Haemogregarine Blood Parasites In Triggerfish And Surgeonfish: Distribution, Transmission & Implications For Their Host Fish

Lynda Curtis (2010). Haemogregarine Blood Parasites In Triggerfish And Surgeonfish: Distribution, Transmission & Implications For Their Host Fish PhD Thesis, School of Biological Sciences, The University of Queensland.

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Author Lynda Curtis
Thesis Title Haemogregarine Blood Parasites In Triggerfish And Surgeonfish: Distribution, Transmission & Implications For Their Host Fish
School, Centre or Institute School of Biological Sciences
Institution The University of Queensland
Publication date 2010-03
Thesis type PhD Thesis
Supervisor Dr Alexandra Grutter
Dr Robert Adlard
Dr Malcolm Jones
Professor Angela Davies
Dr Nico Smit
Total pages 145
Total colour pages 7
Total black and white pages 138
Subjects 06 Biological Sciences
Abstract/Summary Haemogregarines are apicomplexan, protozoan parasites that have been documented in the blood of many vertebrate hosts including birds, snakes, lizards, frogs and fishes. Previous reports have focussed on haemogregarine morphology, hosts and locality with relatively little information pertaining to parasite transmission and consequences of infection for the host. While there have been some surveys and a few reports of haemogregarines in coral reef fishes, studies examining likely vectors in a coral reef system and the effect of haemogregarines on their coral reef fish hosts are lacking. Therefore using several triggerfish and surgeonfish species as model hosts for haemogregarines, surveys and experiments on triggerfishes and surgeonfishes inhabiting coral reefs in Indonesia, the Great Barrier Reef (GBR), South East Queensland and French Polynesia were conducted and the relationship between haemogregarines and their hosts was examined. Initially the distribution of haemogregarines in triggerfishes across several locations in the Indo-Pacific was determined by examining fish blood films. Many species of triggerfish were infected with Haemogregarina balistapi. Within the model host group, the flag-tailed triggerfish, Sufflamen chrysopterum, H. balistapi infection intensity and prevalence varied among these locations. When H. balistapi was quantified in a population of S. chrysopterum at Lizard Island on the GBR, differences were not found in parasite intensity and prevalence over the 17 month sampling period. Possibly, the spatial variation in infection intensity is related to variation in water temperature or vector abundance among locations. The intensity of H. balistapi infections in the blackbar triggerfish, Rhinecanthus aculeatus and S. chrysopterum at Lizard Island did not vary with the standard length (SL) of the host fish. However, the prevalence of H. balistapi infections did vary as the SL of non-parasitised S. chrysopterum and R. aculeatus at Lizard Island was significantly higher than parasitised fish. Larger non-parasitised fish might have been expected if H. balistapi were detrimental to their hosts and affected their growth, or if the fish becomes resistant to the infection with increasing age. Although the vectors of haemogregarines among coral reef fish are unknown, previous studies in rocky reef systems in Europe and South Africa suggest that juvenile ectoparasitic stages of gnathiid isopods could be potential vectors. Therefore, whether gnathiid isopods are the definitive hosts of H. balistapi at Lizard Island on the GBR was examined. While blood-sucking, juvenile gnathiids were found on many fishes, no other possible vector, such as a leech, was detected on fish. Furthermore, when the triggerfish R. aculeatus was kept in a gnathiid-free environment in the laboratory, the intensityof their H. balistapi infections decreased when compared with tagged fish in the wild. This supported the idea that gnathiids are potential vectors of H. balistapi and that the host fish may need continued contact with the vector for infections to persist in the vertebrate host population. Whether the life cycle of H. balistapi could be completed in a gnathiid was then examined. Cultured juveniles of Gnathia aureamaculosa were fed on the blood of the triggerfish R. aculeatus infected with H. balistapi and squashes of gnathiids and blood smears from the fish were prepared over the following days. Gnathiid squashes contained mature haemogregarine gamonts, like those seen in the fish blood smears, as well as haemogregarine developmental stages including oocysts, sporozoites, meronts and merozoites. This provided very strong evidence that G. aureamaculosa is a definitive host for H. balistapi and that this, and possibly other gnathiids, have the potential to act as vectors of this haemogregarine. Despite increasing evidence that gnathiids may act as vectors of haemogregarines, until this study, biological transmission experiments in a coral reef system had not been conducted. Therefore, for the first time, this study tested whether G. aureamaculosa transmitted H. balistapi and a second fish haemogregarine Haemogregarina bigemina to recipient triggerfish S. chrysopterum and the yellowfin surgeonfish, Acanthurus xanthopterus. Two possible modes of transmission to the clean fish under test were investigated: 1) by ingestion of gnathiids (recipient fish=32) and 2) by bite through gnathiid feeding activity (recipient fish=3). Recipient fish S. chrysopterum and A. xanthopterus were reared from larvae and did not have any detectable haemogregarines before exposure to gnathiids. Uninfected gnathiids were obtained by allowing them to feed on the thick-lipped wrasse, Hemigymnus melapterus, a fish species that has never been found to be infected with haemogregarines; recipients exposed to control gnathiids did not become infected with haemogregarines. Gnathiids were exposed to H. balistapi by allowing them to feed on a donor triggerfish R. aculeatus and gnathiids exposed to H. bigemina were obtained by allowing them to feed on a donor surgeonfish, the twotone tang, Zebrasoma scopas. A single specimen of the surgeonfish