Introduction -
An organism that lives on or in another animal and use them for food, shelter and transportation are known as parasites. The larger animals that are being used for food, shelter and transportation are known as the host. Parasites are unable to live independently, they need a host to survive and fulfil their life cycle. There are many different types of parasites throughout the animal kingdom which lives on or in many different hosts, yet all parasites have one thing in common, it is to increase their chance of survival and complete their life cycle by reproducing.
When a parasite infests within another species this term is known as parasitism, this is when only one of the species receives any benefits and the other results in their fitness being reduced. Parasitism results in noticeable symptoms to the host's fitness and ultimately reducing the life time reproductive success. Parasites do not always kill their host they use small amounts of its nutrients over time which causes little or no pathological affects yet there are few parasites that causes that much illness to their host it results in host death. In some cases the best interest for the parasite is to keep their host alive as it relies on body functions such as blood circulation or the digestive system to live. By allowing the host to survive, the host can respond to the parasites selective pressures by minimising the negative fitness effects (Buckling & Hodgson 2007).
Parasites are able to reduce their host's fitness in a number of ways which will ultimately increase the parasites chances of survival. Many use their mechanisms to reduce host fecundity and survival, parasites are able to interfere with the host's fitness components such as body size, sex allocation, predator escape tactics, castration or even induce body growth (Ecology 2005). There are also parasites that may cause their hosts to become infertile, if this happens before they have had a chance to reproduce then in the terms of Darwinian Fitness, this is the equivalent to killing them. Almost all animals reproduce to pass on their genes, yet if they do not reproduce they help their brothers, sisters or parents to.
Over time and evolution, parasites have gained the ability and developed mechanisms and methods to enable them to alter their host's behaviour physiology, development and life history which will all then help the parasite increase their chances of survival. Though there are a number of parasites that do not manipulate their hosts there are also manipulations that are not beneficial to the parasite, but the majority of manipulations caused by the parasite has a great result in benefiting the parasites chance of survival. (Combes, 1991)
Many parasites may need to use a mode of transmission from one host to another to enable them to complete their life cycle. This can be through a number of transmissions such as vertically, horizontally, via water or vectors, or even through respiratory transmission. Vertical transmission is used when the parasite transmits from the parent host to the offspring (Poulin et al 2000). Here the parasite does not cause too much harm to the parent host as it needs it to live long enough to reproduce so the parasite can transmit to the offspring. Horizontal transmission is between unrelated individuals such as the malaria causing Plasmodiumthe mosquito and the human. (Buckling & Hodgson 2007) Transmission through vector is again the case of malaria - the mosquito being the vector. And finally transmission through respiratory is the case of the common cold virus.
Parasites have evolved into manipulative organisms to ensure their hosts are suitable for the parasite to begin their life cycle within them. The parasite not only uses the host as a source of food but also a source of transport or transmission. Parasites may sometimes need their host to be consumed by a definitive host for the parasite to fulfil its life cycle and possibly reproduce. (Their host are therefore the intermediate host and the definitive host being a predator of the intermediate host). Being able to manipulate the intermediate host would therefore result in the definitive host to consume the intermediate host and the parasite fulfilling its lifecycle.
Parasites tend to be host taxon specific. This is where parasites only parasitise a specific species, family, order or genus. Parasites are able to determine the specificity of their host by two ways: Encounter and Compatibility. Encounter is whether the parasite has to come into contact with the host, whether on a geographical scale - at the habitat or due to the hosts feeding habits (Kaltz et al 1999). Compatibility is whether the parasite was successful in reproducing within the host. Parasites also tend to be site specific, this is where they settle in a specific part of the body, organ or cell. By parasites choosing the taxon and site of which provides the highest levels of fitness, the parasite has more chances of surviving.
