Altitudinal distribution of chytrid (Batrachochytrium dendrobatidis) infection in subtropical Australian frogs

The disappearance of amphibian populations from seemingly pristine upland areas worldwide has become a major focus of conservation efforts in the last two decades, and a parasitic chytrid fungus, Batrachochytrium dendrobatidis, is thought to be the causative agent of the population declines. We examined the altitudinal distribution of chytrid infections in three stream‐dwelling frog species (Litoria wilcoxii, L. pearsoniana and L. chloris) in southeast Queensland, Australia, and hypothesized that if B. dendrobatidis were responsible for the disappearance of high‐altitude frog populations, infection prevalence and intensity would be greatest at higher altitudes. Overall, 37.7% of the 798 adult frogs we sampled were infected with B. dendrobatidis, and infections were found in all the populations we examined. Contrary to our initial hypothesis, we found no consistent evidence that high‐altitude frogs were more likely to be infected than were lowland frogs. Further, the intensity of fungal infections (number of zoospores) on high‐altitude frogs did not differ significantly from that of lowland frogs. Batrachochytrium dendrobatidis appears to be capable of infecting frogs at all altitudes in the subtropics, suggesting that all populations are at risk of decline when conditions favour disease outbreaks. We did find evidence, however, that chytrid infections persist longer into summer in upland as compared with lowland areas, suggesting that montane amphibian populations remain susceptible to disease outbreaks for longer periods than do lowland populations. Further, we found that at high altitudes, temperatures optimal for chytrid growth and reproduction coincide with frog metamorphosis, the life‐stage at which frogs are most susceptible to chytrid infections. While these altitudinal differences may account for the differential population‐level responses to the presence of B. dendrobatidis, the reason why many of southeast Queensland's montane frog populations declined precipitously while lowland populations remained stable has yet to be resolved.     

Temperature Alters Host Genotype-Specific Susceptibility to Chytrid Infection

The cost of parasitism often depends on environmental conditions and host identity. Therefore, variation in the biotic and abiotic environment can have repercussions on both, species-level host-parasite interaction patterns but also on host genotype-specific susceptibility to disease. We exposed seven genetically different but concurrent strains of the diatom Asterionella formosa to one genotype of its naturally co-occurring chytrid parasite Zygorhizidium planktonicum across five environmentally relevant temperatures. We found that the thermal tolerance range of the tested parasite genotype was narrower than that of its host, providing the host with a “cold” and “hot” thermal refuge of very low or no infection. Susceptibility to disease was host genotype-specific and varied with temperature level so that no genotype was most or least resistant across all temperatures. This suggests a role of thermal variation in the maintenance of diversity in disease related traits in this phytoplankton host. The duration and intensity of chytrid parasite pressure on host populations is likely to be affected by the projected changes in temperature patterns due to climate warming both through altering temperature dependent disease susceptibility of the host and, potentially, through en- or disabling thermal host refugia. This, in turn may affect the selective strength of the parasite on the genetic architecture of the host population.     

Warming accelerates termination of a phytoplankton spring bloom by fungal parasites

Climate change is expected to favour infectious diseases across ecosystems worldwide. In freshwater and marine environments, parasites play a crucial role in controlling plankton population dynamics. Infection of phytoplankton populations will cause a transfer of carbon and nutrients into parasites, which may change the type of food available for higher trophic levels. Some phytoplankton species are inedible to zooplankton, and the termination of their population by parasites may liberate otherwise unavailable carbon and nutrients. Phytoplankton spring blooms often consist of large diatoms inedible for zooplankton, but the zoospores of their fungal parasites may serve as a food source for this higher trophic level. Here, we investigated the impact of warming on the fungal infection of a natural phytoplankton spring bloom and followed the response of a zooplankton community. Experiments were performed in ca. 1000 L indoor mesocosms exposed to a controlled seasonal temperature cycle and a warm (+4 °C) treatment in the period from March to June 2014. The spring bloom was dominated by the diatom Synedra. At the peak of infection over 40% of the Synedra population was infected by a fungal parasite (i.e. a chytrid) in both treatments. Warming did not affect the onset of the Synedra bloom, but accelerated its termination. Peak population density of Synedra tended to be lower in the warm treatments. Furthermore, Synedra carbon: phosphorus stoichiometry increased during the bloom, particularly in the control treatments. This indicates enhanced phosphorus limitation in the control treatments, which may have constrained chytrid development. Timing of the rotifer Keratella advanced in the warm treatments and closely followed chytrid infections. The chytrids' zoospores may thus have served as an alternative food source to Keratella. Our study thus emphasizes the importance of incorporating not only nutrient limitation and grazing, but also parasitism in understanding the response of plankton communities towards global warming.     

