según los criterios de UICN, pueden modificar sustancialmente e incrementar el número de especies en los niveles de amenaza(CR, EN, VU) que surjan de próximas evaluaciones a nivel nacional o global y probablemente, en la medida que conozcamos más sobre la situación real, se incrementen también tristemente en la categoría de extinta (EX). Esta situación nos señala que las exploraciones de campo deben ser una prioridad para la investigación en el futuro y dentro de ellas las que contribuyan a implementar actividades de monitoreo de las especies identificadas como amenazadas y los inventarios de sitios inexplorados. Con esta gran preocupación en mente este manual recoge la experiencia
de varios investigadores quienes han dedicado buena parte de su vida profesional al desarrollo de técnicas de seguimiento y a la ardua tarea de ponerlas en prueba por largos periodos para ver sus bondades en los resultados generados. De la misma manera estas experiencias se han puesto en práctica en los tres cursos de campo sobre inventario y monitoreo de anfibios desarrollados por la Iniciativa Atelopus de Conservación Internacional y la Iniciativa Darwin en Perú, Venezuela y Bolivia. El resultado final de este proceso de
depuración es el producto que hoy se presenta a la comunidad académica y en general a todos aquellos interesados en los anfibios. Igualmente este manual representa una pequeña pero estratégica parte del esfuerzo global para enfrentar las disminuciones y extinciones como se menciona en el Plan para la Conservación de los Anfibios (ACAP), documento desarrollado durante la Cumbre de la Conservación de los Anfibios que se reunió en Washington, D.C. en septiembre de 2005, y que es la guía para las acciones de conservación de los anfibios que se implementen, a nivel global, durante los próximos años. Esperamos que al promover la investigación con iniciativas como ésta, podamos incrementar nuestro conocimiento
During the present studies, the impact of fragmentation was analyzed using
species richness, density and incidence of occurrence, along with concurrent data
on vegetation, climate and physico-chemical parameters of water and soil. The study was made using the species richness to test the hypothesis that "native habitats support high anuran species richness, while fragmentation induces changes in species richness and distribution".
Rana catesbeiana was introduced into California between 1914 and 1920 and has since spread throughout the state. In the San Joaquin Valley it has become the dominant frog on the valley floor and has spread into the Sierra Nevada foothills. It is most abundant in the warm low elevation pools of the foothill streams, in areas heavily altered by man, although at least two populations are established above 1600 m elevation. Of the two frog species native to this region, R. aurora is either absent or very rare at the present time, while R. boylii is found mostly in small permanent foothill streams higher than 200 m elevation, in areas not occupied by R. catesbeiana. The disappearance of R. aurora from the region, and the continuing reduction in range of R. boylii, is attributed to habitat alteration coupled with predation and competition from R. catesbeiana.
the golden toad, is an endangered species endemic to Costa Rica. Every year from the early 1970s through 1987 golden toads have emerged from retreats to breed during April-June. The most recent known breeding episode occurred during April-May 1987; more than 1500 adults were observed at five breeding pools, but a maximum of 29 tadpoles metamorphosed from these sites. During April-June 1988-90, we found only 11 toads during surveys of the breeding habitat. To examine the species' apparent decline, we analyzed data on rainfall, water temperature, and pH of the breeding pools. Our baseline data on weather patterns and characteristics of the breeding habitat suggest that warmer water temperatures and less advective precipitation during dry season post-1987 may have produced adverse breeding conditions. The toads may be alive and hiding in retreats awaiting appropriate weather conditions. The apparent scarcity of toads may reflect a normal population re-sponse to an unpredictable environment. On the other hand, because other an-urans with different breeding specializations seem to be declining from the area as well, one wonders whether warmer temperatures and dry conditions could be responsible for real population declines. Because the habitat is protected and pristine, potential causes of anuran de-clines such as habitat destruction, introduced predators, and collecting seem unlikely. Measurements of pH of the breeding pools, cloud water, and precipi-tation do not suggest acid precipitation effects, although we cannot rule out the possibility of environmental degradation some time prior to our measurements. Long-term monitoring programs combined with carefully controlled field ex-periments are needed to address factors responsible for declining amphibians.
