Host Behavior Manipulation by Parasitic Insects and Insect Parasites

Rustie Robison Department of Bioagricultural Sciences and Pest Management

April 8, 2009 RustieLRobison@gmail.com

Abstract Insects and parasites are ubiquitous. In any environment, there are numerous insects and

parasites. Independent evolutionary selection has occurred and parasites and insects are

taxonomically diverse (Roy et al, 2006). However, many insect-parasite interacts have evolved

between insects and parasites due to the number and habitat overlap of the groups (Roy et al,

2006). In addition, to the separation of the groups there are insects that have evolved to be

parasites. Over the course of evolutionary time these parasite-host interactions have resulted in

numerous modifications of the insect host including morphology, behavior, and physiological by

many methods. The behavior of the insect host is modified, often to the benefit of the parasite.

However, these relationships are not always negative. There are numerous examples of host-

parasite interactions that are mutualistic.

Introduction General Overview of Host-Parasite Relationships

Parasitism is a type of symbiotic relationship between two different organisms. The

relationship is often one-sided and the parasite uses the host for resources. A parasitoid is a type

of parasite that usually has only one host for the completion of the life cycle and the host is

usually killed (Cole et al, 2002). There are many types of relationships in the host-parasite

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interactions. The host-parasite paradigm has and continues to be a puzzle in the hands of

researchers and scientists. The arms race of the host and parasite, including the evolution and

selection, is an enigma. Independent evolutionary selection has occurred on taxa of parasites and

insects resulting in taxonomic diversification (Roy et al, 2006). However, many interacts

between these two groups have evolved, due to the sheer number and habitat overlap (Roy et al,

2006). These interactions may lead to an evolutionary arms race between the parasite and its

insect host (Hoffman et al, 2008; Rolff et al, 2001, Ives, 1995). In addition, these interactions

lead to many questions. How do parasites and their insect hosts interact and communicate?

How do parasites control insect behavior? Even though there are many unanswered questions,

parasites controlling host behavior is a widespread phenomenon. Parasites cause a whole suite

of changes in host behavior, physiology, and morphology (Poulin, 1998). Both parasites and

parasitoids alter the physiology and the behavior of the host (Cole et al, 2002). There are many

reasons for the alteration of host behavior. These reasons range from simple pathology to more

complex selection of the population (Poulin, 1998). Many studies on manipulation of host

behavior by parasites have been conducted. The diversity and abundance of both insects and

microbes, as well as the similarity of habitats, has lead to insect and microbial symbiotic

relationships (Roy et al, 2006). In addition, the abundance and diversity of insects has also lead

to the commonality of insects being parasitized by other insects. Insects are continuously

affected by insect parasites and parasitic insects.

Host behavioral manipulations are commonly caused by both insect parasites and

parasites of insects. Insect parasites include microbial organisms such as fungus and bacteria.

Insect parasites include numerous other organisms such as protozoans, insects, and nematodes, to

name a few. These parasitic insects can be divided into endoparasitic (internal) or exoparasitic

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(external). External parasites include organisms such as ticks, mites, insect larvae such as wasps,

and other organisms. External parasites are not as much as an influence on host behavior

because the hormone and immune system are not in direct interaction with the parasite.

Endoparasitic, internal, parasites are much more influential on behavior of the host due to the

intimate interaction with host immune and endocrine systems (Caldera et al, 2009; Beckage,

1985; Beckage, 1991; Cole et al, 2002; Truman and Riddiford, 2002; Poulin, 1998). In current

research the endocrine system is the major factor in the defense, regulation, and control of

parasites (Libersat et al, 2009). Endoparasitic insects and parasites usually develop in the

hemocoel of the infected insect host (Beckage, 1985; Gross, 1993). The hemocoel of the insect

is where the regulation of hormones occurs (Beckage, 1985). These types of interactions involve

endocrine changes that are mediated by the hemocoel where developmental, behavioral, and

metabolic signals are transported to regulate behavior changes (Beckage, 1985; Cole et al, 2002).