Some Observation on the Alga Fragilaria crotonensis Kitton and its Parasitism by Two Chytridiaceous Fungi

It has been shown by experimentation that two morphologicallydistinct clones of Fragilaria crotonensis Kitton, isolated fromthe plankton of Windermere at approximately the same time, wereaffected quite differently by the chytrid Rhizophydium fragilariaeCanter. In one case the diatom filaments became heavily parasitizedand could be used for the maintenance of the fungus. In theother case infection was negligible. Additional clones, representative of these two morphologicalforms, from other bodies of water in the Windermere drainagebasin were tested. The same pattern of infection or relativenon-infection again ensued in direct accordance with the particulartype of filament used. Some preliminary experiments undertaken with a second, as yetlittle known chytrid parasite of F. crotonensis are reported.In this instance the fungus appeared to find its natural hoston cells belonging to the morphological form which failed tosupport the continued increase of R. fragilariae. The parasitism of morphological variants of F. crotonensis bythese fungi in the wild from Britain and else where is discussed. Fragilaria crotonensis Kitton, Rhizophydium fragilariae Canter, chytrid, diatom, parasitism, culture     

How Does Chytrid Infection Vary Among Habitats? The Case of Litoria wilcoxii (Anura, Hylidae) in SE Queensland, Australia

Most analyses dealing with the geographical distribution of the chytrid fungus (Batrachochytrium dendrobatidis) have been performed on large geographical scales and data on more localized distribution of the chytrid within catchments are scarce. In this study, we compare the prevalence and intensity of infection of chytrid within and outside rainforest habitats at five independent catchments in southeast Queensland. In each catchment, we sampled adult Litoria wilcoxii along two transects on the same stream: one in forested areas, and the other in open nearby farmland. We analyzed swabs using quantitative PCR techniques. Male frogs were in higher densities in open habitats compared with the nearby forested areas. Infected male frogs were found in all catchments surveyed; however, prevalence of B. dendrobatidis in adult males was higher in the forested habitats than in the open habitats in four of the catchments. There was no significant difference in intensity of infection between forested and open habitats. For adult females and juveniles, sample sizes were not high enough for comparisons. Our results suggest that habitat influences chytrid prevalence and open areas may provide refuge from chytrid-induced population declines.     

Performance of moth larvae on birch in relation to altitude, climate, host quality and parasitoids

We studied topographical and year-to-year variation in the performance (pupal weights, survival) and larval parasitism of Epirrita autumnata larvae feeding on mountain birch in northernmost Finland in 1993–1996. We found differences in both food plant quality and parasitism between sites ranging from 80 m to 320 m above sea level. Variation in food plant quality had particularly marked effects on larval survival. The advanced phenology of the birches in relation to the start of the larval period reduced pupal weights. Parasitism rates were different between years and between sites. The clearest site differences were in the proportions of different parasitoid species: Eulophus larvarum was most abundant at the lowest-altitude sites, and Cotesia jucunda at the highest. Differences in the performance of E. autumnata were related to temperature conditions: at higher temperatures, survival and the egg production index were lower, and larval parasitism was higher than at lower temperatures. The higher parasitism at higher temperatures was probably due to greater parasitoid activity during warmer days. In the comparison of different sources of spatial and annual variation in the performance of E. autumnata, the most important factor appeared to be egg mortality related to minimum winter temperature, followed by parasitism and, finally, the variation in food plant quality. If, as predicted, the climate gradually warms up, the effects of warmer summers on the outbreaks of E. autumnata suggest a decrease in outbreak intensity. Received: 4 January 1999 / Accepted: 22 March 1999     