Breeding ecology and mating patterns of the western toad, Bufo boreas, were examined in three large explosively breeding populations in the Oregon Cascade Mountains. Two mating patterns occurred variably within and among the three populations. First, a large male mating advantage was observed in two of the three populations when data from all the days of data collection were combined. When each day of breeding was analyzed separately, there was a large male mating advantage on 3 of 5 days at one population, and mating was random on all days at the two other populations. The second mating pattern, positive assortative mating by size, was observed at two of the three populations. This pattern was found on separate days of breeding as well as when data from all days were combined at one population, and on only one day of breeding at the second population.
In a survey of anuran amphibian mating patterns, intraspecific variation was found in 13 of 15 species, including the present study of the western toad. Intrapopulation variation in mating patterns among breeding years has been observed in 5 of 8 anurans, whereas within-site, within-year mating pattern variation has only been reported for the western toad. These results strongly suggest that anuran mating patterns are frequently neither species-specific nor population-specific attributes. Variable mating patterns were most commonly observed in explosively-breeding anurans. Explosive breeders may be susceptible to variable mating patterns because they may be more sensitive to fluctuations in environmental conditions, demographic parameters, and the intensities of intrasexual competition and mate choice.
Basal levels of glucocorticoids maintained by negative feedback regulation are known to modulate a wide range of physiological processes, through a variety of effects such as those on carbohydrate metabolism and “permissive” actions on effects of other hormones. Glucocorticoid levels increase sharply in response to the stress of any kind of threat to homeostasis. The increased levels have traditionally been ascribed the function of enhancing the organism’s resistance to stress. How known physiological and pharmacological effects of high levels of glucocorticoids might accomplish this function, however, has been a mystery.
A generalization that is beginning to emerge is that many of these effects may be secondary to modulation by glucocorticoids of the actions of numerous intercellular mediators, including established hormones, prostanoids, neutral proteinases, and cytokines such as interferon. These mediators participate in physiological mechanisms — endocrine, renal, immune, neural, etc. — that mount a first line of defense against such challenges to homeostasis as hemorrhage, metabolic disturbances, infection, anxiety, and others.
Contrary to the traditional view that the role of glucocorticoids in stress is to enhance these defense mechanisms, it has become increasingly clear that glucocorticoids at moderate to high levels generally suppress them. This paradox first emerged when glucocorticoids were discovered to be antiinflammatory agents, and had remained a major obstacle to a unified picture of glucocorticoid function.
We have suggested that stress-induced increases in glucocorticoid levels protect not against the source of stress itself but rather against the body’s normal reactions to stress, preventing those reactions from overshooting and themselves threatening homeostasis. This hypothesis, the seeds of which are to be found in many earlier discussions of glucocorticoid effects, immediately accounts for the paradox noted above, and provides glucocorticoid physiology with a unified conceptual framework that can accommodate such apparently unrelated physiological and pharmacological effects as those on carbohydrate metabolism, inflammatory processes, shock and water balance. It also leads us to propose that some enzymes rapidly induced by glucocorticoids detoxify mediators released during stress-induced activation of primary defense mechanisms; those mediators could themselves cause damage if left unchecked.
Reports of declining amphibian populations in many parts of the world are numerous, but supporting long-term census data are generally unavailable. Census data from 1979 to 1990 for three salamander species and one frog species at a breeding pond in South Carolina showed fluctuations of substantial magnitude in both the size of breeding populations and in recruitment of juveniles. Breeding population sizes exhibited no overall trend in three species and increased in the fourth. Recent droughts account satisfactorily for an increase in recruitment failures. These data illustrate that to distinguish between natural population fluctuations and declines with anthropogenic causes may require long-term studies.