In this paper the endoparasites, those that feed internally, will be the focus. These changes occur

at a genetic level, which affect the organism and potentially the population. How does

parasitism affect selection? Many of these changes involve individual behavior variation due to

manipulations of the nervous system directly, or by indirect changes in the endocrine and

immune systems hormones or metabolism changes. The function of the parasitized insects in

populations, communities or ecosystems will be altered due to changes in foraging, sexual

behavior, behavior, communication, and activity levels (Caldera et al, 2009; Beckage, 1985;

Beckage, 1991; Cole et al, 2002; Truman and Riddiford, 2002; Poulin, 1998). These changes

have large scale consequences on processes of natural selection and evolution.

Not all host-parasite interactions are negative; there are examples of symbiotic

relationships between host and parasite. Certain ant species (Formicidae: Hymenoptera) engage

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in obligatory mutualism with fungi. The research is continuous in this complicated field. The

mechanisms of host manipulation by insect parasites and parasitic insects are being researched

extensively.

Figure 1: The imagReproduced from Li

Parasitic Insects

There are ma

the order Hymenopt

parasitoids. Though

specialists. These sp

developed over time

(a) Camponotus ant with Hirsutella emergence from cuticle

(b) Cricket (Memobius sylvestris) with hairworm (Tellinii spinochordes) emerging

(c)Ampulex compressa stinging a cockroach (Periplaneta americana)

es show general types of fatal interactions between parasites and insect hosts. bersat et al, 2009

ny groups of insects that act as parasites on other insects. Most notably are

era, specifically the wasps. These wasps are highly evolved to be

the wasps are parasitoids of many species, many of the parasitoids are

ecialist wasps have co- evolved with their host and an interaction has

. Wasps are very common as parasites of other insects. In fact,

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Hymenoptera are one of the most diverse groups of parasitic insects (Whitfield, 1998).

Hymenopterans live in nearly all habitats, terrestrial and aquatic and fill ecological niches,

including pollinator, predator, and parasite (Whitfield, 1998). There are many examples of wasp

parasitism of insect hosts. Libersat et al (2009), describes the process of envenomization of a

cock roach (Periplaneta americana) by Ampulex compressa (see figure 1 & 2). This

envenomization affects the walking-related behaviors of the roach (Libersat et al, 2009).

Figure 2: This image represents the current model of the neurophysiological effects induced by envenomization of cockroaches by Ampulex compresa (see figure 1 for image of envenomization of the cockroach) Reproduced from Libersat et al, 2009.

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The wasp parasitoid’s venom is inserted into the cerebral ganglia which controls the

thoracic movements, including walking patterns. Inhibition is the result and the roach is not able

to escape using normal escape patterns (Libersat et al, 2009). If the wasp does not inject the

venom into the correct location the cockroach will be unaffected. Therefore, Libersat et al

(2009) addresses the question of how envenomization can be so selective. The answer is related

to the venom targets that are for specific pathways, specifically for the control of the escape

response. The escape response is related to the success of the wasp offspring and the overall

fitness. The selectiveness of the interaction is important in the survival of the parasitoid

(Libersat et al, 2009; Gross, 1993). Once the cockroach has been injected with venom the wasp

parasitoid can deposit the egg into the host for further development. The egg will hatch and the

larvae will continue to grow within the cockroach until it reaches maturity and kills the roach by

escape, or outgrowing the cockroach host. The processes that occur during the development of

the endoparasite life stages will be discussed later in the paper.

In addition to wasps, numerous other insects are parasites of other insects (see appendix

A). These include many families in the Hymenoptera, Diptera, and Strepsiptera. For example,

Compsilura concinnata (Diptera: Tachinidae) parasitizes a Lymantriidae caterpillar, Lymantria

dispar (Beckage, 1985). These endoparasites are developmentally synchronized with their hosts’

endocrine systems in order to ensure success of the parasite offspring.