The Isolation, Maintenance and Host Range Studies of a Chytrid Rhizophydium planktonicum Canter emend., Parasitic on Asterionella formosa Hassall

The methods of isolation and maintenance in dual clone cultureof the chytrid Rhizophydium planktonicum Canter emend, parasiticon Asterionella formosa Hass. from the plankton are described.The ability of a single fungal isolate to infect other clonesof Asterionella, Fragilaria, Tabellaria, Synedra and Cyclotella,as well as dead material was also tested. All the clones of Asterionella proved to be highly susceptibleto infection whereas only in rare instances could a sporangiumbe found which had grown and dehisced on Fragilaria and Synedra.Very few zoospores encysted on Tabellaria and Cyclotella andthose which did died without further growth. There was no evidenceto suggest that the chytrid could complete its life historyon dead material. freshwater phytoplankton, culture, parasitism, host–parasite relationships, chytridiomycetes, Rhizophydium, Zygorhizidium, diatoms, Asterionella, Fragilaria     

Possible implications of chytrid parasitism for population subdivision in freshwater cyanobacteria of the genus Planktothrix

Populations of the cyanobacterium Planktothrix comprise multiple coexisting oligopeptide chemotypes that can behave differently in nature. We tested whether this population subdivision can, in principle, be driven by parasitic chytrid fungi, which are almost neglected agents of Planktothrix mortality. Two chytrid strains, Chy-Lys2009 and Chy-Kol2008, were isolated from Planktothrix-dominated lakes in Norway. The two strains shared 98.2% and 86.2% of their 28S and internal transcribe spacer rRNA gene sequences, respectively. A phylogenetic analysis placed them in the order Rhizophydiales family Angulomycetaceae. Chy-Lys2009 and Chy-Kol2008 could completely lyse Planktothrix cultures within days, while they failed to infect other filamentous cyanobacteria. The effect on Planktothrix was chemotype dependent, and both chytrid strains showed distinct chemotype preferences. These findings identify chytrid fungi infecting Planktothrix as highly potent and specialized parasites which may exert strong selective pressure on their hosts. According to established hypotheses on host-parasite coevolution, parasitism with the above properties may result in subdivision of Planktothrix populations into coexisting chemotypes and periodic shifts in the relative Planktothrix chemotype composition. These predictions are in agreement with field observations. Moreover, a genetic analysis verified the co-occurrence of Chy-Lys2009 and Chy-Kol2008 or related chytrid strains along with distinct Planktothrix chemotypes in at least one water body. Our findings are consistent with a scenario where chytrid parasitism is one driving force of Planktothrix population subdivision, which in turn leads to polymorphism in parasitic chytrid fungi. Future studies should test the validity of this scenario under field conditions.     

Simultaneous infection by red rot and chytrid diseases in <Emphasis Type="Italic">Porphyra yezoensis</Emphasis>Ueda

This paper presents the results of a study on the diseases of Porphyra yezoensisUeda along the north coast of China, where red rot (Pythium porphyrae) and the chytrid Olpidiopsis sp. diseases were both found to be present. Infection by the mycelia of Pythium porphyraeand the thallus of Olpidiopsis sp. was studied in detail. At the early stage of infecton the mycelia of Pythium porphyraeand the fungus of chytrid can be found in host cells at the same time. In the middle and late stages of the complication, it mainly appears as red rot disease, toward the end appearing almost completely as red rot disease. The complication even can be found on the cells of fronds from the freeze-storage nori nets. However, the freeze-storage nets can help prevent spread of the infection and improve nori quality.     

