Larval helminths in intermediate hosts: Does competition early in life determine the fitness of adult parasites?

Abstract

Density-dependent effects on parasite fitness have been documented from adult helminths in their definitive hosts. There have, however, been no studies on the cost of sharing an intermediate host with other parasites in terms of reduced adult parasite fecundity. Even if larval parasites suffer a reduction in size, caused by crowding, virtually nothing is known about longer-lasting effects after transmission to the definitive host. This study is the first to use in vitro cultivation with feeding of adult trematodes to investigate how numbers of parasites in the intermediate host affect the size and fecundity of adult parasites. For this purpose, we examined two different infracommunities of parasites in crustacean hosts. Firstly, we used experimental infections of Maritrema novaezealandensis in the amphipod, Paracalliope novizealandiae, to investigate potential density-dependent effects in single-species infections. Secondly, we used the crab, Macrophthalmus hirtipes (Ocypodidae), naturally infected by the trematodes, M. novaezealandensis and Levinseniella sp., the acanthocephalan, Profilicollis spp., and an acuariid nematode. These four helminths all develop and grow in their crustacean host before transmission to their bird definitive host by predation. In experimental infections, we found an intensity-dependent establishment success, with a decrease in the success rate of cercariae developing into infective metacercariae with an increasing dose of cercariae applied to each amphipod. In natural infections, we found that M. novaezealandensis-metacercariae achieved a smaller volume, on average, when infrapopulations of this parasite were large. Small metacercariae produced small in vitro-adult worms, which in turn produced fewer eggs. Crowding effects in the intermediate host thus were expressed at the adult stage in spite of the worms being cultured in a nutrient-rich medium. Furthermore, excystment success and eggproduction in M. novaezealandensis in naturally infected crabs were influenced by the number of co-occurring Profilicollis cystacanths, indicating interspecific interactions between the two species. Our results thus indicate that the infracommunity of larval helminths in their intermediate host is interactive and that any density-dependent effect in the intermediate host may have lasting effects on individual parasite fitness. q

Natal-Host Environmental Effects on Juvenile Size, Transmission Success, and Operational Sex Ratio in the Entomopathogenic NematodeSteinernema carpocapsae

“…Possibly, greater size provides nematodes with a growth advantage in the new host (cf. Fredensborg and Poulin, 2005) that may then facilitate survival. Alternatively, larger nematodes have been shown to have larger bacteria storage vesicles (Flores-Lara et al, 2007) that may allow them to store and release more bacteria and cause a faster disabling of the insect immune system (Richards and Goodrich-Blair, 2009).…”

“…However, of special importance in parasites is how these competitive effects affect the success of parasite transmission to and establishment within new hosts. Indeed, such trans-host effects have been found in parasitic worms, as high density within an intermediate host can reduce parasite size, in turn, affecting parasite survival and fecundity in the definitive host (Steinauer and Nickol, 2003;Fredensborg and Poulin, 2005). Despite these studies, the generality of trans-host effects has not been established, nor fully integrated into our understanding of ecological and evolutionary dynamics of host-parasite interactions (Tseng, 2006;Little et al, 2007).…”

Effects of Season, Size and Parasitism by the Acanthocephalan, Profilicollis altmani, on the Carotenoid Concentration and Composition of the Pacific Mole Crab, Emerita analoga

“…Many host-parasite systems involving aquatic crustaceans have been identified, and a large body of research exists specifically on the effects of larval helminths in these systems. This includes the larvae of nematodes, trematodes and acanthocephalans, all of which have been shown to infect various species of amphipods, isopods, copepods, cirripeds,and decapods (Eickstaedt 1969, Schlechte 1969, Haye and Ojeda 1998, Gaillard et al 2004, Fredensborg and Poulin 2005, Dezfuli et al 2007). …”

The influence of clonal diversity and intensity-dependence on trematode infections in an amphipod

“…Indeed, reductions in metacercariae size with increasing parasite load have been detected in several trematode species (Sandland and Goater, 2000 ;Brown et al 2003 ;Fredensborg and Poulin, 2005). Unlike many trematodes, M. novaezealandensis metacercariae grow and develop substantially during the first few weeks after infection (Poulin and Latham, 2003 ;Fredensborg et al 2004).…”

“…Also, if the degree of exploitation by parasites influences host survival, selection could favour decreased growth with increasing numbers in parasites that require host survival for transmission (Parker et al 2003). Fredensborg and Poulin (2005) found lower individual mean sizes of fully developed M. novaezealandensis metacercariae within heavily-infected crabs ; they suggested this could result from resource limitations during initial growth when multiple parasites infect the host, as the slight size differences would not impact host fitness. Our results support differences occurring during early growth, but we do not rule out the possibility that parasite growth strategy could also influence M. novaezealandensis during this stage as the smaller amphipod hosts may be more sensitive to parasite growth.…”