An ecological study was conducted on the Western Chorus Frog, Pseudacris triseriata, at Terre Haute, Vigo County, Indiana, between 1963 and 1969. Descriptions of adults are given with comparisons between sexes and ponds. Descriptive information is included on the development of tadpoles, froglets, and young individuals. Data on breeding congresses, incubation periods and food habits are presented. The relation of P. triseriata to Hyla crucifer, Natrix sipedon and Thamnophis sauritus is discussed. P. triseriata contained trematodes and nematodes. Eggs were generally laid in March or April at Terre Haute (12 March-22 April) and usually coincided with major rainstorms. In any one year most egg laying occurred over a relatively short period or periods. The number of eggs ranged from 12 to 245 in 96 masses (mean of 79.8). The total complement of eggs varied in 10 females from 440 to 752 (mean of 597.33). Water temperature affects the incubation period. In 1965, eggs in the field hatched in 8 to 13 days, while in 1969, during a colder period, eggs hatched in 15 to 27 days. In temperature control chambers at 44 degrees, eggs hatched between the 25th and 46th days, while nearly all eggs at 73 F hatched on the fourth and fifth days. The time from egg laying to metamorphosis, in one group of eggs in the field in 1965, took 52 days and in 1969, about 70 days. Metamorphosis at Terre Haute occurred in late May or early June. P. triseriata and Hyla crucifer occupied the same breeding ponds at the same time. Pseudacris would often sing both day and night, Hyla only at night. The two species were often segregated in individual breeding ponds. P. triseriata tadpoles were most abundant in water 11 to 22 cm deep and where emergent vegetation was less dense. There was no relation between tadpoles and distance to shore or presence or absence of Hyla crucifer tadpoles. P. triseriata tadpoles fed mostly on filamentous and non-filamentous algae. Metamorphosing individuals did not feed. Recently transformed froglets fed on Collembola, mites, small insects, and possibly shed skin. Individuals collected in summer and fall from terrestrial habitats fed on various invertebrates with ants and spiders being the most important. Adults of P. triseriata in the breeding ponds, unlike those of Hyla crucifer, fed, with lepidopterous larvae, spiders, curculionids, and chironomids being some of the important items utilized. Vegetation was also important. P. triseriata is a terrestrial rather than an aquatic feeder. Natrix sipedon was listed as a predator and Thamnophis sauritus as a probable predator on Pseudacris. A total of 291 (40.9%) of the male frogs, and 46 (28.3%) of the females yielded trematode parasites, a new species in the genus Glypthelmins currently being described by Robert E. Geyer. Of male frogs, 48.6% contained nematodes (Oswaldocruzia sp. and Aplectana sp.), as did 44.0% of the females. The average number of trematodes per frog was 7.2 in males and 3.9 in females, and for nematodes similar figures were 1.7 in males and 1.5 in females.
(1) Adult natterjack population density and toadlet production per 100 m2 of breeding water were substantially higher (5-fold and 2-9-fold, respectively) on a eutrophic (dune) habitat than on an oligotrophic (heathland) study site. (2) Key factors in mortality during development were desiccation of shallow, natural dune slacks and saltmarsh pools and predation of tadpoles by invertebrates in all pool types. Developmental failure of spawn was caused primarily by Saprolegnia infestation at low temperatures or by low pH (<6). (3) Metamorphic success was correlated with high tadpole growth rates. These rates were determined primarily by temperature and food supply, and the latter was a function of water chemistry. Tadpoles grew faster in the more eutrophic pools, though low pH (<6) reduced growth rates irrespective of food supply. (4) Major predators of natterjack larvae were dytiscid water beetles; others of significance included Notonecta species, Odonata larvae and the newt Triturus cristatus (Linnaeus). (5) Toadlet production varied inversely with respect to numbers of invertebrate predators in the breeding pools, and these in turn varied as a function of pond permanence. Deeper artificial pools exhibited lower tadpole mortality from desiccation but correspondingly higher mortality from invertebrate predation.
