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Modification of the intermediate hosts Caecidotea intermedius and Asellus intermedius by Acanthocephalus dirus: A Review

Lorraine Salterelli

11/22/2015

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Abstract

Parasite is a term used to describe the dependence of one organism on another

physiologically. It encompasses species of protozoans, worms, and arthropods, among others,

and no species is immune to parasitic infection. They’ve adapted ways to overcome any type of

obstacle, and have evolved to take advantage of various aspects of a host’s body in order to

achieve its ultimate goal: maturation and reproduction. Some have become able to alter an

intermediate host’s appearance or behavior, resulting in the host’s death through predation by a

definitive host. One such species, Anthocephalus dirus, is able to induce changes in both

appearance and behavior of an isopod, its intermediate host, resulting in heightened vulnerability

to its definitive host, typically fish or birds. Many studies show evidence of altered pigmentation,

body morphology, and behavior of two isopod intermediate hosts in particular, Caecidotea

intermedius and Asellus intermedius. Behavior modifications include anti-predation and

reproductive behaviors. This goal of this review is to sum the research performed on A. dirus and

the effects it has on its intermediate hosts, focusing on the more recent research performed.

Much research appears to have been performed in the past, however, still holds true as evidenced

by recent research.

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Introduction

The life cycle of a parasite is full of continuous, variable challenges every step it takes

from hatching to adulthood. We aren’t talking about kids who are 25 and still live with their

parents; we are talking about the small organisms that are physiologically dependent upon

another different organism (the host) for at least part of its life cycle. These parasites live on or

within the organism and result in harm to the host, though usually do not directly cause the host

to die. During their life cycle, they are faced with challenges of the environment, including both

biotic and abiotic factors. Some are released into the environment as a hatchling and have only

hours to find a suitable host, while others are helpless in egg form as they must be ingested

before they can hatch. Within the host, they face challenges of host immunity. If they survive,

some may make this host their permanent home, while this is only what is referred to as the

intermediate host for others. For the latter, the parasite must make their way through this host as

the parasite develops to find a final host, called the definitive host, where it will grow to full

maturity. In the intermediate host, the juvenile parasite may exit the host, once again facing the

challenges of the outside environment as it searches frantically for its final host to pass by.

Alternatively, it must wait for the intermediate host to be eaten by its definitive host for

transmission to occur. This general life cycle of a parasite, described by Roberts et al. (2012),

still has other variations that include other host types.

The parasite then has evolved ways to overcome these challenges and make it to their

definitive host, where they become mature adults able to begin sexual reproduction and continue

the cycle. Some have special attachments in different stages that allow them to penetrate the

host, attach the host, evade or even take advantage of host defenses, among others. One

interesting evolution of parasites has even made it possible for them to alter behavior or

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appearance of their intermediate host in such a way that they are more likely to be eaten by the

definitive host and successfully transmit the parasite to its final location. This may have become

most aware to the public by the article from Cracked, which relates the ability of Toxoplasmosa

gondii to control host behavior to a potential zombie apocalypse (Sloth and Wong 2007).

It turns out, T. gondii is not the only parasite with the ability to alter its intermediate

host’s susceptibility to predation. Various studies have shown that multiple species found within

the phylum Acanthocephala, whose life cycle consists of an arthropod intermediate and

vertebrate definitive host (Baldauf et al. 2007), have shown the ability to alter the intermediate

host in different ways to make it more susceptible to predators. According to the Field Manual of

Wildlife Diseases, Acanthocephalans are parasitic worms commonly referred to as “thorny-

headed worms” due to their characteristic retractable proboscis with sharp, recurved hooks or

spines. These species absorb nutrients directly from their host as they lack a digestive system,

and require an intermediate host. Fish, snakes, and frogs are common paratenic hosts, or hosts

that act to transport parasites from intermediate hosts to their definitive hosts. Within paratenic

hosts, development is halted until it reaches the definitive host. Figure 1 below shows the

general life cycle of acanthocephalan worms with avian definitive hosts. Birds are not the only

definitive host of acanthocephalans; some species are also able to infect higher vertebrates,

including humans. Species that infect humans include Maccracanthorhynchus hirudinaceous and

Moniliformis moniliformis as well as some Bolbosoma species (Acanthocephaliasis 2013).