Parasites try many ways in which to interact or infect their host but most host animals have defence behavioural systems in place which will protect them from parasites. Some parasites such as flies may try biting their host, when this happens to animals such as deer's, the deer moves to higher ground to get out of the same temperature area, horses may move to shaded areas and hippopotamus tend to enter water. Birds are known for making new nests, this is to avoid any parasites which remain in the old nest from the infective stage. Some animal's behaviour is defensive and may cause the animals to flee from the parasites, animals that have been attacked by a parasite may be able to release alarm pheromones which will then alert closely related individuals to flee from the area. Some species are able to undertake coprophobia, this is to avoid faeces and contaminated locations. Usually cattle and horses are able to do this by avoiding eating in areas where fresh cow pats and droppings are present. Animals also recognise a difference in behaviour of fellow mates especially during mating seasons, courtship behaviour displays in males shows signs of good health, this enables females to choose the male with the highest fitness levels and less chances of being infected by parasites.
There are many different behavioural traits that many different species undertake to prevent the attack of parasites such as adjusting posture, applying an insect repellent, skin twitching, ear wriggling, tail flicking, swatting, slapping, grooming and selective feeding. Some animal's behaviour may alter its physiology which can also protect them from parasites. This could range from altering their diet or self medicating, animals such as domesticated dogs and cats self medicate by eating leaves and grass which is a form of self medication. Ectothermal animals use behavioural fever as a behavioural repertoire to defend themselves from parasites. Cockroaches and grasshoppers that have been infected tend to prefer places of higher temperatures, this will delay the development of the parasites. The opposite to this is behavioural chilling, animals such as bumble bees prefer colder areas when they have been infected by parasites, again at these lower temperatures the development of the parasites is delayed.
Some animals have morphological defences such as camouflage, thicker or a denser pelage or thicker skin. Camouflage, like the pattern in zebra stripes, Tsetse flies are reported to attack zebras less often than any other ungulates as they are more difficult to spot from a distance (Allan S.A. et. Al. 1987). A thicker or denser pelage can make it more difficult for ectoparasites to feed. Thicker skin especially with Hippopotamus makes it very difficult for flies to pierce through the skin to feed.
Many animals are known for having biochemical physiological defences such as skin secretions, release of histamine, eye secretions, vaginal secretions, respiratory tract defences in mammals, gastric juices, diarrhoea, haemoglobin variation and immunity. All these biochemical physiological defences are an animal's way to help protect it from becoming parasitized.
Though the majority of animals have these defences there is a cost to their survival and fitness in having them. There is an energy cost for behavioural avoidance, defensive tactics and physiological responses. Behavioural tactics are expensive in terms of lost feeding and reproductive opportunities, and there is an increased predation risk, increased risk of death from abiotic factors such as behavioural chilling, which all then results in reduction in Darwinian fitness.
Parasite Counter Adaptations against host attack - Both Ectoparasites and Endoparasites have developed mechanisms which will help their chances of survival and reproducing, these include their attachment mechanisms, mimicking non parasitic animals, feeding site preference, fleeing from grooming, anticoagulant saliva, resistant body covering, parasite and host stage that lacks a key defence, anticoagulant action, antigenic variation, sequestration, molecular mimicry, and disruption of host's immune response.
Most host manipulation mechanisms are within the boundaries of damage or disruption to organs, this can include interference to sensory organs, the gonads, the Central Nervous System and the muscles. Changes in the metabolic or nutritional status can be caused from anorexia, interference to the metabolic processes and damage to organs. Interference to the hosts control system such as hormone production and distribution. (de Castro & Bolker 2005b) The out come of these mechanisms which are put to work by the parasite can then affect the behaviour of the host in a three main ways; changes in social behaviour, changes in activity and conspicuous behaviour. (de Castro & Bolker 2005b).
Social behaviour caused by parasites includes altering the behaviour that affects members of the same species. An example of this is the parasitic nematode which infects the Gryllodes sigillatus (decorated cricket). This parasite relies on the host to transmit the infection through sexual transmission. The parasite causes a reduced amount of spermatophylax produced in the male cricket, so when the male mates with the female he transmits the infection to her but also releases a reduced amount of spermatophylax causing the female to copulate with more male in order for her eggs to become fertilised. By the female mating with a number of males this leads to the infection becoming more wide spread. This is a form of parasitic castration and is used by parasites to increase its rate of transmission and reduce the fertility of its host. (Farmer and Barnard 1999).