Gambusia affinis starved 1 to 4 days and offered normally deposited eggs of Acris crepitans, Bufo valliceps, Gastrophryne olivacea, Hyla chrysoscelis, Pseudacris clarki, Scaphiopus couchi, or Rana pipiens ate a significantly larger number and volume of eggs of those species which usually breed in temporary as opposed to permanent water. The differential predation seemed to result from the larger, firmer egg capsule of the permanent water breeders acting as a mechanical defense mechanism. There was no evidence of chemical repellents or toxicity in the egg species studied.
(1) Fertilization and embryonic development in Rana temporaria (L.) were studied in two field-based experiments. (2) Thirty-six ponds in northern England were used, ranging in altitude from 183 m to 617 m. Several of these ponds were cold, acidic and had high concentrations of toxic metal ions. (3) Inorganic monomeric aluminium concentration was the principal factor reducing fertilization success. (4) Exposure to a high zine concentration, early in development, subsequently increased the number of abnormal embryos. (5) Low minimum pond temperature was the principal factor increasing embryonic mortality. This factor may be less significant in warmer breeding seasons. Most dead eggs were at the mid to late cleavage or early gastrula stage. (6) Most embryonic abnormalities were associated with the incomplete absorption of the yolk plug during gastrulation. Inorganic monomeric aluminium concentration was the principal factor associated with this type of abnormality (7) Saprolegnia sp. infection of frog eggs was greatest in cold, acidic ponds, with low calcium concentrations.
We report finding 12 Lucke renal carcinomas from autopsy of 409 frogs (2.9%) since 30 January 1987 to the present date (6 April 1989). While tumor prevalence remains low, tumors appear more abundant now than they have been in the recent past. Between 1977 and 30 January 1987, only one tumor was found at autopsy of 4532 frogs.
(1) The colonization of clean (apparently uninfected), dead salmonid fish by Saprolegniaceae was studied both in the laboratory and in Windermere. Colonization proceeds in two stages in water: initially there is superficial mycelium, which is easily removed, and later there is a deeper penetration into the epidermis and dermis. There was evidence that colonization can occur as an intimately mixed mosaic of different Saprolegniaceae. (2) Live char and other salmonids are normally colonized only by the specific Saprolegnia pathogen in Windermere. However, this specificity broke down when there was colonization of dead tissue on a live char. This situation was seen to be analogous to that in 'perch disease'; it is deduced that the role of the various fungi here is saprophytic only. (3) In post-mortem, salmonid fish killed by the specific Saprolegnia pathogen do not attract other Saprolegniaceae subsequently and explanations for this are proposed.
Rana muscosa is one of several high-elevation amphibians that have recently disappeared from seemingly pristine sites. The present study documents an event of mass mortality among larval and metamorphosed R. muscosa in a lake in Kings Canyon National Park, California, and the ultimate extinction of the population. In 1979 metamorphosed individuals declined from ca. 800 individuals in early summer to nearly zero in late summer. During this time many carcasses were collected, individuals showed symptoms of red-leg disease, and blood from an affected individual contained the bacterial pathogen characteristic of this disease, Aeromonas hydrophila. Also during the summer of 1979, nearly all of the approximately 1100 tadpoles began metamorphosis, but all metamorphosing individuals were consumed by Brewer's blackbirds (Euphagus cyanocephalus). This population of R. muscosa continued to exist until at least 1983, but was extinct by 1989. Recolonization of the site will probably never occur because streams connecting to extant populations of R. muscosa now contain introduced fishes.
Saprolegniaceous fungi associated with the rainbow trout (Salmo gairdneri) were observed at Ma-ling Hatchery in Tai-Chung Prefecture, Taiwan during December, 1979 to February, 1980. One strain among the isolated fungi attached a male spawning fish was identified as Aphanomyces laevis. Another strain infected mainly on the peduncle and caudal fin of a female spawning fish was examined and identified as Saprolegnia diclina. The former was incubated at 10°C and gave well-developed sexual organs, and the latter was kept at 16°C and appeared both asexual and sexual structures. It may produce abundant of antheridia and oogonia either short after or after prolonged period of time when mycelium was removed from diseased fish. Oogonial wall of this fungus is usually pitted under point of attachment of antheridial cell and shows antheridia of diclinous form only. Some isolates of S. dicline were heavily affected by Woronina polycystis (in the Order Plasmodiophorales) which acts as an obligate parasite and eventual destruction of host hyphae.
