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The interactions between parasites and biodiversity, in particular, their stabilising and destabilising effect on species and gene diversity is discussed. Parasites evidently play a role in biodiversity by interfering in various processes, which becomes more apparent if there is a disruption to the norm, such as in competition, speciation, migration, fecundity and extinction. The certain examples selected for stabilising role of parasites shows that they are essential in maintaining equilibrium, where they can make two unlikely species coexist and also stop a foreign species taking over the native species, thus maintaining biodiversity. PARASITIC DNA. They are also influential at the genetic level where parasites are able to preserve gene pools as seen in Sage et al (1986) work on mice. However, they can also have destabilising roles where they can have fatal effects, dismantling a food web, leading a species to become extinct, and decreasing host fecundity. It has also been found that they can indirectly cause devastation, as seen in the nesting example where parasitising the young can decrease the parents fecundity. Additionally, parasites can regulate host hormones, and increase or decrease their own and their hosts' fecundity. Males have been found to be more susceptible to parasites than females in most cases owing to testosterone which reduces the immune response. It is evident that parasites play a pivotal role and can either increase or decrease biodiversity depending upon the situation. Not to mention the fact that parasites are a major part of biodiversity should not be overlooked.
The Earth is inhabited somewhere within the region of three to a hundred million species (Heywood, 1995). Picturing this vast range of diversity seems impossible let alone describing. It wasn't until 1986 that this was achieved by Walter Rosen, who came up with the term "bio diversity" (Wilson, 1988). The term can be applied much more broadly with the UN Convention on Biological Diversity defining biodiversity as "the variability among living organisms from all sources including, inter alia, terrestrial, marine and other aquatic ecosystems and the ecological complexes of which they are part; this includes diversity within species, between species and of ecosystems" (United Nations Environment Programme, 1992). Thus, biodiversity can be summed up as an umbrella that covers the diversity of species, genes, and ecosystems.
The major threat to biodiversity is human activity which can have various consequences such as, an increased global rate of species becoming extinct. One of the primary concerns is habitat loss, which can be caused by various factors, one of which is land being converted for another use, for instance, agriculture that prevents many species from persisting (Armsworth, 2004). Another cause could be degradation, where humans reduce the habitat to a poor quality such as, pollution and pesticides. These can also reduce the survival rates of some species, where some can become locally extinct. Harvesting such as fishing could have a negative effect on the particular species, and thus potentially parts of the food web. The introduction rate of foreign species from different continents has greatly increased. Lastly, climate change is a well known threat where changes in the temperature or rainfall patterns can dictate the survival of a species, leading to a decline in population. This can be prevented if the species is able to adapt or migrate to a more appropriate location. All the threats above can be unsettling to a species or community. Furthermore, climate change is thought to be an increasing concern. Where as, in the short term the most damaging threat to biodiversity especially in terrestrial systems is habitat loss (Armsworth, 2004).
Parasitology is a field that has been often misunderstood, where its significance is greatly underestimated. However, it has not been long since this area of biology has been accepted as important by ecologists and evolutionary biologists as Dawkins stated: " Eavesdrop morning coffee at any major centre of evolutionary theory, and you will find 'parasite' to be one of the commonest words in the language" (Combes, 1995).
Parasitism is a symbiotic relationship in which one organism (parasite) lives in or on another organism (the host) and consequently harms the host while it benefits. They can be classed on the basis of the location they reside in, endoparasites are the ones that are remain within the host whereas, endoparasites are those that live on the host's exterior. Additionally, they can be further classed on the basis of size where microparasites are small and not visible to the naked eye and macroparasites is where they can be seen without a microscope
Parasites can directly influence the host by affecting its growth, reproduction and survival chances, which indirectly impacts the ecosystem it lives within and consequently the whole biosphere. Parasites may play a pivotal role indirectly on biodiversity of species by intervening in various processes such as competition, migration, speciation and stability (Combes, 1995). It is because of the role of parasites in these processes that its importance in controlling biodiversity is apparent, where they can either protect or harm biodiversity.
Parasitism and biodiversity individually are areas with vast depth; as a consequence I will primarily be focussing on parasites in animals and humans within the terrestrial ecosystem. There are various studies conducted on species and genes diversity thus this will be the focus of this paper. The roles of parasites will be differentiated based on stabilising and destabilising, which is discussed subsequently in the Anderson and May model.