Insect Parasites

There are also many groups of insect parasites including bacteria, viruses, fungus,

nematodes, and other insects. Most notably fungal insect relationships have been studied by

numerous researchers. Roy (2006) states that fungi are common parasites of arthropods. There

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are about 700 known species of Entomopathogenic fungi (Roy et al, 2006) (see figure 3). Many

of these parasitic fungus may have an alternative host in order to complete the life cycle, often

the alternative host of the Entomopathogenic fungus is another insect (Roy et al, 2006).

Figure 3: Life cycle of an entomopathogenic fungi, Entomophthora muscae in Delia radicum. (Reproduced from Roy et al, 2006)

Blanford and Thomas (2001) noted that in the desert locust, Schistocerca gregaria it

became infected with a fungus, Metarhizium anisopliae var acridum. Arthurs and Thomas

(2001) also noted that in the field, locusts and grasshoppers were observed to be infected with

Metarhizium anisopliae var. acridum, the same fungal entomopathogen. Arthurs and Thomas

(2001) reported the pathogen increases the susceptibility of the host to predation. To test this

field observation a laboratory experiment was conducted and the results show that infection with

Metarhizium anisopliae var. acridum does cause behavioral changes that effect survivorship of

the locusts (Arthurs and Thomas, 2001). In a related paper, Metarhizium anisopliae var. acridum

was associated with behavioral fever in acridids (Blanford and Thomas, 2001). This change in

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behavior by increasing preferred body temperature is associated with host searching of new

microclimates that are beneficial for the parasite (Arthurs and Thomas, 2001).

Mechanisms of Behavior Modification Induced by Insect Parasites and Parasitic Insects

The effects of the parasite on the insect host behavior can be direct or indirect (Libersat et

al, 2009). Direct manipulation of host behavior is often associated with nervous system

modification. The indirect manipulation of behavior is more often associated with host

endocrine and metabolism (Libersat et al, 2009). The endocrine system in an insect host is

responsible for the production and regulation of hormones. In addition to hormone production

and regulation, the endocrine system maintains growth and development, as well as,

physiological function. Manipulations of host behavior by both insect parasites and parasitic

insects include increases in temperature (behavioral fever), feeding behavior changes

(consumption and location), reproductive behavior changes, and social behavior (Roy et al,

2006; Moore, 1995; Arthurs and Thomas, 2001; Poulin, 1998; Beckage, 1985). The American

cockroach (Periplanta americana) is frequently infected with Monofiliformis moniformis. This

infection by the parasite species causes erratic behavior changes when the cockroach is in high

light situations. The cockroach will move toward the light and will become hyperactive as well

(Moore, 1995).

There also been many phylogenic approaches to try to understand the unique

relationships between insect parasites and parasitic insects and their insect hosts. Poulin (1998)

found that changes in the manipulation of host behavior may be related to phylogeny. This

would make sense from a evolutionary sense if a specific behavior is a host or a parasite adaption

(Poulin, 1998). Many of these behavior traits are thought to have evolved independently, in

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many diverse insect hosts and parasites (Poulin, 1998). Poulin (1998) notes that two distinct taxa

develop similar juvenile and adult life cycles even though they are not related in lineage; these

life cycles are noted to cause very similar behavior manipulation of the host. Parasitism and the

manipulation of host behavior has evolved independently over time (Poulin, 1998).

Behavioral Fever

When the body temperature of an insect host is increased to levels above normal due to

the presence of a parasite this is termed behavioral fever (Roy et al, 2006; Arthurs and Thomas,

2001). This increase in the body temperature outside the normal range is a common response to

a parasite invasion, especially a fungal parasite. The production of heat is energetically costly

and may not be effective in ridding the host of the parasite but it has been shown to delay

mortality of the insect host (Roy et al, 2006). In Musca domestica, a house fly, experiments

were conducted to monitor “fever” of the fly when it was infected with Entomophthora

schizophorae (Roy et al, 2006). The results of the experiments do indicate that higher

temperatures are preferred in the house flies that are infected with the parasite (see figure 4).

