Manipulative Parasites’ role in Community Composition and Habitat Change: a Closer look at Nematomorpha’s Impact, both Direct and Indirect

by Christopher Paquette
BIOL 490, Fall 2014

Key taxa: Nematomorpha, Gordioida

Parasite-induced behavior manipulation is widespread throughout the world and, until the last decade, has been poorly understood. These parasites come from a vast range of taxa, and are characterized by their ability to cause behavioral changes in a host which benefits the continuation of the parasite life cycle. Parasite manipulation can alter competition, increase biodiversity and change entire communities. It is pivotal for the fields of ecology and evolutionary biology and will be examined in this essay using horsehair worms from the phylum Nematomorpha as a study subject. The clear evidence of behavioral manipulation, seen in histological and morphological analysis, is very important in understanding the impacts of behavior modifying parasites in almost all biomes of our planet.

The case of Bitillaria cumingi, the Asian mud snail, is a textbook example of how specific changes in behavior can lead to changes in competition throughout food webs. Different populations of the mud snail separate themselves based on the presence or absence of the trematode, Cercaria batillariae (Lefevre et al., 2008). Populations infected with C. batillariae are induced to spend more time in the lower tidal zones where they are susceptible to predation. This change, coupled with induced gigantism, causes increased numbers of snails to be eaten by predatory fish, a necessary event for the parasite to complete its life cycle. This modification leads to two distinct populations of B. cumingi living at different depths, minimizing competition and increasing available resources to higher trophic levels (Lefevre et al., 2008). In doing so, intraspecific competition between the mud snails is reduced due to the spacial separation of the two populations. Competition for predatory fish is also reduced in the presence of C. batillariae because of increased accessibility to prey.

Parasitism not only effects intraspecies dynamics, but can also have a great influence on community diversity. Two populations of crustaceans, Gammarus insensibilis and Gammarus aequicauda are able to coexist in certain conditions based on the presence of the trematode, Microphallus papillorobustus (Lefevre et al., 2008). In the absence of M. papillorobustus, G. insensibilis would normally overcome G. aequicauda populations due to a higher success in reproduction. This reproductive advantage is negated in trematode infections due to the ease of behavioral modification in G. insensibilis, causing population loss from predation. Both species of crustacean can serve as the intermediate host, but as only one is easily modified, the presence of M. papillorobustus allows for greater biodiversity due to the sympatric existence of both species where only one would normally exist (Lefevre et al., 2008).

Perhaps the greatest impacts of manipulating parasites can be seen in intertidal soft bottom communities of New Zealand. In these intertidal communities, two species of echinostomes (trematode parasites) are known to use cockles, a common bivalve, as an intermediate host. These parasites rely on behavior modification to increase the trophic transmission of the cockles to the definitive host, a shorebird. The effectiveness of this tactic is profound, as the trematode causes extensive damage to the foot region of the cockle, rendering it incapable of burying itself for protection or relocating to safe areas. A study done by Mouritsen and Poulin (2005) observed the effects on community dynamics when parasite density was increased, as well as the effects of increased sessile cockles on top of the seabed rather than buried underneath it. The result of increasing the parasite density was a significant reduction in the disturbance of the upper sediment, causing large invertebrate populations to increase by more than 30%, including the emergence of some rare species. The experiment observing the presence of cockles at the surface showed very similar results, with a great increase in benthic animals. There was also a staggering increase in species richness and diversity with surfaced cockles, representing an increase in new niches and specialties. This study is unique, as it doesn’t focus the change in the host population, but instead shows the reformatting of the entire ecosystem by a change in the host behavior (Mouritsen and Poulin, 2005). The cockle is by no means a keystone species in the soft bottomed tidal zone, and the fact that a change in its behavior can drastically change its community shows the indirect impact that these behavior manipulating parasites have on their surroundings.

The relationship between nematomorphs and their hosts is a widely accepted case of parasite manipulation, and serves as a well-studied example of how behavioral modification can affect the community in which the host lives. Nematomorphs can be found in almost every part of the world and, as indicated by a study done on nematomporph-mantid relationships, are quite abundant and common in the entire range of their hosts (Schmidt-Rhaesa and Ehrmann, 2001). The life cycle of gordiid worms (Nematomorpha) has been quite clouded until the last decade. The unique aspect of gordiid worms is their alternation between a free-living adult stage and a parasitic larval stage (protelean life cycle), as well as being an obligate parasitoid (kills the host upon emergence) (Schmidt-Rhaesa and Ehrmann, 2001). The larval stage develops in the body cavity of a coleopteran or orthopteran host, feeding on the reproductive organs and stored fat bodies (Hanelt and Janovy, 1999). Juveniles have been known to emerge from the host in a dramatic fashion where they complete their life in freshwater or marine environments. This behavior indicates that there is some maladaptive change going on in the host which may or may not be caused by the parasite. Based on the extensive distribution of nematomorphs, any possible behavioral change has the ability to affect ecosystems worldwide.