Host's activities are also able to be changed in order to increase or decrease the parasites transmission rates. An example of this is with the fungus in the genus Cordyceps and the carpenter ant. The fungus invades the body of the ant then at the time of sporulation the mycelia then grows in to the ant's brain altering the perception of the pheromones. This alteration causes the ant to change its activities and climb to the top of the tree or plant and secure itself around the stem or leaf with its mandibles. After a few days the ant then dies allowing the fruiting bodies of the fungus to sprout through the body of the ant. As the ant is at the top of a tree the wind will the spread the spores into the area around the ant which will then infect other hosts. (Mains 1949)
Conspicuous behaviour is when an animal's activity becomes more noticeable and obvious in its environment, this will then make it more vulnerable to being attacked by a predator. In many cases of conspicuous behaviour, the parasite manipulates the behaviour of its intermediate host, this then leads to the chances of predation by the definitive host being increased resulting in the parasite completing its life cycle. An example of this is Toxoplasma gondii, this is a protozoan parasite which infects a rodent by causing an alteration to the dopamine levels in the brain which then in affect causes the rodent to become less frightened and possibly attracted to the scent of cats, (the rodent being the intermediate host), and also infects the feline, which is the definitive host. The rodent becoming less afraid of its predator which will then increase the chances of predation by the definitive host therefore the parasite is able to continue its life cycle. (Berdoy, Webster & MacDonald 2000).
Conspicuous behaviour can also be found in the relationship between the Polymorphis laevis and its host the amphipod, the small fresh water crustacean. Amphipods would normally prefer to hide in small dark places which make them at less risk of predation, they are also known for being photobiotic creatures. However, when they become infected with Polymorphis laevis they become photophilia and also an increase amount of haemocyanin (invertebrate haemoglobin) is released causing a noticeable colour change in the amphipod (Bakker 1997). Amphipods may also become attracted to scent of the fish that would normally prey up on them (Baldauf 2007). So a creature which is usually dark and well hidden becomes a bright red, ambiguous target for its predator after becoming infected with Polymorphis laevis. It is extremely important for the parasite that the amphipod is consumed by the fish as the fish is the definitive host for the parasite to complete its life cycle.
Many studies have looked into parasites and how they change the way in which their host acts, looks or behaves and are still studying to find out if these changes are just side affects to being parasitized or whether the parasites are causing the changes to benefit themselves.
Not all behavioural changes are beneficial to the parasite, some can be side affects which may have no effect to the parasite at all. An example of this is proven by Boorstein and Ewald 1987 that when some insects are infected by parasites they undergo behavioural fever which allows the insect to raise their body temperature enough to kill the parasite.
Many investigations have taken place and are still taking place in order to find out if parasites are causing the behaviour changes in their hosts. I am going to assess the evidence of host manipulation caused by parasites and find out whether it is causation or coincidence and compare the evidence both for and against the reasons why scientists have come up with their conclusions.
Literature Analysis; Review and discussion
Redirection of metabolism in the Flesh Fly, Sarcophaga bullata, following envenomation by the ectoparasitoid Nasonia vitripennis and the correlation of metabolic Effects with the diapause status of the host (Rivers, D.B. and Denlinger, D.L., 1993)
As mentioned in the introduction, parasites are able to alter their host's behaviour in many different ways, Rivers and Denlinger 1993 based their study on how the metabolism is redirected in the fresh fly Sarcophaga bullata(Image 1) after it had been envenomed by Nasonia vitripennes (Image 2) the ectoparasitoid, and they also monitored the metabolic effects with the diapause status of the host.