Any insect species that can regulate body temperature has the possibility of retaining normal

behavior and inhibiting parasite growth (Roy et al, 2006; Arthurs and Thomas, 2001).

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Figure 4: The images show general types of interactions between parasites and insect hosts. (Reproduced from Libersat et al, 2009

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Feeding Behavior Host feeding behaviors are often manipulated by parasites. The consumption and the

location of the feeding are shown to be affected by the presence of insect parasites and parasitic

insects in the host (Roy et al, 2006). When the dose of the parasite is high, there is a reduction in

feeding this is due to a reduction in digestive abilities by the host (Roy et al, 2006). In addition,

some insects will change feeding locations. This location change may be a dispersal mechanism

for the parasite (Roy et al, 2006). There is very few studies that have tried to address the

question of feeding behavior changes in parasite infected insect hosts.

Reproductive Behavior

A very important behavior in all insects is the reproductive behavior. Reproductive

behavior can be very specific in some insects and more general in others. Regardless of the

specificity the reproductive behavior ensures lifetime fitness and reproductive success. Any

modifications to this system could have enormous consequences for the fitness of an insect.

Resources for reproduction can be diverted to the parasite (Roy et al, 2006); this alternative

allocation can reduce fecundity of the insect host (Roy et al, 2006; Poulin, 1998). Roy et al

(2006) suggest this may be an effect of reduction of juvenile hormone, though experimentation is

needed to prove that statement.

In addition, sex pheromones may be changed. Roy et al (2006) note that female moths

that were infected with Z. radicans significantly reduced sex pheromone production. The

reproductive behavior and the pheromone behavior may be altered when an insect is parasitized.

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Social Behavior

Many aspects of social behavior may be affected by insect parasites and parasitic insects.

Ants are a complex social group. The introduction of a parasite could be detrimental to the entire

colony. A whole suite of behaviors are noted in social and eusocial insects including increased

grooming, cleaning, antibiotic production, removal of infected individuals. Avoidance is another

behavior to ensure against parasites, individuals can avoid parasites and the colony can be moved

to avoid pandemic parasitic infection (Roy et al, 2006). It is common in many eusocial colonies

to remove the dead. In red fire ants, the individuals that are infected with B. bassiana are buried

(Roy et al, 2006). The density of the colony makes it highly susceptible to parasite invasions.

The constant grooming and tidiness of the colony will reduce the chances of parasite infection.

The behavior of the colony is dictated by the altruistic behavior of the individuals. If these

behaviors are manipulated by insect parasites or parasitic insects then the whole colony would be

in jeopardy. More research is needed to understand the interactions of eusocial insect-parasite

dynamic and to detect possible evolutionary consequences of parasite infection.

Defensive Reactions Taken by the Parasitized Host

There are numerous strategies that are utilized to defend against parasites. Many of these

strategies involve the same behavioral changes that are induced by the parasite itself (Roy et al,

2006). In addition, these defensive strategies can be broad spectrum or a very specific response

much like the response seen in plants to pathogens.

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Insect Symbioses

Not all insect-parasite interactions are detrimental to the host and have a negative

connotation. There are numerous examples of symbioses between an insect host and a parasite.

Many insects, such as termites and cockroaches utilize microbes for digestion of food (Caldera et

al, 2009). Other insects utilize microbes for aiding in the growing of food. These fungus-

growing ants (Formicidae), the leaf-cutters, use manure to grow fungus. The fungus is then

applied to the hyphal tips which allow enlarged food structures much like our own agricultural

practices of fertilizer addition (Caldera et al, 2009).

Evolutionary Consequences

Though many questions remain numerous studies are being conducted to answer the

complicated questions about insect-parasite dynamics. The questions are big in scale and relate

to the future of both the parasite and the insect host. Where will the co-evolutionary arms race

take the involved individuals? How does this shape reproduction of the insect and the parasite?

What other long term consequences?

