Effects of parasites on the survivorship growth and fecundity of hosts

According to strict definition, parasites cause harm to their host. But it is not always easy to demonstrate this harm, which may be detectable only at some peculiarly sensitive stage of the host's life history or under particular circumstances (Toft & Karter, 1990). Indeed, there are examples of 'parasites' that feed on a host but prevalence, intensity and mean intensity

M 200

Poisson

Negative binomial Observed l

2 4 6 8 10 Number of parasites per host

Hyperendemic

1 10 100 Number of worms per mg skin-snip

1000

Figure 12.12 Examples of aggregated distributions of parasite numbers per host. (a) Crayfish, Orconectes rusticus, infected with the flatworm Paragonimus kellicotti. The distribution is significantly different from Poisson (random) (X2 = 723, P < 0.001) but conforms well with a 'negative binomial', which is good at describing aggregated distributions: X2 = 12, P ~ 0.4. (After Stromberg et al., 1978; Shaw & Dobson, 1995.) (b) Distribution of Onchocerca vulvulus worms, which cause onchocerciasis or 'river blindness', in human Yanomami communities in southern Venezuela. Again the distributions, plotted as cumulative frequencies (black lines), conform well to a negative binomial distribution (colored lines), whether the typical intensity of infection is low (hypoendemic), moderate (mesoendemic) or high (hyperendemic). (After Vivas-Martinez et al., 2000.)

appear to do it no harm. For example, in natural populations of Australia's sleepy lizard, Tiliqua rugosa, longevity was either not correlated or was positively associated with their load of ecto-parasitic ticks (Aponomma hydrosauri and Amblyomma limbatum). There was no evidence that the ticks reduced host fitness (Bull & Burzacott, 1993).

There are of course, none the less, examples in which a detrimental effect of a parasite on host fitness has been demonstrated. Table 12.3, for example, shows one particular compilation of studies in which experimental manipulation of the loads of animal parasites revealed effects on either host fecundity or survival. (And while an effect on fecundity may seem less drastic than one on mortality, this seems less to be the case if one thinks of it as the death of potentially large numbers of offspring.)

On the other hand, the effects of parasites are often more subtle than a simple reduction in survival or fecundity. For example, the pied flycatcher effects are often subtle...

Table 12.3 The impact of various parasites on the fecundity and survival of wild animals, as demonstrated through the experimental manipulation of parasite loads. (After Tompkins & Begon, 1999, where the original references may be found.)

Host

Parasite

Impact

Anderson's gerbil (Gerbillus andersoni)

Synoternus cleopatrae (flea)

Reduced survival

Barn swallow (Hirundo rustica)

Ornithonyssus bursa (mite)

Reduced fecundity

Cliff swallow (Hirundo pyrrhonota)

Oeciacus vicarius (bug)

Reduced fecundity

European starling (Sturnus vulgaris)

Dermanyssus gallinae (mite)

Reduced fecundity

Ornithonyssus sylvarium (mite)

Reduced fecundity

Great tit (Parus major)

Ceratophyllus gallinae (flea)

Reduced fecundity

House martin (Delichon urbica)

Oeciacus hirundinis (bug)

Reduced fecundity

Pearly-eyed thrasher (Margarops fuscatus)

Philinus deceptivus (fly)

Reduced fecundity

Purple martin (Progne subis)

Dermanyssus prognephilus (mite)

Reduced fecundity

Red grouse (Lagopus lagopus)

Trichostrongylus tenuis (nematode)

Reduced fecundity

Snowshoe hare (Lepus americanus)

Obeliscoides cuniculi (nematode)

Reduced survival

Soay sheep (Ovis aries)

Teladorsagia circumcincta (nematode)

Reduced survival

Figure 12.13 The mean date of arrival (1 = May 1) in Finland of male pied flycatchers (Fidecula hypoleuca) infected and uninfected with Trypanosoma: (a) 1989 and (b) 1990. adult males; o, yearling males. Sample sizes are indicated near the standard deviation bars. (c) The proportion of males infected with Trypanosoma amongst groups of migrants arriving in Finland at different times. (After Ratti et al., 1993.)

Figure 12.13 The mean date of arrival (1 = May 1) in Finland of male pied flycatchers (Fidecula hypoleuca) infected and uninfected with Trypanosoma: (a) 1989 and (b) 1990. adult males; o, yearling males. Sample sizes are indicated near the standard deviation bars. (c) The proportion of males infected with Trypanosoma amongst groups of migrants arriving in Finland at different times. (After Ratti et al., 1993.)