From previous tests, it became clear that manipulation can cause the host's development to suppress and this suppression was being caused by the hormonal status being altered in the host. (Baronion and Sehnal, 1980; Beckage, 1985; Lawrence, 1986; Webb and dahlman, 1986; Brown and Reed-Larsen, 1991) Along with the hormonal status being altered there were also a number of parasitoid induced changes including lipid levels, protein levels and carbohydrate levels being altered. (Barlow 1962; Barras et al 1970; Dahlman 1970 and 1975; Thompson and Binder 1984; Thompson et al 1990) The parasitoid Nasonia vitripennisinjects its host with venom before feeding or oviposition (Rivers and Denlinger 1994) which leads to a developmental arrest in the pharate adults and pupae of the S. bullata. For the parasitoid to develop, the arrestment of its host is essential, but there is suggestion that a deficiency in the ecdysteroid was not the only cause for the host to arrest. Rivers and Denlinger 1993 examined the rates of consumption of oxygen in both non evenomated flies and pharate adults of S. bullata which were developmentally arrested. Effects caused by being envenomated were monitored by looking at the host during the arrestment and monitoring the levels of protein, carbohydrate, pyruvate, amino acid, lipid and oxaloacetate. They also compared if envenomation induced alterations of the metabolic reserves were present in the host that had already been in environmentally induced developmental arrest, diapuase. (Rivers and Denlinger 1993)
A number of different examinations were completed to fulfil their requirements including; Parasitoid and host rearing, exposure of parasitoid to host, oxygen consumption determination, glycogen and trehalose isolation, protein determination, lipid extractions, keto acid isolation and amino acid analysis. A full methods, materials and results section can be found in Rivers and Denlinger 1993.
In earlier experiments it was clear that hosts died as soon as they were envenomated, (Roubaud 1917, Beard 1964, Ratcliffe and King 1967) if this was true then the intermediary metabolism of the host would not be redirected, but more recent studies have shown that only hosts that were either very old or very young died straight after being envenomated. (Rivers and Denlinger 1994) The results of the examinations completed by Rivers and Denlinger 1993 shows that a host of an intermediate age will have the developmental stage arresting leaving the metabolic changes of the host consistent with the fly's metabolism.
With the results that Rivers and Denlinger came to and with advise from other peoples work it was clear evidence that metabolism is redirected after envenomation. The evidence for this includes; certain metabolites levels of concentration being altered, rates of oxygen consumption being suppressed and both host pharate adults and pupae has their developmental stage arrested.
Levels of oxygen consumption had reduced after envenomation of the host which was also monitored in experiments involving the endoparasitic Hymenoptera, the experiments including the Hymenoptera observed the respiratory suppression. (Edwards and Sernka 1969, Dahlman and Herald 1971, Jones and Lewis 1971) This resulted in the host staying alive approximately 16 days after it had been envenomated. This suggested that in the pharate adult hosts, N. Vitripennis induces a low respiratory metabolism and confirms all past observations, being injected by venom does not kill S. Bullata immediately (Rivers et al 1993, Rivers and Denlinger 1993).
A number of studies have been completed to monitor the carbohydrate levels altering in host parasite associations (Dahlman 1970, Von Brand 1979 and Thompson 1983, 1986) In many of these studies the levels of Carbohydrate within the host has decreased due to it being consumed by the growing parasites, however this was not the case for Rivers and Denlinger as they removed the parasitoids egg from the host before starting this part of the experiment. There was also an increase in the hosts pyruvate levels, together with the decrease in the carbohydrate levels of the envenomated hosts this suggests there may have been an increase in the levels of lipogenesis of nondiapause hosts. This also runs parallel with the levels of body lipids that are extracted from envenomated hosts. From these findings suggestions of increased lipid levels plays a role in the development of N. Viripennis larvae. This has also been demonstrated by other parasitoids (Bracken and Barlow 1967, Espelie and Brown 1990, Thompson and Barlow 1976) The glycogen levels initially increased in Rivers and Denlinger 1993 but then decreased after a few hours, this was probably caused by the stress of the insertion of the wasps ovipositor.
