Lee Berger and Rick
Speare
School of Public
Health and Tropical Medicine
James Cook University
Townsville 4811
Australia.
Pathogenic protozoa
Amphibians have a large range of protozoa, many of which appear to be commensuals in the gastrointestinal tract. Only the potentially pathogenic protozoa are mentioned in this section. Most research has been done on taxonomy of the protozoa and very little on pathogenicity and biology.
Microsporidia
The microsporidian, Pleistophora myotrophica, caused high mortality rates in captive B. bufo (Canning et al 1964). This parasite infected all striated muscles resulting in atrophy and emaciation. White streaks between muscle fibres were obvious grossly, and microscopically these were spaces in the muscle fibres packed with microsporidian spores. Muscle regeneration occurred with long chains of sarcoblasts adjacent to damaged muscle. Experimental infections were achieved by feeding toads infected muscle. Tadpoles did not become infected experimentally but their development was arrested. Only one of 12 experimental R. temporaria became infected and had spores in the tongue, whereas 100% of B. bufo were infected.
A captive, wild-caught Phyllomedusa bicolor was successfully treated for an ulcerative dermatitis that was associated with a variety of infective agents including microsporidia (Graczyk et al 1996). The microsporidia were not identified.
Myxidium
Although
the myxozoan parasite Myxidium immersum
has not been associated with mortality, it is included here as it was
introduced to Australia with the cane toad. M.
immersum has low host specificity and has spread into native frog species.
It has been recorded in 12 species of Litoria,
4 species of Limnodynastes, and one
each of Mixophyes, Ranidella, and Uperoleia. The large immobile trophozoites (1-5 mm) are found
freely floating in bile in the gall bladder (Delvinquier 1986).
Trypanosomes
Over 60 species of trypanosomes
have been reported in anurans but the taxonomy is confused (Bardsley and
Harmsen 1973). Most infections are non-pathogenic. Trypanosoma inopinatum is the only trypanosome of anurans whose
pathogenicity has been well studied. Experimental infections with the blood
borne flagellate were lethal to European green frogs and caused
haemorrhages, swollen lymph glands and anaemia (Brumpt 1924). Death resulted
from destruction of the reticulo endothelial system. The lymph fluid was abundant and contained numerous trypanosomes
agglutinated in rosettes with the flagellates in the centre (Brumpt 1924; Bardsley
and Harmsen 1973). T. rotatorium can
be pathogenic in tadpoles or in heavy infections, with trypanosomes
accumulating in the kidneys (Bardsley and Harmsen 1973). T. pipientis causes spleen enlargement but rarely causes death
(Flynn 1973). Trypanosomes are quite common in frogs from Queensland, but none
has been associated with disease (Delvinquier
and Freeland 1989).
Myxobolus hylae
Myxobolus
hylae was found in the
reproductive organs of L. aurea from
Sydney (Johnston and Bancroft 1918). Infected frogs appeared sickly and
emaciated. The testes and vasa efferentia were infected in males and the
oviducts were infected in females. High prevalences were observed with
infections in 7/7 males and 2/~ 23 females. In cases of heavy infection, the
whole testis was swollen and covered with white cysts up to 2‑3 mm
composed of myriads of spores (Johnston and Bancroft 1918).
Ichthyophonus-like organisms
Myositis associated with infection by Ichthyophonus-like organisms was reported in wild amphibians collected in Quebec, Canada, from 1959 to 1964 and 1992 to 1999 (Mikaelian et al 2000). Infection was diagnosed in 6 species (frogs Rana clamitans, R. sylvatica, R. catesbeiana, R. palustris, Pseudacris crucifer, and newts Notophthalmus viridescens). Spores of the organisms invaded striated muscle fibers and were associated with variable degrees of granulomatous and eosinophilic inflammation. Infection was considered fatal in 2 green frogs, 1 wood frog, and 1 red-spotted newt. It was considered potentially significant in 3 additional green frogs in which up to 100% of the fibres of some muscles were replaced by spores associated with a severe granulomatous reaction. This report shows that ichthyophonosis is enzootic in amphibians from Quebec.