Figure 2 below shows the life cycle of these parasites, further describing larval development

from acanthor to acanthella, to cystacanth.

Acanthocephalas dirus, the subject of this review and a member of the phylum

Acanthocephala, also has been shown to alter the intermediate host’s antipredator behavior,

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Figure 1. Life Cycle Variations with Avian Definitive hosts shows various stages and hosts of an

Acanthocephalan parasite. Arrows indicate the next host or stage of development. Adapted from the Field Manual of

Wildlife Diseases: General Field Procedures and Diseases of Birds.

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Figure 2. Life Cycle of Acanthocephalans with Human host shows the life cycle of species that are able

to infect humans as accidental hosts, including Maccracanthorhynchus hirudinaceous and Moniliformis

moniliformis as well as some Bolbosoma species. The figure is slightly more descriptive, indicating when the

parasite is infective and when it is possible to be diagnosed. Adapted from the Center for Disease Control Website:

Acanthocephaliasis

reproductive behavior, and morphological appearance in studies that will be described

here. Shed in the feces of its definitive host, the acanthor (larval form of A. dirus) is ingested by

the intermediate host, an isopod such as Caecidotea intermedius. Once ingested the acanthor

hatches and develops into acanthella, and then into a cystacanth. The parasite is not infective

until it reaches the cystacanth stage. The ispod must be ingested by the definitive host for the

parasite to continue to develop to maturity; this occurs in the intestines of a fish (Sparkes et al.

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2006). A. dirus has been shown to cause many side-effects or alterations to the intermediate host,

C. intermedius. The studies showing these alterations will be the focus of this review.

Antipredator Behavior

There are a variety of ways in which a parasite can alter a hosts behavior in order to make

it more obvious to predators; including altering times they are active, places they inhabit or feed,

or increasing movement or altering movement to be more erratic are some examples.

Researchers Camp and Huiizinga (1979) tested the susceptibility of infected and uninfected A.

intermedius to predation by placing 10 isopods from each group with a starved creek chub for

three hours. After 3 hours, the creek chubs were euthanized and examined for their gut contents.

Remaining isopods were counted to determine how many of each group had been eaten. This

was performed 10 times each for using light and dark substrates. Infected isopods were observed

to be more active and exhibited greater movement; whereas uninfected isopods were not as

active and would burrow into the substrate. They found that the substrate did not have an effect

on the number of isopods eaten, however there was significantly more infected isopods eaten

independent of the substrate type.

Some behaviors may not be directly caused by the parasite, but instead may be a side-

effect of infection. For instance, a parasite that causes diarrhea in a host means the host may

become dehydrated, causing them to increase their fluid intake. This behavior was not induced

specifically by the parasite, and may or may not benefit the parasite. Some researchers have

questioned whether the behavioral changes induced by A. dirus are adapted, such that the

parasite directly causes this behavioral change in order to increase transmission and fulfill its life

cycle, or whether they are mere by-products of an increased energy requirements.

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Hechtel et al. (1993) performed research in order to shed light on the subject and reach a

conclusion. The goal or their study was to observe whether infection by A. dirus did in fact alter

antipredator behaviors of C. intermedius. They tested whether the isopod was able to react to

different risks of predation, whether this changed when inoculated with the parasite, and whether

these were simply the result of increased foraging due to higher energy requirements or if they

are specific adaptations resulting in greater vulnerability to predation.

They found a significant different in the avoidance behaviors between infected and

uninfected C. intermedius. When uninfected hosts were given the choice between one side of a

setting with no fish opposite the side with predators, hosts favored the side opposite the fish.