Fungal Parasitism: Life Cycle,Dynamics and Impact on Cyanobacterial Blooms

Many species of phytoplankton are susceptible to parasitism by fungi from the phylum Chytridiomycota (i.e. chytrids). However, few studies have reported the effects of fungal parasites on filamentous cyanobacterial blooms. To investigate the missing components of bloom ecosystems, we examined an entire field bloom of the cyanobacterium Anabaena macrospora for evidence of chytrid infection in a productive freshwater lake, using a high resolution sampling strategy. A. macrospora was infected by two species of the genus Rhizosiphon which have similar life cycles but differed in their infective regimes depending on the cellular niches offered by their host. R. crassum infected both vegetative cells and akinetes while R. akinetum infected only akinetes. A tentative reconstruction of the developmental stages suggested that the life cycle of R. crassum was completed in about 3 days. The infection affected 6% of total cells (and 4% of akinètes), spread over a maximum of 17% of the filaments of cyanobacteria, in which 60% of the cells could be parasitized. Furthermore, chytrids may reduce the length of filaments of Anabaena macrospora significantly by “mechanistic fragmentation” following infection. All these results suggest that chytrid parasitism is one of the driving factors involved in the decline of a cyanobacteria blooms, by direct mortality of parasitized cells and indirectly by the mechanistic fragmentation, which could weaken the resistance of A. macrospora to grazing.     

Emerging disease of amphibians cured by elevated body temperature

The emerging infectious disease chytridiomycosis is thought to have contributed to many of the recent alarming declines in amphibian populations. Mortalities associated with these declines have often occurred during cooler seasons and at high elevations, suggesting that environmental temperature may be an important factor in disease emergence. We found that thermal environment affects the progress of the disease, and that housing frogs Litoria chloris at an environmental temperature of 37 degrees C for less than 16 h can clear them of the chytrid pathogen Batrachochytrium dendrobatidis. Our experiment demonstrated that elevated body temperatures similar to those experienced in behavioral fever and during normal thermoregulation can clear frogs of chytrid infection; therefore, variation in thermoregulatory opportunities and behaviors are likely to contribute to the differences in disease incidence observed among host species, populations, and regions. Although further refinement of the technique is needed to encompass various host species, appropriately applied thermal manipulations of amphibians and their enclosures may prove to be a safe and effective way of eliminating the fungal pathogen from captive amphibian populations and: preventing accidental spread of the pathogen when animals are translocated or released from captivity.     

Chytridiomycosis Widespread in Anurans of Northeastern United States

ABSTRACT An emerging disease of amphibians caused by the chytrid fungus Batrachochytrium dendrobatidis has been associated with morbidity, mortality, and extinction of species. Typically, researchers have detected B. dendrobatidis only when examining amphibians for causes of mortalities; few data exist on infection rates where mortalities are lacking. During May-September 2000–2002 we obtained amphibian specimens killed by vehicles and others collected at remote off-road sites throughout Maine, USA, and from federal lands in 5 states in the Northeast. We detected infected specimens, mostly green frogs (Rana clamitans), at 5 of 7 national wildlife refuges, a federal waterfowl production area, and Acadia National Park. Seven of 9 species, including all Ranidae species, were infected throughout Maine; rates ranged from 14.6% in American toads (Bufo americanus) to 25.7% in northern leopard frogs (Rana pipiens). We did not detect any infections in 50 eastern gray tree frogs (Hyla versicolor) or 21 spring peepers (Pseudacris crucifer). Species that hibernate in terrestrial habitats seem to have lower rates of infection than species that hibernate in aquatic habitats. Infections peaked in spring and autumn and were associated with air temperatures optimal for B. dendrobatidis growth. The relatively high infection rates among species without documented die-offs suggest that either losses have occurred undetected, that the fungus is endemic and species have attained a level of resistance to infections becoming lethal, or that climatic conditions of the Northeast have a role in preventing infections from being lethal. Data on prevalence and distribution of this chytrid fungus in the Northeast may be useful in modeling its origins and predicting long-term ecosystem effects involving anurans.     