From this experiment it is clear to see that a number of different reactions occur when the fresh fly S. Bullata is envenomated by N. Vitripennis, but from the results of everything it is still unclear if whether the suppression of the developmental stage is caused by the hosts metabolism being altered or whether it precedes the metabolic disturbances. Intermediary metabolism is altered in the fly host after it has been envenomated, these alterations appear to work together with certain developmental stages during the life of the larval parasitoid, so this in affect suggests that host metabolism can be redirected by N. Vitripennis to benefit the progeny of the wasp causing the host to arrest. This could therefore be a consequence of actually altering the metabolic reserves of the host.
Evidence that the parasitic nematode Skrjabinoclava manipulates host Corophium behaviour to increase transmission to the sandpiper, Calidrispursilla(McCurdy, D.G., Forbes, M.R. and Boates, J.S. 1998)
Over many years now biologists and ecologists have been working on parasites and their interactions with their hosts. McCurdy et al based the nature of their studies on whether Skrjabinoclava morrisoni (Image 3), an acuaroid nematode (Wong and Anderson) could manipulation the behaviour of its intermediate host the Corophium volutator, (Image 4) an amphipod, to increases the transmission from the intermediate host to the definitive host the Calidris pusilla, (Image 5) a sandpiper
From previous studies it has been proven that timing of manipulation plays a vital role of the actual outcome of the manipulation. (Combes 1991, Poulin 1994, Poulin et al 1994, McCurdy et al 1998) Manipulation of the host by the parasite should only begin once the parasite has developed enough and is able to be transmitted to the final host successfully. If this timing is not accurate then it could result in the death of the parasite especially if the parasite had not reached the infective stage and has been ingested. (McCurdy et al 1998).
As with many other studies, it has proven difficult to test for actual adaptive host behavioural manipulation as it is unclear whether the changes are caused by the parasite, the host or both. (Milinski 1990, Poulin et al 1994, McCurdy et al 1998) Poulin has been involved in many studies to look into this and has found that using Meta-analysis, the behaviour of the hosts has been altered by its parasites and he also suggests that phylogenetic constraints could cause many of these behavioural changes. (McCurdy et al 1998)
For McCurdy et al to complete their studies they observed the behaviour of both infected and uninfected amphipods in both the laboratory and the field. They also observed if the infected C. Volutator showed any behavioural changes in different times of day (light intensity) - night and day time. This was monitored as Sandpipers cue for food searching changes from visual at day to tactile at night. (Mouritsen 1994, Robert and McNeil 1989, McCurdy et al.1998) So the amount of prey eaten during the day time would be much more than by night. (Boates 1980, Manseau and Ferron 1991, McCurdy et al 1997, McCurdy et al. 1998) therefore for the nematode to increase the levels of transmission to the sandpiper it would need to increase the crawling activity of the intermediate host during the day time. If the level of crawling activity was increased by night then the parasites would not be increasing their rates of transmission.
McCurdy et al. 1998 also observed many other affects the nematode may have had on the amphipod which included unrelated behaviours to the probability of being consumed by the final host. The distances that infected and non infected amphipods would travel to burrows, trail complexity, this can be affected if the organism is stressed (Alados et al. 1996) and also if the infected amphipod was phototactic whilst crawling. (A complete methods section for both laboratory and field studies can be found at McCurdy et al. 1998 along with an analysis section for the results)
The results of the experiments completed at the field sites verified that in a natural environment, the C. volutator was definitely an intermediate host for the S. morrisoni but parasitisation only took place during the summer generation of amphipods, if over winter parasitisation was taking place then the amphipods were not surviving long enough to be sampled during the sampling season of spring. Due to the sandpipers not arriving at the mud flats until July, the larval stage of the parasites were not coming to light until August causing the developmental stage to be approximately 4-5 weeks. This meant that the parasite had to complete its life cycle in a short period of time before the sandpipers migrated. (Boates 1980) Overall there was an increased presence of amphipods on the mudflats throughout the daytime which was a result of host manipulation caused by parasites. This was concluded due to the rates of transmission for amphipods that had been infected by parasites are normally low, but during this experiment the rates were high (>10,000/m2 McCurdy et al., 1997 & 1998) It was also noted that during the day, parasites which have the ability to infect were found more in crawling amphipods than in the substrate dwelling amphipods. This provides strong evidence that the parasites cause host behavioural manipulation because in previous experiments <1% of uninfected amphipods crawl (Boates et al., 1996) Whilst observing the difference in day light and night of the amphipods crawling behaviour, it was also confirmed - as predicted, that due to the sandpiper eating mainly during day time, there would be no reason for the parasite to manipulate the behaviour of the host during the night.