When fish were placed on both sides of the tank and hosts were placed between predators,

distribution appeared uniform between both sides. The number of infected hosts that favored the

“safe” side was significantly reduced. Furthermore, they were not uniform in dispersion between

the sides and actually favored the side with predators. Similar to uninfected fish, when predators

were placed on both sides, infected hosts were uniformly distributed between the sides. For both

groups there was a significant difference observed between tests where a safe side was given and

when fish were placed on both sides.

Similarly, Hechtel et al. (1993) observed that uninfected C. intermedius varied

significantly in their hiding behaviors between zero and two-fish treatments. That is to say, the

number of hosts hiding when zero fish were present were significantly different from the number

of hosts hiding when 1 fish was present as well as when 2 fish were present. This difference in

hiding between number of fish present was not observed for isopods when infected with A. dirus.

They refuted the hypothesis that this was simply the result of increased energy demands as the

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higher rate of uninfected hosts in hiding implied that infected hosts are less likely than

uninfected hosts to be in a food source.

Morphological Effects

Effects of parasites on the body size and morphology of individuals has been observed

previously in some parasite-host models. Oetigner (1987) set out to determine the relationship

between morphology of an isopod host infected with Acanthocephalus dirus. 201 ispods of the

genus species Caecidotea intermedius were obtained from the banks of a creek in Illinois. After

two weeks of behavioral observations, they were physically examined to determine the sex, total

length of the isopod, and dissected to separate various body segments. The lengths of propodus

and dactylus pereiopods, both right and left, as well as width were also measured. The isopod

sample contained 55 members that were infected with A. dirus, of which 23 and 46 female and

male isopods, respectively, were infected with one parasite. The remaining infected sample

exhibited a greater A. dirus population. This appears as though males are more likely to be

infected, however when compared with the twenty female and seventy male population that was

uninfected it seems more likely that this is simply due to a greater proportion of males which

constitute the sample size, representative of sampling error.

Where morphometrics are concerned, infected female isopods were observed to be

significantly longer (total length) than those uninfected. The opposite was true for males. As an

interesting note, Sparkes et al (2006) found a greater body size in infected males compared to

uninfected males, however, this was only when the parasite was in the non-infective stages.

Male parasites tended to have a greater coefficient of variation pertaining to their influence on

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total length of isopods, whereas female parasites were observed to have a smaller coefficient of

variation among its hosts.

The pattern describing total length of isopods in males versus females was also observed

in propodus length of first pereiopods and dactylus lengths. The opposite is true when looking at

hosts infected with female parasites and uninfected male isopods compared with uninfected

female isopods and male hosts, specifically with male parasites. A Linear relationship was

observed between propodus and dactylus length with total body length for isopods of both sexes,

and it appeared that A. dirus did not affect this relationship.

It has been shown previously that A. dirus causes lightening of the pigments of some

isopods, including Asellus Intermedius (Camp and Huiizinga 1979). In the previous study by

Camp and Huiizinga (1979), they believe that in addition to the hyperactive behavior observed in

infected hosts, the lighter pigmentation reduced their ability to hide from predators. In previous

research, Oetinger and Nickol (1982) observed that altered pigmentation is also associated with

the male reproductive system, but not the isopod eyes. Furthermore, the level of alteration is

independent of infection intensity, sex, or size of the parasites infecting the isopod. In their

current study, they describe the nature and quantity of the integumental pigments of the isopod

A. intermedius, comparing both uninfected and infected isopods with A. dirus. In their

experiment, they saw that there was lower intensity in the extracts of infected isopods compared

with uninfected isopods. Three of the four extracts were believed to be ommochromes. The

remaining extract was methanol soluble. The methanol-soluble extract had greatest resistance to

alteration by the parasite, whereas the pigment of ommatins was reduced by 25%. Ommins were

affected the greatest. The effect of the parasite was described as “pigmentation dystrophy,” as

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depigmentation and nonpigmentation could not have occurred. A possible mechanism for this

may be due by competition for amino acids between A. intermedius and A. dirus.