Tadpoles involved in predator-prey interactions were studied in tropical wet forest in Costa Rica under laboratory and field conditions. Larvae of the frog Leptodactylus pentadactylus and naiads of the odonate Pantala flavescens are im- portant predators on larvae of several species of frogs. The predators discriminate the prey on the basis of size and species, but not type of habitat in which predation occurs. A graphical model is proposed to illustrate the rela- tionships between species diversity and habitat complexity as they affect the composition of tadpole communities. The model is used to evaluate the relative importance of abiotic and biotic factors in determining the use of specific kinds of aquatic habitats by frogs with larval stages. Predation by permanent aquatic predators (primarily fish) is con- sidered to be the most important biotic factor influencing the temporal and spatial composition of tadpole communi- ties. The development and maintenance of predatory feeding modes, including cannibalism, in certain tadpoles is ex- amined in light of the model.
The germination and growth of zoospores of the Saprolegnia (S. diclina-S. parasitica complex) from brown trout Salmo trutta was followed. A large amount of growth occurred in natural Windermere water on two occasions in October 1983 and the mycelia went on to form two-spored sporangia (abbreviated life-cycle). On several other occasions Windermere water gave a much smaller amount of growth but this was sufficient to support a single-spored sporangium (micro life-cycle). A large amount of growth always occurred in fish hatchery water but small sporangia were never observed. -from Author
Extensive die-offs of rainbow smelt, Osmerus mordax (Mitchell), have occurred in the western end of Lake Superior during each of the past several springs. Sex, age composition, and incidence of fungus infection in smelt from the 1977 die-off were compared with the same characteristics of smelt of the extant spawning population to determine the extent and possible causes of mortality. The die-off in 1977 began about 3 weeks after the end of the spawning run and continued for approximately 2 weeks. The occurrence of dead rainbow smelt was greatest near the Superior-Duluth harbor and decreased as distance from the harbor increased. Age structure of smelt that died was similar to that of the spawning population. Some factor or factors related to spawning may have caused the mortality. The most probable cause of the die-off was temperature stress on spawning smelt in the spawning areas which increased the susceptibility of smelt to the fungus Saprolegnia sp. and may have promoted osmoregulatory imbalance. Male smelt were more vulnerable to the cause of the die-off than female smelt; young fish, especially females, were more resistant than older fish.
Largemouth bass (Micropterus salmoides), when starved for 1 day, almost totally abstain from eating toad (Bufo americanus and Bufo woodhousei) tadpoles. However, there is a positive relationship between bass hunger levels and the acceptability of Bufo larvae as food items. With experience, there is a decrease in the number of toad tadpoles engulfed (taken into the mouth), and that actually consumed by the bass, while the number of larvae expelled (spat out) increases. Bass strongly prefer Hyla crucifer tadpoles to B. americanus larvae, and learn to distinguish between the two species. These results agree with the hypothesis that the schooling behaviour found in B. americanus tadpoles functions, at least in part, as a deterrent to predation.
At a recent workshop in California, scientists discussed the decline of amphibian populations and suggested that these animals may be biological indicators of advanced degradation of the environment. One study described the effects of snowmelt contamination with acid deposition from smog and smelters on the breeding ponds of salamanders. Other possible reasons for decline include: heavy metals and pesticides; global climate changes; imbalances in mammal populations that prey on amphibians; predation by fishes stocked in lakes by wildlife managers; and human predation.
During the course of present investigations 43 isolates representing 5 genera of Saprolegniaceous fungi were isolated from 19 different species of freshwater fishes. The parasitic abilities of these isolates have been demonstrated by conducting artificial inoculation experiments under laboratory conditions using the species of Puntius and Colisa as test fishes.