Anderson and May Model
In parasitology mathematical modelling is incredibly useful in understanding the relationship between host and parasite populations. The equations allow us to gain an insight to describe and predict the effect of different variables on particular outcomes. However, this tool has its limitations, where the variables are often oversimplified, and factors such as genetic diversity are overlooked. Although, these models are still valuable as they provide an insight into host parasite relationships (Combes,1995). The first model was proposed by Crofton (1971) describing a relationship between parasite and host populations, fuelling the progression of work in parasite ecology. Crofton took into account the following five variables:
reproductive rate of the host
reproductive rate of the parasite
the extent of parasite transmission
the degree of parasite aggregation
lethal threshold of parasitism
However, this model was too simple, and it was Anderson and May (1978) who built on this model. Their advanced model is of great significance, where they show some processes either having a stabilising or a destabilising effect on host- parasite systems. The stabilising factors include total distribution of parasites in the host population, a non-linear relationship involving host mortality and parasite load and also regulation of density dependant parasites in infra populations. Whereas, destabilising factors include parasites lessening the fecundity of the host, parasites reproducing in the host, and waiting stages during their life cycle. In general, this advanced model shows that the stability of host-parasite systems is reliant upon the stabilising and destabilising factors. Consequently, altering any of the variables in the model enables realistic simulation of the changes to be viewed (Anderson & May, 1978). Generally, this model shows that parasites can regulate their host populations as long either the parasites are collectively distributed or the pathogenic effect has to be faster than the parasite load.
The stabilising role of parasites
Preserving gene pools
An example in humans where their genes dictate their susceptibility to parasites is seen in Malaria. Malaria is a mosquito borne infectious disease caused by the protist, Plasmodium. The parasite can only penetrate blood cells once it recognises and uses protein receptors on the cell membrane. The protein that is required for the internalisation of Plasmodium vivax into red blood cells is absent in black Africans and protects them from P.vivax (Miller,1994). In addition, genetic mutations of erythrocytes could affect receptivity to malaria, which can be seen in the link between malaria and sickle cell anaemia. People with sickle cell anaemia have a single nucleotide mutation in their DNA that causes the formation of S haemoglobin instead of the normal H. Those that are homozygous for the sickle cell genotype have a reduce life expectancy whereas the heterozygous survive and are protected against the malarial agent. Thus, it would be assumed that (SS) homozygous would be severely sickle cell disease, and those homozygotes (HH) would get malaria, and the heterozygotes (HS) would be better off and escape both fatalities (Freidman et al 1979). This explains the high frequency of genetic disease like sickle cell in countries where malaria is endemic. The parasite is preserving SS gene pool in these regions, and ensuring that the gene isn't eradicated, by targeting those that have normal haemoglobin genes. Also the absence of the antigen from Africans protects them from invasion from the Europeans. It is apparent in the individual cases such as malaria, where the person's genetic makeup dictates their susceptibility to infection.
The various diverse species present on Earth is owing to reproductive isolation. This process allows reproductive barriers to form to prevent genomes from mixing thus we have humans, dogs and parasites. Research conducted has led the role of parasites in host speciation to be questioned and whether they have a role in species composition of ecosystems (Combes,1995). This is seen in particular in a study by Sage et al (1986) on two species of mice in Europe, Mus musculus musculus and Mus musculus domesticus. M.musculus is found in the east and M. domesticus in the west, and where these areas join in the centre is known as the hybrid zone. This is where the two species of mice form hybrid mice.
Despite both species being in effect "semi species" they strangely did not mix even though they were able to hybridise. Sage et al (1986) identified more than 10,840 worms in 93 mice.
Figure 1(original) - Wormy mice found and their genetic makeup
The figure above shows they found that heavily parasitised mice were hybrids, suggesting that increased parasitism has a genetic basis, where by hybrid mice are more susceptible than pure mice to parasites. Further research by Moulia et al (1991) where they undertook genetic analysis confirms that these findings. It appears that the areas of the two semi species are most probably preserved by parasites. This explains why despite hybrids being formed the two semi-species still do not merge, making the hybrid zone appear almost like a 'sink' for recombinant genes. Furthermore, their findings suggest that parasitism could influence genetic structuring and isolation of populations. In this case, it is clear that parasites can stabilise and preserve gene pools through reproductive isolation where they prevent the mixing of the two semi species of the Musculus mice. The extent to which parasites' have control is evident, where they could potentially be a part of shaping the evolutionary path by segregating genomes, forming the different species we have today.