Pathogenic Helminths
Many helminth species infect amphibians, and some cause disease with heavy burdens. The pathogenic effects of trematodes, cestodes and nematodes are reviewed in detail by Flynn (1973). Disease is common in captivity but none has been reported to cause epidemics in the wild. Amphibians have a depauperate helminth fauna with low diversity and low infection levels compared to other vertebrates (Barton and Richards 1996). This may be due to host specificity of the parasites or to aspects of host biology (Barton and Richards 1996).
Rhabdias
Rhabdias is a genus of parasitic
nematode found in commonly in the lungs of anuran amphibians (Flynn 1973).
Usually they are incidental findings but heavy experimental infections can
cause disease (Tinsley 1995). Experimental transmission of Rhabdias
bufonis to B. bufo resulted in a dose dependent decrease in growth
rates, fitness and survival (Tinsley 1995). B. marinus
were placed on a culture of infective larvae of R. sphaerocephala which rapidly
burrowed through the skin and the toads died overnight (Williams 1960). The
skin had numerous tufts of cast nematode skins. Hundreds of larvae were found
internally including heart muscle, liver and eye (Williams 1960). Larvae may reach
the lungs indirectly via the blood stream or by direct migration to the lungs.
Some larvae do not reach the lungs and encyst in other organs. These aberrant migrating larvae incite granuloma formation
that may affect the host (Reichenbach-Klinke and Elkan 1965). Only a small
proportion of wild amphibians have heavy burdens (Tinsley 1995). In Australia R.
hylae is the most widespread species (Barton
1994).
Pseudocapillaroides xenopi
Pseudocapillaroides
xenopi is a capillarioid nematode
that burrows in the epidermis. Infection resulted in deaths in captive X. laevis. Bacterial and fungal
opportunists contributed to the pathogenesis. Clinical signs developed over
four months and included ulcers, sloughing of the epidermis, erythema and
weight loss (Cunningham et al 1996b; Brayton 1992).
Filarioids
Foleyella spp. can cause death due to heavy infections with microfiliaria or adult worms (Reichenbach-Klinke and Elkan 1965). Infections may occur at high prevalence in a population and appear asymptomatic. Foleyella confusa and Icosiella hoogstraali were described from Philippine amphibians (Schmidt and Kuntz 1969), but no details about their pathology were given.
Spargana
Spargana are the intermediate stage of cestodes (Order Pseudophyllidea) that occur in frogs worldwide (Flynn 1973). They are potentially pathogenic but their effects in frogs have not been well studied. The adult stage of the cestode, Spirometra erinacei (the only species of pseudophyllidean cestode known to occur in Australia), inhabits the small intestine of carnivores such as dog, cat, fox and dingo. The procercoid stage occurs in copepods and the plerocercoid stage (spargana) is found in tadpoles and adult frogs that ingest infected copepods (Sandars 1953).
In Australian amphibians, spargana have been reported in wild adults of B. marinus, L. aurea, L. caerulea, L. nasuta and L. rubella (Barton 1994; Sastrawan 1978), and experimental infections were produced in adults of L. latopalmata and Limnodynastes tasmaniensis and tadpoles of L. latopalmata, L. caerulea and L. tasmaniensis (Bennett 1978; Sastrawan 1978; Sandars 1953). Sandars (1953) reported that about one quarter of the population of L. caerulea in the Brisbane area was infected with spargana. In a group of 1000 B. marinus from Ingham, Queensland, 37 (3.7%) were found with infections of spargana provisionally called S. mansoni (Bennett 1978). These toads had light infections, an average of 6.3 spargana per toad with 59% spargana found in thighs. There was a marked local inflammatory response in these toads and over half the spargana were dead. Immunodiffusion and immuno-electrophoretic tests in the toads revealed antibodies were produced to components of the spargana. Attempts to study the reactions in experimental L. tasmaniensis failed due to inconsistent infection rates and frequent deaths of infected frogs and tadpoles, which were thought to be due to the combined stress of parasitism and captive conditions (Bennett 1978). Growth of experimentally infected L. latopalmata tadpoles was inhibited (Sandars 1953). In a survey of 948 Malaysian frogs, 11.8 % were found infected with spargana, 57% of which had bleeding and/or swelling at infection sites (Mastura et al 1996).