The results of the laboratory based experiments showed that infected amphipods were more likely to be consumed by their predators than uninfected amphipods as infected males tend to be found closer to the surface which inevitably puts it at greater risk. During the laboratory based experiments there were no signs of the amphipods being phototactic, nor were there any different crawling responses in the amphipods that were infected compared to those who were not infected. A potential explanation for this is that amphipods responses are manipulated by parasites in the field with natural cues around them, these natural cues will be missing in the laboratory causing different responses to happen.
As with the results of Wong and Anderson 1988, this experiment found that the infective stage of the nematode larvae was reached earlier whilst in the laboratory than in the field. This could have been caused by the temperatures in the field fluctuating greatly due to abiotic factors and in the laboratory the fluctuations of these abiotic factors are not possible.
From the comparison of the experiments mentioned here, it is clear to see that parasites do manipulate the behaviour of their hosts but only when the timing is right. The parasite needs to have developed to a certain stage in its life cycle to enable complete transmission successfully. There is also a possibility that the cost for the parasite to manipulate the host to undertake a number of responses to make it more susceptible to predation is too much so therefore only one change in behaviour is enough for the parasite?
The risk of parasitism may not be of too much of a risk take for the sandpipers as it was noted that they continued to eat crawling amphipods even though there was a high chance of ingesting parasites, possibly the benefits of eating prey was much higher to the sandpiper than the cost of parasitism. (Lafferty 1992)
Conclusions and Future directions
The infamous parasite which has the ability to manipulate its host's activity; the Gordian worm Spinochordodes telliniiis able to utilise land living arthropods bodies (i.e. crickets). The Gordian worm impedes with the cricket's neurotransmitter systems and as a result causes the cricket to navigate itself towards water, which is his final destination. The cricket then drowns itself in the water where the Gordian worm is able to escape from the body of the cricket and fulfil its aquatic stage in its life cycle (Biron 2005). This is clear evidence that parasites are able to manipulate their host's behaviour to suit themselves at the expense of their host. Although this example seems very clear that manipulation of the host is caused by the parasite, this is not always the case as show in the previous examples.
The interaction of two different organisms has proven to be highly complicated to all scientists. The majority of my investigation has looked mainly at behavioural traits, though the first two experiments shows how the manipulation of the host is caused by the parasite and how this is beneficial to the parasite and detrimental to the host, not all experiments conclude with this and without the correct investigations of both the phylogenetic investigation of the evolution of manipulation of that organism and the immediate reason for the change of an organism then the results will be inconclusive. (Poulin, R. 2002)
Suggest new experimental strategies with a brief outline of the research techniques you would use.