The effect of fungal parasitism on the succession of diatoms in Lake Maarsseveen I (The Netherlands)

SUMMARY. During late winter and early spring, diatoms are predominant in Lake Maarsseveen I and show a succession in blooming. To elucidate the role of parasitism in this succession, samples were taken once a week in 1978, 1979and 1980 and examined for fungal parasites, further, factors which presumably influenced the phytoplankton growth. including temperature and chemical compounds, were studied. Parasites were found on Asterionella formosa Hass., Stephanodiscus astraea (Ehr) Grun. and Cyclotella comta (Ehr) Kütz. The chytrid fungus Zygorhizidium planktonicum
Canter was parasitic tin Asterionella formosa. This was the only case where high infection percentages were registered. The developmental phases of Zygorhizidium plunktonicum on Asterionella formosa were studied. The fungus was capable of affecting the spring increase and bringing about a premature end to the bloom. Only when the fungus was temporarily inhibited in its parasitic activity (this phenomenon coincided with periods of frost) was A. formosa able to reach a high abundance. Severe parasitism on A. formosa favoured the development of other diatoms (mainly of Fragilaria crotoriensis Kitt., Stephanodiscus hantzschii Grun. and Stephanodiscus astraea) .
Host-parasite interrelationship studies performed in the laboratory showed that temperature can be an important environmental factor associated with epidemics of Zygorhizidium plankiomcum on Asterionella formosa. At very low temepratures (1.5. 1) the fungal activity was inhibited while Asterionella fortnosa still grew well. However, at 5, 10 and 18 the fungus manifested a high infection rate and was able to overtake A sterionella .     

A Further Study on Parasitism of the Diatom Fragilaria crotonensis Kitton by Chytridiaceous Fungi in Culture

Further detailed experiments under laboratory conditions havebeen carried out using clones of Fragilaria crotonensis Kitton.Two morphologically distinct types (rod- and flared-cell forms)were investigated in relation to their infection by a chytridreferred to as species 3. The pathogenicity of the chytrid Rhizophydiumfragilariae Canter towards four newly isolated clones of F.crotonensis was also studied. The results in general confirmedthat clones of the diatom composed of flared-type cells werecompatible with the development and increase of species 3 butremained more or less resistant to R. fragilariae. In contrast,rod-celled type clones showed exactly the opposite host parasiterelationships. Further study has shown that slight differencesin susceptibility towards a particular chytrid can occur withindiatom clones of similar morphological type. The presence ofhypersensitive algal cells was noted in relation to parasitismby both fungi. Some observations are recorded on the developmentof mucilage around filaments of the Fragilaria clones. Fragilaria crotonensis Kitton, Rhizophydium fragilariae Canter, chytrid, diatom, culture, parasitism, hypersensitivity, mucilage envelope     

Microsporidiosis in a Daphnia pulex population

The impact of parasitism by Thelohania sp., an intracellular microsporidian, on Daphnia pulex inhabiting a vernal pond was studied for three years. Three issues were considered: the distribution of parasites among hosts, the effect of parasites on individuals, and the impact of parasitism on population growth. Each year, Thelohania infected members of at least half of the generations of Daphnia produced in the pond. When the frequency of infection was low, parasites were found only in large adults. As infection frequency increased, parasitism spread downward through host size classes. However, parasites were rarely found in juveniles. Parasitism reduced clutch size drastically, increased mortality to a variable extent, had little impact on egg size or on per instar growth and none on molt frequency. Interaction with other stresses, such as food limitation, exacerbated some of these effects. Parasitism reduced instantaneous birth rate much more than it elevated instantaneous death rate. Population growth was reduced significantly but it is unlikely that Thelohania alone regulates the growth of this Daphnia population.     

Environmental Conditions Determine the Course and Outcome of Phytoplankton Chytridiomycosis