What defines a parasite is very broad, to the extent where there is even controversy surrounding whether 'junk DNA' can be called parasitic. It may come as a surprise to many that even nucleic acids can be parasites Usually this junk DNA is in the form of transposable elements (TEs), which are DNA sequences that can move around the genome and are found in bacteria, plants and animals. (Kidwell, 2000) . They are able to change the DNA quantity and cause mutations. It is thought that TEs enable the host genome to develop its own evolution. Furthermore, TEs could be a primary source for genetic diversity, allowing reactions to any changes such as environmental to occur. Jordan et al (2003) examined the human genome where they looked at varying classes of regulatory region to analyse the possible involvement of TEs in gene regulation. They found that around 25% of the analysed promoter regions enclosed TE-derived sequences. There were also TE derived sequences within the scaffold/matrix attachment regions (S/MARs) and locus control regions (LCRs), both are implicated in the simultaneous regulation of several genes (Jordan et al, 2003). Therefore, TEs have almost certainly contributed significantly to the evolution of gene-specific and global patterns of human gene regulation. This highlights that regulation of biodiversity can even occur at the molecular level where even DNA sequences are believed to be capable of gene regulation.
Parasites can have profound impacts on the structure of animal communities, and a primary process that this is achieved by is competition. Competition can have catastrophic effects where parasitism can favour one species more than the other and consequently decrease the population of the dominated species dramatically, thus reducing biodiversity. This is seen in a study by Tompkins et al 2000 where they investigated introduced pheasants, Phasianus colchicus, which carried the caecal nematode Heterakis gallinarum, which infected the wild grey partridge Perdix perdix. This caused a decline in the partridge population in the UK (Tompkins et al, 2000). Whereas the pheasants are generally unaffected but rather act as a reservoir for the parasite and is necessary for the persistence of the parasite in the partridge population. However, parasites are also able to have a stabilising effect where they can maintain an equilibrium between two species known as parasitic arbitration ( Combes,1995). A classic example was reported in Texas with ants, where the ant Pheidole dentata is usually dominates over Solenopsis texana However, during certain times of the year a dipteran parasite is present and reverses the dominance to favour S.texana. This is because the parasitoid attacks the soldiers of P.dentata and these solidiers are the ones that attack S.texana when they approach the bait (Feener 1981). This highlights a parasites ability to maintain biodiversity where the decreased population of S.texana is allowed to recover.
Parasites are known to be involved in animal migration, where they can dictate if a species is able to relocate, which as a consequence impacts biodiversity of the habitats. If a species is able to relocate this could increase biodiversity, where they could move to a more suitable habitat that favours them and where conditions increase their fecundity. Freeland (1983) considers that differences in a host's susceptibility to parasites may be significant in a species' ability in migrating to a new location. This could be problematic for migrations whereby a foreign species can only invade an ecosystem if it's less vulnerable to parasites that the resident species. It is not allowing foreign species to migrate which allows parasites to have a stabilising effect where they protect local species from invasion. This is seen in an example where the North American ungulate species, Odocoileus virginiatus, is protected from invasion of foreign species by Parelaphostrongylus tenuis, a nematode. This is owing to its adaptation, especially in comparison to other ungulates such as the moose Alces alces which is highly susceptible and experiences high mortality rates whilst invading the zones inhabited by O.virginiatus ( Anderson,1972).
Additionally, migration of humans has also been affected, particularly, when taking into account that malaria prevented the conquest for many years of the sub-saharan Africa by Caucasians whereas the Africans' broad genetic diversity allowed them to resist any pathogens brought by Europeans. Similarly, in cattle efforts in importing European cattle into Africa failed because of sleeping sickness, African trypanosomasis (Combes, 1995).
