Complex life cycles are a hallmark characteristic of many parasites; however, little is known about the process by which life cycles become more complex through the addition of hosts. Paratenic hosts are present in the life cycles of several phylogenetically distinct groups of helminths; this suggests that they may play a key role during this process. This study examined the development of metacercariae of Halipegus eccentricus within intermediate microcrustacean and odonate paratenic hosts. Then a comparative approach was used to evaluate how life history traits of H. eccentricus within the anuran definitive hosts differ between metacercariae of the same age that developed within an intermediate ostracod host or a paratenic odonate host. The results of this study indicate that metacercariae of H. eccentricus do not grow at the same rate in different intermediate hosts, and significant differences exist in growth within intermediate and paratenic hosts. Individuals from odonate paratenic hosts always had larger bodies and suckers than those of metacercariae of the same age that develop within microcrustacean intermediate hosts. Furthermore, metacercariae from odonates were more successful in establishing and migrating in definitive anuran hosts. Last, individuals from paratenic hosts began reproducing earlier within anuran definitive hosts than age-matched worms that develop within the intermediate hosts. Collectively these results suggest that the variation in body and sucker sizes within odonate and microcrustacean hosts may carry over to the definitive host and in the case of H. eccentricus using the paratenic host increases transmission and alters other life history traits within definitive hosts. These results indicate that using a paratenic host can affect the success of parasites in subsequent hosts, and therefore these hosts may provide benefits other than just increasing transmission by bridging an ecological gap.
Host specificity of parasites is a basic principle in parasitology; however, it is not easily measured. Previously, host specificity was calculated as the number of species that a parasite infected, but this is not an accurate description of host usage because some species are capable of being infected but do not contribute to the completion of the life cycle. Instead, measures of host specificity should take into consideration interactions between a parasite and a potential host species as well as interactions between current and subsequent hosts in the life cycle. The objectives of this study were to track the development of 2 trematode species, Halipegus eccentricus and Halipegus occidualis , in 3 phylogenetically and ecologically distinct microcrustacean second intermediate hosts, and then evaluate the extent to which each of these hosts contributed to transmission of each Halipegus species to the next odonate host in the life cycle. All 3 microcrustacean species exposed became infected with both species of Halipegus. The patterns of growth of H. eccentricus and H. occidualis were similar, but there were consistent differences in the rates of growth among the microcrustacean species in both Halipegus species. Regardless of host species infected, all individuals of both species were considered to be developmentally infective to the next host in the life cycle by 19 days postexposure (DPE) when they lost their excretory bladder. Worms of varying sizes were capable of surviving without this structure, suggesting that there is not a strong relationship between the rate of growth of the metacercariae and the development of their osmoregulatory system. Although Halipegus species were capable of living without an excretory bladder at 19 DPE, there were differences in their size and rates at which the 3 microcrustaceans contributed to transmission of the parasites to subsequent odonate hosts. Collectively, under controlled laboratory conditions, there was an approximate 2-fold difference in the average percentage of worms that established in odonates from the ostracod, Cypridopsis sp., than from the harpacticoid copepod, Phyllognathopus sp., and the difference was nearly 3-fold between Cypridopsis sp. and the cyclopoid copepod, Thermocyclops sp. Therefore, despite all 3 microcrustacean species becoming infected, not all species were equally suited for transmission and completion of the life cycle. Differences among the 3 microcrustacean species in cercaria ingestion, metacercarial growth and development, and odonate predation rates on infected microcrustacean species were important factors in determining transmission of the 2 Halipegus species to odonate hosts.
Helminths often demonstrate preferential site selection in which a parasite will only occur in 1 microhabitat or a restricted portion of its fundamental niche within its host. However, factors responsible for helminth site specificity are poorly understood, and very little is known about how these factors vary among multiple host species. Some helminths, such as Halipegus occidualis, have been reported from different habitats (stomach or under the tongue) within multiple anuran host species, suggesting that the site selected varies within anuran species. This study examined the site selection by H. occidualis in 7 definitive anuran host species using experimental infections. Then, the site fidelity of H. occidualis was further tested by transplanting worms from under the tongue to the stomach and vice versa in different anuran host combinations, and the movement of worms was recorded. Halipegus occidualis individuals occupied the habitat under the tongue in 6 of 7 anuran species. However, worms always occupied the stomach of American bullfrogs (Lithobates catesbeianus) and were never found under the tongue or in the mouth of these hosts. More importantly, all worms remained in the original habitat when transplanted from the stomach to the stomach or the buccal cavity to the buccal cavity within another individual of the same amphibian species. However, when worms were transplanted from the stomach to the buccal cavity or vice versa in the same host species, the worms always migrated back to the original habitat. The main contribution of this study is that it experimentally documented the variability in the site fidelity of H. occidualis within multiple definitive host species and determined that site fidelity is not as strongly conserved in this genus as suggested previously. Additionally, this work suggests that the variation in site selection in different host species could lead to speciation of the parasites.
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