Chytrid fungi are highly potent parasites of phytoplankton. They are thought to force phytoplankton organisms into an evolutionary arms race with high population diversity as the outcome. The underlying selection regime is known as Red Queen dynamics. However, our study suggests a more complex picture for chytrid parasitism in the cyanobacterium Planktothrix. Laboratory experiments identified a “cold thermal refuge”, inside which Planktothrix can grow without chytrid infection. A field study in two Norwegian lakes underlined the ecological significance of this finding. The study utilized sediment DNA as a biological archive in combination with existing monitoring data. In one lake, temperature and light conditions forced Planktothrix outside the thermal refuge for most of the growing season. This probably resulted in Red Queen dynamics as suggested by a high parasitic pressure exerted by chytrids, an increase in Planktothrix genotype diversity over time, and a correlation between Planktothrix genotype diversity and duration of bloom events. In the second lake, a colder climate allowed Planktothrix to largely stay inside the thermal refuge. The parasitic pressure exerted by chytrids and Planktothrix genotype diversity remained low, indicating that Planktothrix successfully evaded the Red Queen dynamics. Episodic Planktothrix blooms were observed during spring and autumn circulation, in the metalimnion or under the ice. Interestingly, both lakes were dominated by the same or related Planktothrix genotypes. Taken together, our data suggest that, depending on environmental conditions, chytrid parasitism can impose distinct selection regimes on conspecific phytoplankton populations with similar genotype composition, causing these populations to behave and perhaps to evolve differently.     

Does habitat-specific variation in trematode infection risks influence habitat distribution of two closely related freshwater snails?

Parasitism may be an important factor determining the geographic distribution of closely related species. A habitat-specific risk of parasitism may lead to exclusion of susceptible host types from parasite-rich environments, and promote speciation if it leads to reproductive isolation between susceptible and resistant types. We surveyed populations of the freshwater snail Lymnaea peregra for differences in habitat distribution and trematode parasitism between its two distinct shell morphs, L. ovata and L. peregra. We surveyed 58 populations (43 L. ovata, 15 L. peregra). At each location we recorded an array of habitat characteristics that were summarized using a nonlinear principal components analysis. This yielded two orthogonal habitat score variables. Discriminant analysis with these habitat dimensions indicated that the snail morphs differed in their habitat distribution. L. ovata preferred larger, more permanent natural habitats surrounded by forests, while L. peregra was found more often at a higher altitude, in nonpermanent habitats, often surrounded by meadows. The snails were parasitized by four cercarial types of castrating trematodes. The morphs had a similar prevalence of infection by each of the parasite types, with one exception: monostomid cercariae were found at a higher prevalence in L. ovata than in L. peregra. However, monostomes were rare parasites, and the difference in prevalence of infection was not significant when only populations with monostomes were compared. Our results indicate that variation in the overall prevalence of infection seems to be independent of snail morph, and do not support the idea that a difference in the rate of parasitism might explain differences in the habitat distribution of these snail morphs. Received: 4 January 1999 / Accepted: 30 June 1999     

The effect of parasitism on host fecundity is dependent on temperature in a cockroach-acanthocephalan system

The fitness of infected organisms can vary greatly depending on the temperature at which they find themselves. Understanding the role of temperature in the fitness of infected organisms can be crucial to population studies, epidemiological studies, and when screening for biological control agents. We measured the effect of parasitism on host survival and reproduction at 4 constant temperatures using the acanthocephalan parasite Moniliformis moniliformis and its intermediate host, the cockroach Supella longipalpa. Infection did not affect cockroach survival at any temperature. Infection had a negative impact on cockroach fecundity but only at higher temperatures (28 and 31 C) and only later in infection (>20 days postinfection). At lower temperatures, infected and uninfected cockroaches had similar fecundities throughout the duration of the experiment (120 days). This study, along with previous studies, suggests that researchers would do well to consider environmental variables when exploring the effects of parasitism.     

Distribution and abundance ofErynniopsis antennata [Dipt.: Tachinidae] andTetrastichus brevistigma [Hym.: eulophidae], two introduced elm leaf beetle parasitoids in Northern California

Erynniopsis antennata (Rondani), an introduced larval and larval-adult parasitoid of the elm leaf beetle (ELB),Xanthogaleruca luteola (Müller), was found in 11 of 12 northern California cities whereUlmus procera Salisbury andUlmus pumila L. were sampled in 1986 and/or 1987. Maximum apparent parasitism was over 40% in 4 of the cities, but mean parasitism for all sites combined was 4.5%. An introduced pupal parasitoid,Tetrastichus brevistigma Gahan, was found in only 7 cities, with mean and maximum apparent parasitism of 1.2 and 22%, respectively.E. antennata may be of value in managing ELB populations, but more knowledge of its biology and improved sampling methods are required.