Conclusions

Many of the behavioral changes associated with insect parasites and parasitic insects may

be determined by changes in the endocrine system, directly or indirectly (Beckage, 1991; Roy et

al, 2006; Gross, 1993). There are many areas of research that are focusing on the interaction

between insect hosts and parasites. The field of Insect Parasitology is broad and many questions

still remain in the enigma of the host-parasite interaction. Independent evolutionary selection

has occurred and parasites and insects are taxonomically diverse (Roy et al, 2006). However,

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many interacts have evolved between insects and parasites due to the number and habitat overlap

of the groups (Roy et al, 2006). In addition, to the separation of the groups there are insects that

have evolved to be parasites. Over the course of evolutionary time these parasite-host

interactions have resulted in numerous modifications of the insect host including morphology,

behavior, and physiological by many methods. The behavior of the insect host is modified, often

for the benefit of the parasite. However, these relationships are not always negative. There are

numerous examples of host-parasite interactions that are mutualistic. Many of these interactions,

as previously mentioned, involve eusocial ants which are at a higher risk for parasite infection

and would have larger number of fitness and evolutionary consequences. In turn, the ants have

evolved to utilize the “potential” fatal pathogen and to direct aspects of the fungus to food

production.

Insects and parasites are ubiquitous. The numbers and the diversity of insects and their

remarkable adaptation to all terrestrial and freshwater niches have allowed for enormous

diversification. Along with this great diversification, come many questions that will need to be

addressed in future research and experimentation of both insect parasite and parasitic insects and

their interactions with the insect hosts.

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References

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THEME. Experimental Parasitology 72, 332-338. Beckage NE. (1993). ENDOCRINE AND NEUROENDOCRINE HOST-PARASITE

RELATIONSHIPS. pp 233-245. Blanford S, Thomas MB. (2001). Adult Survival, Maturation, and Reproduction of the Desert

Locust Schistocerca gregaria Infected with the Fungus Metarhizium anisopliae var acridum. Journal of Invertebrate Pathology 78, 1-8.

Caldera EJ, Poulsen M, Suen G, Currie CR. (2009). Insect Symbioses: A Case Study of Past,

Present, and Future Fungus-growing Ant Research. Environmental Entomology 38, 78-92.

Cole TJ, Beckage NE, Tan FF, Srinivasan A, Ramaswamy SB. (2002). Parasitoid-host endocrine

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Gross P. (1993). INSECT BEHAVIORAL AND MORPHOLOGICAL DEFENSES AGAINST

PARASITOIDS. Annual Review of Entomology 38, 251-273. Hoffman EA, Kovacs JL, Goodisman MAD. (2008). Genetic Structure and breeding system in

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Insect Parasites. Annual Review of Entomology 54, 189-207. Moore J. (1995). The Behavior of Parasitized Animals. BioScience 45, 89-96. Moore J, ed. (2002). Parasites and the Behavior of Animals. Oxford: Oxford University Press. Poulin R. (1998). Evolution and phylogeny of behavior manipulation of insect hosts by

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Rolff J, Vogel C, Poethke HJ. (2001). Co-evolution between ectoparasites and their insect hosts: a simulation study of a damselfly-water mite interaction. Ecological Entomology 26, 638-645.

Roy HE, Steinkraus DC, Eilenberg J, Hajek AE, Pell JK. (2006). BIZARRE INTERACTIONS

AND ENDGAMES: Entomopathogenic Fungi and Their Arthropod Hosts. Annual Review of Entomology 51, 331-357.

Truman JW, Riddiford LM. (2002). ENDOCRINE INSIGHTS INTO THE EVOLUTION OF

METAMORPHOSIS IN INSECTS. Annual Review of Entomology 47, 467-500. Whitfield JB. (1998). PHYLOGENY AND EVOLUTION OF HOST-PARASITOID INTERACTIONS IN HYMENOPTERA. Annual Review of Entomology 43, 129-151.

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Appendixes

Appendix A

Developmental synchrony between endoparasites and their hosts (Reproduced from

Beckage, 1985)

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Appendix B

Summary of Endocrine Effects of

endoparasitism on insect hosts

(reproduced from Beckage, 1985)

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