Trematode metacercaria
Metacercariae of various
trematode species occur in tadpoles and frogs. The definitive host may be
snakes, frogs, birds or mammals (Reichenbach-Klinke and Elkan 1965). Usually
encysted larvae are not pathogenic although infections have been found in vital
organs such as eyes, heart, liver, lung and CNS where they may cause disease.
Metacercariae of Neascus group
encysted in the dermis along the lateral line system of captive adults of X. laevis, leading to paralysis and
death (Elkan and Murray 1951). Diplostomulum
xenopi infected the pericardial cavity of X. laevis causing pericarditis, respiratory distress and death
(Flynn 1973). Heavy experimental infections with Cercaria ranae caused bloat in tadpoles (Cort and Brackett 1938).
Acanthocephala
The spines of acanthocephala inhabiting the stomach and intestine of frogs can cause perforation and death. Acanthocephalus ranae is a common species in Europe (Reichenbach-Klinke and Elkan 1965).
Pathogenic arthropods
Diptera
Various
fly species from the families Sarcophagidae, Calliphoridae and Chloropidae have
larvae that can develop within amphibians (Reichenbach-Klinke and Elkan 1965;
Crump and Pounds 1985). The “toad fly” Bufolucilia
bufonivora lays eggs in the nostrils of toads and the larvae destroy the
epithelium and can penetrate deeper into the orbit or brain. Few toads survive
an infection (Reichenbach-Klinke and Elkan 1965). Larvae of Notochaeta bufonivora parasitised wild A. varius along a stream in Costa Rica
during the dry season. Frogs in early stages of myiasis had a single small wound
on the posterior surface of one thigh, and all hosts died within four days
after they were found. Female frogs were parasitised more often (Crump and Pounds 1985).
Larvae of Notochaeta
sp. infected farmed R. catesbiana
in Brazil. Larvae occurred in the mouth and caused necrotic perforations
associated with a range of aerobic and anaerobic bacteria including Clostridium spp. (Baldassi et al 1995).
In Australia the genus Batrachomyia contains several species
that have been found in 11 frog species (Elkan 1965). They inhabit the dorsal
lymph sac with their posterior spiracles in or close to a hole in the frog’s
skin. When they are ready to pupate they leave the frog and drop to the ground.
The number of maggots (1-5) is much less than seen with B. bufonivora, suggesting the eggs are not laid directly on frog
skin but are picked up from the soil. Frogs are reported to have survived
infection and had little obvious tissue damage, although death can result at
the time of larval emergence (Elkan 1965; Vogelnest 1994). Especially with
small frogs, the hole left in the skin after escape of the maggot would be
expected to seriously affect the frog. A Pseudophryne
bibronii was found with a perforation of the peritoneal wall and the
rostral end of the maggot lay within the peritoneal cavity (Elkan 1965). A L. caerulea infected with a larva of B. mertensis was in poor body condition
and did not eat well until the larva was surgically removed (Vogelnest 1994).
Arachnids
Larval trombiculid mites infect the skin of frogs and toads and cause small vesicles in the skin (Flynn 1973). Ticks of the genus Amblyomma occur on B. marinus in Central and South America. They occur on all areas of the body and cause transient focal congestion and haemorrhage. Ticks have not been found on B. marinus in Australia or on native amphibians (Speare 1990).
Updated 16 February, 2003
Rick Speare