Acknowledgements
References
Alados, C.L., Escos, J.M. Emlen, .M. 1996. Fractal structure of sequential behaviour patterns: an indicator of stress. Anim. Behav. 51:437-443
Allan, S.A., Day, J.F., and Edman, J.D. 1987. Visual Ecology of Biting Flies. Annual review of Entomology. Vol. 32:297-314
Bakker, T.C.M. 1997. Parasite-induced changes in behaviour and colour make Gammarex pulex prone to fish predation. Ecology 78: 1098 - 1104
Baldouf, S. 2007. Infection with acanthocephalan manipulates an amphipod's reaction to a fish predator's odours. Int. J. Parasite. 37:61-65
Barlow, J.S. 1962. An effect of parasitism on hemolymph electro-pherograms. J. Insect Physiol. 36:274-275
Baronio, P and Sehnal, F. 1980.Dependence of the parasitoid Gonia cinercascens on the hormones of its lepidopterous hosts. J. Insect Physiology. 26: 619-626
Barras, D.J., Joiner, R.L., and Vinson, S.B. 1970. Neutral lipid composition of the tobacco budworm, Heliothis virescens (Fab.) as affected by its habitual parasite, Cardiochiles nigriceps Viereck. Comp. Biochem Physiol. 36:775-783
Beckage, N.E. 1985. Endocrine interactions between endoparasitic insects and their hosts. A. Rev. Entomol. 30: 371-413
Berdoy, M., Webster, J.P., MacDonald, D.W. 2000. Fatal attraction in rats infected with Toxoplasmosis gondii. Proc. R. Soc. B. 267(1452): 1591-1594
Biron, D.G. 2005. Behavioural manipulation in a grasshopper harbouring hairworm: a proteomics approach. Proc. R. Soc. B. 272:2117-2126
Boates, J.S. 1980. Foraging semipalmated sandpipers (Calidris prusilla L.) and their major prey, C. volutator (Pallas) on the Starrs Point mudflat, Minas Basin (MSc dissertation). Kentville, Nova Scotia: Arcadia University.
Boates, J.S. Forbes, M. Zinck, M. and McNeil, N. 1995 Male amphipods Corophium volutator [Pallas] show flexible behaviour in relation to risk of predation by sandpipers. Ecoscience 2: 123-128
Bracken, G.K. and Barlow J.S., 1967. Fatty acid composition of Exteristes comstockii reared on different foods. Can. J. Zool. 45;57-61
Brown. J.J and Reed-Larsen D 1991. Ecdysteroids and insect host / parasitoid interactions. Biol. Control. 1:136-143
Buckling, A., Hodgson, D.J. 2007. Short-term rates of parasite evolution predict the evolution of host diversity. J. Evol. Biol. 20(5):1682-1688
Combes, C. 1991. Ethological aspects of parasite transmission. The American Naturalist. Vol. 138, No. 4. 866-880
Coombes, C. 2001. Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago. 192-196
Dahlman, D.L. 1970. Trehalose levels in parasitized and nonparasitised tobacco hornworm, Manduca sexia, larvae. Ann. Entomol. Soc. Am. 63:615-617
Dahlman, D.L 1975. Trehalose and glucose levels in hemolymph of diet-reared tobacco leaf-reared and parasitized tobacco hornworm larvae. Comp. Biochem. Physiol. 50A;165-167
Dahlman, D.L. and Herald, F. 1971. Effects of the parasite, Apanteles congregates, on respiration of tobacco hornworm, Manduca sexta, larvae. Comp. Biochem. Physiol. 40A; 871-880.
de Castro, F., Bolker, B.M. 2005b. Parasite establishment and host extinction in model communities. Oikos 111 (3): 501-513 Bethesda, MD: National Library of Medicine (US), National Center for Biotechnology Information, c2005.
Edwards, J.S. and Sernka T.J. 1969. On the action of Bracon venom Toxicon 6; 303-305.
Espelie, K. and Brown, J.J. 1990. Cuticular hydrocarbons of species which interact on four trophic levels: apple Malus pumilla, codling moth Cydia pomonella L, a hymenopteran parasitoid Ascogaster quadridentata Wesmael; and a hyperparasite, Perilampus fulvicornis Ashmead. Comp. Biochem. Physiol. 95B; 131-136
Farmer, D.C. and Barnard C.J. 1999. Fluctuating asymmetry and sperm transfer in male decorated field crickets (Gryllodes sigillatus). Behav Ecol Sociobiol 2000 47:287-292.