The natural history of horsehair worms reveals their potential to impact the communities in which they live, but it is also important to determine the legitimacy of their behavioral manipulation. For decades, anecdotal accounts have described the behavioral change in coleopteran and orthopteran hosts to seek out water and make a suicidal leap into the abyss, followed shortly by the emergence of a slender gordiian worm in its new freshwater home. In the past care has been taken not to assume that this behavioral change is caused by the parasite because, although many parasites manipulate their host’s behavior to complete their life cycle, many changes are only coincidental and are not beneficial to the parasite. A study performed at a small rural pool in southern France was designed to show that this behavioral change in crickets was not just a coincidence, but was only present in infections of the parasite and was linked with the emergence of the gordiian worm (Thomas et al., 2002). Infected insects repeatedly jumped into the water, followed shortly by an emergence of the adult worm. Field and lab studies resulted in the same conclusion: that the behavioral change is only present in infected hosts and that it is perfectly timed to complete the parasite’s life cycle. Though there was no evidence to suggest that the host actually seeks out water from long distances, the behavioral manipulation which causes the host to enter the water is not normal for uninfected hosts and is necessary for the emergence of the adult parasite. These changes are not just pathological consequences of infection, but are required for the parasite due to the inability to survive as adults on land, and result in increased fitness for mating pairs of nematomorphs (Thomas et al., 2002). Nematomorphs are one of the few groups of parasites to be undoubtedly classified as behavioral manipulators because the direct physiological changes in the host have been revealed. Histological changes in the brain as well as biochemical changes have shown that insects infected with gordiian worms show a reduction in many amino acids, resulting in lower brain function, which could interfere with memory and behavioral inhibition. In essence, the biochemical changes as well as the disruption in the CNS would cause insects to spend more time near water and dilute the fear of drowning that a normally behaving insect may experience (Thomas et al., 2003).

The broad host specificity and wide range of the phylum Nematomorpha sets the stage for a great influence on the communities in which they exist. The presence of Nematomorpha may serve as a control agent for insects by reducing nematomorph-favored populations, or it may indirectly result in increased fish abundance in local streams due to increased accessibility to insect prey jumping in the water. Since the parasite kills its host 100% of the time, slowly eating away at the reproductive organs, the host is removed from the genetic pool and can cause huge changes in the genetic variation of the host populations. Further research is necessary to determine if the removal or addition of nematomorph populations would create a change in either native insect or native fish populations in a controlled study area. A study performed by Hanelt and Janovy (1999) using laboratory conditions and manually infected hosts provided strong evidence that although definitive hosts have been infected directly in the lab in a few cases, an intermediate host is almost always required in the environmental conditions which nematomorphs live. This evidence indicates that smaller invertebrates may also be manipulated to spend more time in shallower areas of the water where they may be eaten by coleopterans and orthopterans, the definitive hosts of the horsehair worm. The fact that so much is known about the mechanisms used by nematomorphs as well as the clear evidence that the change in insect host behavior is caused by the invasion of the nematomorph parasite shows the potential for the impact on the whole community and the ecosystem.

The effects of parasite manipulation are greatly understudied and underappreciated by many ecologists, and represent a relatively new view of population dynamics. Parasites are present in nearly every ecosystem and create changes that are not only directly linked to their host, but can significantly impact the makeup of the ecosystem around them. The small amount of research that has been done provides strong support that the composition of certain communities has been greatly influenced by manipulative parasites. This category of parasitic organisms may be found to have a significant influence on the rate of evolution, speciation, and could be one of the greatest factors for the biodiversity which we see today.

References Cited

• Hanelt, B. & J. Janovy. 1999. The life cycle of a horsehair worm, Gordius robustas (Nematomorpha: Gordioidea). The Journal of Parasitology 85(1): 139-141.
• Lefevre, T., C. Lebarbenchon, M. Gauthier-Clerc, D. Misse, R. Poulin, & F. Thomas. 2008. The ecological significance of manipulative parasites. Trends in Ecology and Evolution 24(1): 41-48.
• Mouritsen, K. & R. Poulin. 2005. Parasite boosts biodiversity and changes animal community structure by trait-mediated indirect effects. OIKOS 108: 344-350.
• Schmidt-Rhaesa, A. & R. Ehrmann. 2001. Horsehair worms (Nematomorpha) as parasites of praying mantids with a discussion of their life cycle. Zoologischer Anzeiger 240: 167-179.
• Thomas, F., A. Schmidt-Rhaesa, G. Martin, C. Manu, P. Durand, F. Renaud. 2002. Do hairworms (Nematomorpha) manipulate the water seeking behavior of their terrestrial hosts? Journal of Evolutionary Biology 15: 356-361.
• Thomas, F., P. Ulitsky , R. Augier, N. Dusticier, D. Samuel, C. Strambi, D.G. Biron, M. Cayre. 2003. Biochemical and histological changes in the brain of the cricket Nemobius sylvestris infected by the manipulative parasite Paragordius tricuspidatus (Nematomorpha). International Journal for Parasitology 33: 435-443.