Reproductive Effects

Infection by parasites commonly results in decreased mating success due to pathological

consequences. Manipulative parasites such as A. dirus can create even greater complexity in

mating dynamics, as the effects are not pathological but part of the parasites adaptive strategy to

increase its likelihood of being transported to its definitive host (Sparkes et al. 2006). That is to

say, parasites may manipulate their intermediate host’s mating behavior in such a way that

causes them to be more obvious to predators.

In the previous study by Oetigner (1987), the reproductive health of C. intermedius

infected with A. dirus was also observed. As far as reproduction is concerned, uninfected male

and female isopods exhibited more frequent clasping behavior; this behavior was not observed in

infected individuals. Furthermore, only one infected female was observed to have a fully-formed

marsupium, albeit empty. Uninfected females exhibited either offspring in the marsupium or

enlarged ovaries, neither were observed in infected females. No differences were observed in the

reproductive development of male isopods

Recall that where morphometrics are concerned, infected female isopods were observed

to be significantly longer than those uninfected; while opposite was true for males. This was

hypothesized to be due to a decrease in growth that contributes to ovarian and egg development.

Instead, growth was shifted to the body, allowing greater body development and thus resulting in

the larger body size observed in females. Male reproductive growth was not obstructed, however,

and instead somatic growth was affected by the parasite. This hypothesis was tested by

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regressional analyses of parasite size and isopod size. A significant relationship was observed

only in male isopods harboring female parasites. They concluded that A. dirus caused parasitic

castration in C. intermedius. Parasitic castration is defined by Wulker (1964) as “destruction or

alteration of gonad tissue, reproduction behavior, hormonal imbalance, or other modification that

results in a reduction of host reproductive effort above and beyond that which results from

nonselective use of host energy reserves by the parasite”.

Recall that the lifecycle of A. dirus was such that all three juvenile worm stages were

found within the intermediate host, but it is the final stage, the cystacanth, that is infective to the

definitive host. It is no surprise then that some studies have shown mating behavioral

modifications do not appear until the infective stage of the parasite is reached. Sparkes et al.

(2006) set out to determine whether development of A. dirus was correlated with a decrease in

pairing success of male C. intermedius, and attempted to identify the mechanism through which

these parasites induce these effects. They found that only male isopods exhibited a lower pairing

success when harboring the infective cystacanth. They observed that these males did not induce

mating contests with females as often as males infected with acanthor or acanthella stages of A.

dirus, which is a necessary step in pair formation. Females may choose to cooperate, which may

then have been a possible cause for male pairing success. The choice of females to cooperate in

the mating contest was ruled out as a mechanism for decreased mating success, as males did not

initiate the mating contest and give females a choice to be cooperative. The mechanistic effects

of the parasitic are believed to induced changes in the efforts of males to respond to a females

presence. They also determined that this was not likely due to male-male competition in mating

or body size.

Conclusion

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In conclusion, it is obvious to see that the Acanthocephalus dirus is a powerful

manipulative parasite that controls the mind and body of its intermediate hosts. Though not much

of the research regarding A. dirus has been performed recently, some recent research still shows

the ability of the parasite to affect its host in a similar fashion. The parasite is able to reduce the

pigmentation of both Caecidotea intermedius and Asellus intermedius, and is at least shown to

alter the antipredator and reproductive behavior as well as the body morphology of C.

intermedius.

This parasite can be a way to maintain isopod populations. Neither sex is more

susceptible to infection, though size of the isopod can play a role in the risks of parasitism by A.

dirus ( Seidenberg 1973). According to Seidenberg (1973), infection begins in the summer and

by March, 60% of an isopod population has become infected. Isopods with a high infection

intensity disappear from the population, most likely by predation due to the parasites effects.

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with an acanthocephalan manipulates an amphipod’s reaction to a fish predator’s odours.

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