It has recently become evident that amphibian species in many areas of the world have suffered serious declines. Healthy, seemingly well-protected populations have disappeared for no obvious reason. Data from historic accounts and museum records indicate that the Cascades frog, Rana cascadae, was once abundant at the southern end of its range in the vicinity of Lassen Volcanic National Park, California, USA. We conducted intensive searches at all 16 sites where R. cascadae had previously been recorded in the Lassen area, plus 34 additional sites with suitable habitat. Whereas earlier biologists could sometimes find 40 or more frogs at some of these sites, we were only able to locate two frogs at a single locality. This represents a precipitous decline over a period of <15 years. The decline seems to have been caused by a combination of local factors, including (1) the presence of non-native, predatory fish which have restricted habitat and limited dispersal of frogs; (2) loss of breeding habitat due to a five-year drought; and (3) the gradual loss of open meadows and associated aquatic habitats. The loss of frogs suggests that some common management practices in parks and wilderness areas may be endangering some of the species these areas are intended to protect. Similar local factors may account for amphibian declines reported elsewhere and should be carefully evaluated along with possible global effects.
For a period of 2.5 years groups of male and female rainbow trout were subjected to light cycles of 3, 6, 9 or 12 months. Both sexes responded to successive 6-, 9- and 12-month cycles in a reliable fashion. Synchronization of individuals within groups increased from cycle to cycle. The spawning pattern of the 3-month group was erratic. The amount of both spermatozoa and eggs yielded per spawning season was highest in the 9-month group. On a yearly basis, maximum sperm output per male was achieved by subjecting them to a light program foreshortened to 9 months. In females maximum output was obtained under a 6-month program. The fertilizing capacity of gametes of either sex was unimpaired by foreshortened light cycles. From a practical point of view a major problem encountered is one of fish health. Due to an increased frequency of stripping, individuals undergo repeated states of physiological exhaustion. This is particularly true for males which, when spent, are prone to disease, especially Saprolegnia infection.
IN VERTEBRATES, four major systems of intercellular communication exist: the neural, the endocrine, the neuroendocrine, and the immune system. For many years evidence has accumulated linking the neural, the endocrine, and the neuroendocrine systems, but the immune system was often viewed as essentially autonomous. The enormous recent increase in our knowledge of how the immune system is regulated has led many scientists to postulate that this autonomy may be more apparent than real: that the immune system is subject to endocrine and neural control, and that it exerts, in turn, a reciprocal effect on neuroendocrine systems. In this review we intend to examine the interactions between the immune system and the hypothalamic-pituitary-adrenal (HPA) axis. In the first part of the review we will discuss products and components from the immune system that stimulate or inhibit the HPA axis. These include monokines and lymphokines, i.e. the regulatory secretions of the immune system, and other peptides such as ACTH and β-endorphin, more frequently associated with endocrine tissues but which may also be produced by immunologically reactive cells. In the second part we will examine the reciprocal arm of this relationship, i.e. the products of the pituitary and adrenal gland that can stimulate or inhibit the immune system. We will also touch briefly on the possibility that these interactions may be involved in certain autoimmune diseases. Table 1 and Fig. 3 present a brief overview of the major topics covered in this review. The table and the figure are intended to be complementary and should be consulted together.
Calicivirus isolations were made from 4 poikilothermic species in a zoologic collection. Viruses were recovered from 8 asymptomatic Aruba Island rattlesnakes (Crotalus unicolor; rectal swab samples) and from 8 symptomatic animals (4 Aruba Island rattlesnakes, 2 Bell's horned frogs [Ceratophrys orata], 1 rock rattlesnake [C lepidus], and 1 eyelash viper [Bothrops schlegeli] tissue samples obtained at necropsy). On the basis of cross-neutralization test results, the 16 isolates were antigenically indistinguishable and were considered to represent a unique calicivirus serotype, tentatively designated reptilian calicivirus Crotalus type 1. These isolations could not be associated causally with any specific disease entity either in naturally infected poikilotherms or in experimentally infected snakes and pigs.