Parasitic protection against enemies
Parasites have the ability to protect hosts from more pathogenic parasites by unexpected means, where simply having the mere presence of more benign species is sufficient. This is owing to the benign species using up most of the necessities such as, food and space. A classic example of this is in nature is in humans where the foetus lacks bacterial colonisation and this is soon overcome when cutaneous microbes (normal flora) rapidly colonise in the birth canal and during contact with the mother ( Price et al, 1986). This colonisation process of various different species and population sizes is completed by the ninth day post birth. This use of the resources by normal flora is absolute that even other strains of the same Staphylococcus species are usually not present in the nose of a neonate. This preemption is prevalent in nature especially amongst human populations. It is the colonisation of these benign strains that prevent infection by pathogenic organisms. This role of parasites conveys their ability to protect their hosts from other pathogens, keeping them healthy and well, which in a sense is a form of regulation, where the presence or absence could dictate susceptibility to certain pathogens and thus diseases and mortality ( Price et al, 1986).
The destabilising role of parasites
Differences in genetic makeup are known to have an effect on the susceptibility to parasite infection, however, this can also been extended to gender differences. In most cases males are known to be more susceptible to parasitic infections than females.( Combes,1995) Many could argue that these differences are based on behavioural and social variations, such as males being more aggressive, involved in more fights and having a larger body size, increasing their exposure which would make them more of a parasitic target (Klein, 2004). However, several studies have shown that differences in immunity to pathogens are based on steroid hormones. One frequently, reported effect is referred to as the "immunocompetence handicap of males". This handicap exists because testosterone decreases the efficacy of the tissues and organs involved in immune defence (Combes, 1995). Male-biased infections are commonly protozoan and nematode parasites in various hosts such as, Leishmania, Plasmodium and Schistosoma parasites. The increased immunity in females can come at a price where they are more likely to develop autoimmune diseases. However, there are exceptions that are thought to be due to endocrine-immune interactions, where females can be more susceptible such as with the Toxoplasma gondii pathogen; mouse models have shown that they develop more severe brain inflammation and have a greater chance of dying post-infection than males (Klein, 2004)
In addition, it has also been found that parasites can produce and alter host hormone concentrations. The extent to which these changes occur is dependent upon the host and parasite in question (Klein, 2004). For example when Plasmodium berghei infects female mice the oestradiol and progesterone concentrations increase (Aina et al, 1990). Whereas, P.chabaudi restrains testosterone concentration in males (Barthelemy et al, 2004). Additionally, when T. crassiceps or T. taeniaeformis infects male rodents they decrease testicular testosterone concentrations and increase oestradiol concentrations. The increase in oestradiol increases parasitic reproduction and hinders mating behaviour (Morales et al 1996). In particular Taenia crassiceps is also able to produce steroid hormones, such as testosterone, which could lead to increase parasitic growth and reproduction and inhibition of host responses. This is owing to the testosterone produced being aromatized into oestradiol (Romano et al 2003).
It is apparent that the genders of species is significant to its susceptibility, where it is thought to be one of the primary causes of amplified death rates among men as compared with women. This could potentially cause an imbalance in various populations where infections occur. Thus, parasites could be controlling biodiversity here. Furthermore, their ability in altering and producing host hormones highlights their capacity to manipulate and regulate host populations whereby they can reduce host fecundity and increase their own reproduction.
It is usually human intervention that leads to radical occurrences. A prime example where the introduction of a foreign species carrying a parasite decreases the native species is of the Caspian sturgeon, Acipenser stellatus in the Aral Sea. This species was parasitized by Nitzchia sturionis, a gill monogenan. This species was introduced for economic purposes and was transferred onto the territory of the native A.nudiventris sturgeon where it cause catastrophic mortalities, where it is reported to have taken 20 years for A. nudiventris to reach a normal population size ( Bauer et al 1976). Additonally, Malmberg (1993) found that the introduction of salmon in the Baltic Sea caused fatal mortalities in the local populations. The cause of this was the parasite, Gyrodactylus salaris, which lived primarily on the fins. It is apparent from these examples that specific parasites for certain host species can have catastrophic effects with species becoming extinct. This clearly is an example of where parasites reduce biodiversity. However, these examples are in extreme situations and though these parasites cause mortalities it points out the possibility that if they have the capacity to exterminate species under normal conditions they most probably have the power to maintain and regulate populations.