A. xanthopterus, that had ingested gnathiids that had fed on the donor surgeonfish Z. scopas that was infected with H. bigemina, was found later to be carrying H. bigemina. However, this conclusion is questionable as a second recipient A. xanthopterus that had ingested gnathiids from the donor triggerfish R. aculeatus infected with H. balistapi, was also found to be carrying H. bigemina. One explanation, of four possible proposed hypotheses, is that because of their feeding patterns gnathiids may carry mixed infections of haemogregarines that can be carried between gnathiid generations resulting in the unexpected H. bigemina infection. Finally, a third recipient A. xanthopterus was found to be carrying H. bigemina after gnathiids fed on a donor surgeonfish infected with this parasite had also fed on its blood. This result supports the idea that gnathiids transmit haemogregarines by bite. However, as not all gnathiids were recovered during these trials, it is possible that recipient fish also ingested some gnathiids during the experiments. While it appears that H. bigemina was transmitted to the recipient surgeonfish, whether it was through ingestion of the gnathiid by the fish or the bite of the gnathiid while feeding on the fish can not be determined with absolute certainty from these experiments. However, that H. bigemina was also found in a fish that theoretically was not exposed to gnathiids carrying this parasite, deserves further explanation and demonstrates that more studies are needed to determine how gnathiids transmit haemogregarines. Infections of H. balistapi were not detected in any of the recipient triggerfish S. chrysopterum or surgeonfish A. xanthopterus, Z. scopas or the orangespot surgeonfish, Acanthurus olivaceous. The apparent failure to transmit H. balistapi to the surgeonfish is not surprising as surgeonfish, while known hosts of H. bigemina, are not known to be a natural host of H. balistapi. The effect of haemogregarines on their vertebrate hosts, though poorly studied overall, apparently varies greatly among animal groups with some impacting significantly on several measures of condition, behaviour and physiology, with others appearing to have little effect. Here, the evaluated effect of H. balistapi on the triggerfishes R. aculeatus and S. chrysopterum was examined at Lizard Island and Moorea Island. It was noted that H. balistapi may cause destruction of the host red blood cells as the parasite often appeared to be lying adjacent to the remains of host cells. Measures of condition, haematocrit and oxygen consumption were significantly higher in parasitised R. aculeatus from Lizard Island when compared to the non-parasitised R. aculeatus at Moorea Island. The elevated levels of condition and haematocrit of the parasitised R. aculeatus, while unusual, were not thought to be detrimental for the host fish. However, the higher rate of oxygen consumption in parasitised fish, may indicate that H. balistapi does have an effect on the host. The rate of oxygen consumption in a vertebrate, can be used as a proxy for metabolic rate. Therefore, in the current study, the higher oxygen consumption rate of the parasitised fish equates to an increased metabolism and consequently increased energy requirements. It is therefore suggested that parasitised R. aculeatus may need to spend more time foraging for food to meet their increased energy requirements, which may expose them to a greater risk of predation. It is recognised, however, that the R. aculeatus from Lizard Island and Moorea Island could have differed in more than one factor and this could have contributed to the differences in condition, haematocrit and oxygen consumption that were observed. No differences were observed in the condition, haematocrit and oxygen consumption of the parasitised and non-parasitised S. chrysopterum examined at Lizard Island. However, this may have been due to the smaller sample size as only a limited number of non-parasitised S. chrysopterum were available at this site. In conclusion, H. balistapi was detected in several species of triggerfishes throughout the Indo-Pacific and varied in intensity and prevalence across this region. While H. balistapi underwent development in juvenile G. aureamaculosa, transmission experiments attempting to transmit haemogregarines to triggerfish and surgeonfish also provided the most conclusive information to date to support the hypothesis that gnathiid isopods are the vector in these fish species. However, the appearance of a haemogregarine species in a fish, different from the haemogregarine species the presumptive gnathiid vector was exposed to, raises questions about the validity of the above conclusion. Future studies should investigate haemogregarine development in the different life cycle stages of gnathiids to determine their potential for carrying several haemogregarine species between gnathiid generations. While the measures of condition, haematocrit and oxygen consumption where higher in parasitised R. aculeatus, it was suggested that only the increased oxygen consumption rates could be detrimental for the host fish. Therefore, this indicated that H. balistapi may have a significant affect on the survival of R. aculeatus. However, it is unclear from this study whether the increased oxygen consumption rates may be due to H. balistapi infections alone or whether other factors may also be involved. This study increased our knowledge of the ecology of haemogregarines, and their interactions with their hypothesized vectors, gnathiid isopods, and will further our understanding of the ecological role of haemogregarines in coral reef fishes.
Keyword Haemogregarines, fish, gnathiids, transmission, parasitic
Additional Notes Pages to be printed in colour:42, 65, 66, 67, 68, 78, 93 Pages to be printed landscape: 64, 70, 71, 74, 76, 128, 129, 130, 131, 132, 133, 134, 135, 136, 137, 138, 139, 140, 141, 142, 143, 144, 145

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Created: Fri, 26 Mar 2010, 10:52:07 EST by Miss Lynda Curtis on behalf of Library - Information Access Service