The larvae of seven species of anurans differ significantly in their abilities to discriminate between kin and nonkin. The ontogeny of kin recognition in certain species is greatly influenced by the environment in which they are reared. In other species, the rearing regime has little affect on the development of kin recognition. Larvae of some anurans develop a kin recognition system in the absence of cues from other individuals. Natural conditions of embryonic development, larval dispersal characteristics, and aggregation behavior are correlated with the kin recognition system of most anurans examined. However, these ecological characteristics are not consistent with the kin recognition systems displayed by a few species. Warning relatives, through the release of chemical signals, and enhancement of growth and development are potential functions of kin association. Intraspecific competition and cannibalism directed toward nonkin are possible functions of kin recognition.
Article de synthese sur le premier Congres Mondial d'Herpetologie (Canterbury, U.K., Septembre 1989) concernant le declin de nombreuses especes d'amphibiens de par le monde. Plusieurs exemples, discussion sur les causes possibles et les strategies a suivre
Microstructure of moulted carp eggs infested with Saprolegnia
- Gajdusek
Gajdusek, J & Rubcov, V. (1985). Microstructure of moulted carp eggs infested with Saprolegnia. Folia Zool., 34, 349-55.
Atlas of Oregon Lakes Largemouth bass Micropterus salmoides learn to avoid feeding on toad Bufo tadpoles
- D M Johnson
- R R Peterson
- D R Lycan
- J W Sweet
- M E Neuhaus
- A L Schaedel
Johnson, D.M., Peterson, R.R., Lycan, D.R., Sweet, J.W., Neuhaus, M.E. & Schaedel, A.L. (1985). Atlas of Oregon Lakes. Oregon State University Press, Corvallis. Kruse, K.C. & Stone, B.M. (1984). Largemouth bass Micropterus salmoides learn to avoid feeding on toad Bufo tadpoles. Anim. Behav., 32, 1035-9.
Rana pipiens (leopard frog) predation
- Cochran
Cochran, P.A. (1983). Rana pipiens (leopard frog) predation. Herpetol. Rev., 14, 18-19.
1989 Progress re-port--Past distribution and current status of the spotted frog in western Washington 1990 progress re-port--Past distribution and current status of the spotted frog in western Washington
- K R Mcallister
- B Leonard
- Olympia
- K R Mcallister
- B Leonard
McAllister, K.R. & Leonard, B. (1990). 1989 Progress re-port--Past distribution and current status of the spotted frog in western Washington. Washington Department of Wildlife, 1989 Progress Report, Olympia. McAllister, K.R. & Leonard, B. (1991). 1990 progress re-port--Past distribution and current status of the spotted frog in western Washington. Washington Department of Wildlife, 1990 Progress Report, Olympia.
Threatened amphibians and reptiles in Europe European Committee for the Conservation of Nature and Natural Resources-Council of Europe, Akademische Verlagsgesellsehaft Are renal carcinomas increasing in Rana pipiens after a decade of reduced prevalence? Amer
- R E Honegger
- Wiesbaden
- B R Hunter
- D L Carlson
- E D Seppanen
- P S Killian
- B K Mckinnell
- R G Mckinnell
Honegger, R.E. (1978). Threatened amphibians and reptiles in Europe. European Committee for the Conservation of Nature and Natural Resources-Council of Europe, Akademische Verlagsgesellsehaft, Wiesbaden. Hunter, B.R., Carlson, D.L., Seppanen, E.D., Killian, P.S., McKinnell, B.K. & McKinnell, R.G. (1989). Are renal carcinomas increasing in Rana pipiens after a decade of reduced prevalence? Amer. Midl. Nat., 122, 307-12.
Parasitism of spadefoot tadpoles by Saprolegnia
- Bragg
1989 Progress report—Past distribution and current status of the spotted frog in Western Washington
- McAllister
The ecological and behavioral dynamics of breeding in three sympatric anuran amphibians
- Olson
1990 progress report—Past distribution and current status of the spotted frog in Western Washington
- McAllister
The northern leopard frog—endangered in Alberta
- Roberts