Parasites are even able to manage their host's fitness by getting involved in their sexual behaviour where they decrease the ability to reproduce or diminish their chances of choosing a suitable mate. This is seen in Morales et al's (1996) work on mice, where after being infected by Taenia crassiceps, the male mice became more feminised and practically lost their masculinity. Five weeks after infection they stopped ejaculating and after seven weeks of infection they stopped copulation. This is owing to a fall in male hormones and then a strong increase in female hormones, thus in this situation these adapted males could be seen as "genetically dead" (Morales et al's 1996).
Parasites can decrease regulation of biodiversity by decreasing its host's fecundity. Albon et al (2002) conducted a six year study on Svalbard reindeer and its gastrointestinal macroparasite, Ostertagia gruehneri. They found that the macroparasite had regulatory effects, whereby it had considerable impact on host population dynamics. They found a strong correlation between reindeer treated with anthelminthic treatment and pregnancy. The effect that this treatment had on calf production is best seen in a comparison where the effect varied between 0.02, in 1996, and 0.13, in 1998. Thus, it is clearly apparent that parasites can regulate host population by decreasing the host's fecundity (Albon et al 2002).
Indirect Cascade effect
Parasites in most situations affect one aspect of biodiversity; however, this change is usually not isolated and can have a domino effect whereby other changes occur. Thus all the topics discussed above could be included, some of which will be apparent in the following example of blood sucking ectoparasites present in birds' nests. Tripet and Richner (1997) investigated the blue tit population in Switzerland where they compared nests that infected with uninfected ones with the bird flea Ceratophyllus gallinae. They found that the parents had to compensate by providing more food for parasite infected nests. If this was done then there was no actual cost of parasitism for the nestlings, hence the there was no great effect on body mass or mortality owing to the fleas. However, when they were normally nourished they would suffer from growth reduction or death. Additionally, Richner and Tripet (1997,1999) found that parasitism had a negative impact on whether the tits would return as breeders. They also found that males increased their food provisioning and were more susceptible to parasitic infections themselves. The cascade effect is evident where parasites have an indirect effect on the parents where they have to invest more effort in providing for their young and are more likely to get parasitized. More importantly, parasites can regulate the host population by decreasing the chance of the parents reproducing again if they already have young (Tripet and Richner (1997).
Parasitic disease is often hard to spot, with its actual influence on its host and consequently on biodiversity being underestimated. However, ignoring the relevance of parasites is now an occurrence of the past, with ecologists and evolutionists paying particular attention to this field. It is often the case that parasites have evolved to coexist with their hosts inconspicuously without causing any real disturbance to their host or at the population level. Though, the examples I have selected clearly indicate that parasites play a major role in each circumstance which affects the habitat. The stabilising roles of the parasites clearly show that they are capable of maintaining biodiversity, whether it be by preserving gene pools or by allowing species to co exist. They are also able protect species from other pathogens and regulate migration.
Additionally, the destabilising roles of parasites, where they can cause destruction, further highlights a parasites ability in manipulating and modifying the diversity of species genetics and ecosystems. It raises the question that if parasites can orchestrate catastrophic events such as, extinctions then it could plausible for them to have regulatory roles under normal conditions. It is imperative to bear in mind that isolating parasitism or other factors that could impact is difficult as well as most host parasite systems being at equilibrium until a slight imbalance.
Overall, it is apparent that parasites can have stabilising or destabilising roles though it is difficult to suggest what they are globally. Parasites can easily preserve biodiversity or even be detrimental to it. The Anderson and May model supports the concept that parasites having regulatory roles, where a minor imbalance in the system could be disruptive. Furthermore, the actual concept of whether parasites regulate biodiversity is itself difficult to conclude as the fact that parasites are a big part of biodiversity cannot be overlooked and thus they can regulate themselves. This is even apparent where the normal flora in a foetus protects other parasitic pathogens from settling, this in a sense is a form of parasitic regulation, whereby it could reduce the diversity of parasitic species in that host. However, for the purposes of this paper and based on the research conducted I conclude that in certain situations, parasites have the capacity to regulate, whether it is gene diversity or species diversity, and thus they can regulate biodiversity. Although, regulation is not always the case; parasites with destabilising roles can have fatal effects such as, reducing the gene pool, and affecting entire food webs possibly by making one species more dominant than the other and causing another to near extinction. However, we need to bear in mind that there could be various contributors to regulation aside from parasites, with the degree of their involvement varying in each situation. It is essential that attention is given to the apparently harmless, regular parasites as it may give an insight into consequences than the more visibly epidemics.