Jones R.L. and Lewis W.J. 1971. Physiology of the host parasite relationship between Heliothis zea and Microplitis croceipes. J. Insect. Physiol. 17;921-927
Kaltz, O., Gandon, S., Michalakis, Y., and Shykoff. J.A. 1999. Local maladaptation of the plant pathogen Microbotryum violaceum to its host Silene latifolia: Evidence from a cross-inoculation experiment. Evolution 53:395-407
Lafferty, K.D. 1992. Foraging on prey that are modified by parasites. American Nature. 140: 854-867
Lawrence, P.O. 1986 Host parasite hormonal interactions: an overview. J. Insect Physiology. 32:295-298
Mains, E.B. 1949. Cordyceps bicephala, berk and c, australis. Bulletin of the Torrey Botanical Club 76(1):24-30
Manseau, M., Ferron, J. 1991. Activite alimentaire nocturne des becasseraux semipalmes (Calidris prusilla) lors d'une halte migratoire dans la baie de fundy. Can J. Zool. 69: 380-384
McCurdy, D.G., Boates, J.S. and Forbes, M. 1997. Diurnal and nocturnal foraging by semipalmated Sandpipers. J. Avian. Biol. 28: 353-356
McCurdy, D.G., Forbes, M.R. and Boates, J.S. 1998. Evidence that the parasitic nematode Skrjabinoclava manipulates host Corophium behaviour to increase transmission to the sandpiper, Calidris pursilla. Behav. Ecol. Vol. 10 No 4: 351-357
Milinski, M. 1990. Parasites and host decision making in: parasitism and host behaviour (Barnard CJ. Behnke JM, eds) London: Taylor and Francis; 193-233
Mouritsen, K.N. 1994. Day and Night feeding in dunlins Calidris alpine choice of habitat, foraging technique and prey. J. Avian Biol 25: 55-62
Poulin, R. 1994a. The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology. 109: S109-S118
Poulin, R. 1994b. Meta analysis of parasite induced behavioural changes. Anim. Behav. 48: 137-146
Poulin, R. 2002. Parasite manipulation of host behaviour. The behavioural ecology of parasites. Chapter 12; 243-257
Poulin, R., Brodeur, J. and Moore, J. 1994. Parasite manipulation of host behaviour: should the hosts always lose? Oikos 70:479-484
Poulin, R., Morand, S., and Skorping, A. 2000. Evolutionary Biology of Host-
Parasite Relationships: Theory meets reality. 97-116.
Rivers, D.B. and Denlinger, D.L. 1994. Developmental fate of the fresh fly, Sarcophaga bullata envenomated by the pupal ectoparasitoid Nasonia vitripennis. J. Insect. Physiol. 40;121-127
Rivers, D.B., Hink, W.F. and Denlinger, D.L. 1993. Toxicity of the venom from Nasonia vitripennis (Hymenoptera: pteromalidae) toward fly host, nontarget insects, different developmental stages and cultured insect calls. Toxicon 31; 755-765
Robert, M. and McNeil, R. 1989. Comparative day and night feeding strategies of shorebird species in a tropical environment. Ibis. 131: 69-79.
Thompson, S.N. 1983. Biochemical and physiological effects of metazoan endoparasites on their host species. Comp. Biochem. Physiol. 74B; 183-211
Thompson, S.N. 1986. Effects of the insect parasite Hyposter exiguae (Viereck) on the carbohydrate metabolism of its host, Trichoplusia ni (Hubner). J. Insect. Physiol. 32; 287-293
Thompson, S.N. and Barlow, J.S. 1976. Regulation of lipid metabolism in the insect parasite Exeristes roborator (Fabricius). J. Parasitol. 62; 303-306
Thompson, S.N. and Binder, B.F. 1984. Altered carbohydrate levels and gluconeogenic enzyme activity in Trichophusia ni parasitized by the insect parasite, Hyposter exiguae. J. Parasitol. 70:644-651
Thompson, S.N., Lee, R.W.K. and Beckage, N.E. 1990. Metabolism of parasitized Manducs sexta examined by nuclear magnetic reasonance. Arch. Insect Biochem. Physiol. 13:127-143
Von Brand, T. 1979 Pathophysiology of the host. In Biochemistry and Physiology of Endoparasites, pp. 321-390. Elsevier/North Holland Biochemical Press. Amsterdam
Webb, B.A and Dahlman, D.L. 1986. Ecdysteroid influence on the development of the host Heliothis virescens and its endoparasite Microplitis craceipes. J. Insect. Physiology. 32:339-345