(Ficedula hypoleuca) migrates from tropical West Africa to Finland to breed, and males that arrive early are particularly successful in finding mates. Males infected with the blood parasite Trypanosoma have shorter tails, tend to have shorter wings and arrive in Finland late and so presumably mate less often (Figure 12.13). Another example is provided by lice that feed on the feathers of birds and are commonly regarded as 'benign' parasites, with little or no effects on the fitness of their hosts. However, a long-term comparison of the effects of lice on feral rock doves (Columba livia) showed that the lice reduced the thermal protection given by the feathers and, in consequence, heavily infected birds incurred the costs of requiring higher metabolic rates to maintain their body temperatures (Booth et al., 1993) and in the time that the birds spent in preening to keep the lice population under control.

In a similar vein, infection may make hosts more susceptible to predation. For example, postmortem examination of red grouse (Lagopus lagopus scoticus) showed that birds killed by predators carried significantly greater burdens of the parasitic nematode Trichostrongylus tenuis than the presumably far more random sample of birds that were shot (Hudson et al., 1992a). Alternatively, the effect of parasitism may be to weaken an aggressive competitor and so allow weaker associated species to persist. For example, of two Anolis lizards that live on the Caribbean island of St Maarten, A. gingivinus is the stronger competitor and appears to exclude A. wattsi from most of the island. But the malarial parasite Plasmodium azurophilum very commonly affects A. gingivinus but rarely affects A. wattsi. Wherever the parasite infects A. gingivinus, A. wattsi is present; wherever the parasite is absent, only A. gingivinus occurs (Schall, 1992). Similarly, the holoparasitic plant, dodder (Cuscuta salina), which has a strong preference for Salicornia in a southern Californian salt marsh, is highly instrumental in determining the outcome of competition between

Salicornia and other plant species within several zones of the marsh (Figure 12.14).

These latter examples make an important point. Parasites often affect their hosts not in isolation, but through an interaction with some other factor: infection may make a host more vulnerable to competition or predation; or competition or shortage of food may make a host more vulnerable to infection or to the effects of infection. This does not mean, however, that the parasites play only a supporting role. Both partners in the interaction may be crucial in determining not only the overall strength of the effect but also which particular hosts are affected.

Organisms that are resistant to parasites avoid the costs of parasitism, but, as with resistance to other natural enemies, resistance itself may carry a cost. This was tested with two cultivars of lettuce (Lactuca sativa), resistant or susceptible by virtue of two tightly linked genes to leaf root aphid (Pemphigus bursarius) and downy mildew (Bremia lactucae). The parasites were controlled by weekly applications of insecticides and fungicides. Resistant forms of lettuce bore fewer axillary buds than susceptibles (Figure 12.15), and this cost of resistance was most marked when the plants were making poor growth because of nutrient deficiency. In nature, hosts must always be caught between the costs of susceptibility and the costs of resistance.

Establishing that parasites have a detrimental effect on host characteristics of demographic importance is a critical first step in establishing that parasites influence the population and community dynamics of their hosts. But it is only a first step. A parasite may increase mortality, directly or indirectly, or decrease fecundity, without this affecting levels or patterns of abundance. The effect may simply be too trivial to have a measurable effect at the population level, or other factors and processes may act in

... affecting an interaction

Arthrocnemum-Salicornia border

• Strong parasite impact

• Strong parasite preference

• Strong symmetric competition

• Strong indirect positive effect

Cuscuta 4

High Salicornia zone

• Strong parasite impact

• Strong parasite preference

• Strong asymmetric competition

• Strong indirect positive effect

Cuscuta V

Limonium Frankenia

Cuscuta 4

Cuscuta V

Limonium Frankenia

Uninfected d Infected

100 r

Salicornia

Arthrocnemum

Salicornia

Arthrocnemum

1994 1995

I Salicornia d Limonium ■ Frankenia

1994 1995

1994 1995

I Salicornia d Limonium ■ Frankenia

Uninfected Infected

Figure 12.14 The effect of dodder, Cascuta salina, on competition between Salicornia and other species in a southern Californian salt marsh. (a) A schematic representation of the main plants in the community in the upper and middle zones of the marsh and the interactions between them (solid lines: direct effects; dashed lines: indirect effects). Salicornia (the relatively low-growing plant in the figure) is most attacked by, and most affected by, dodder (which is not itself shown in the figure). When uninfected, Salicornia competes strongly and symmetrically with Arthrocnemum at the Arthrocnemum-Salicornia border, and is a dominant competitor over Limonium and Frankenia in the middle (high Salicornia) zone. However, dodder significantly shifts the competitive balances. (b) Over time, Salicornia decreased and Arthrocnemum increased in plots infected with dodder. (c) Large patches of dodder suppress Salicornia and favor Limonium and Frankenia. (After Pennings & Callaway, 2002.)

Figure 12.14 The effect of dodder, Cascuta salina, on competition between Salicornia and other species in a southern Californian salt marsh. (a) A schematic representation of the main plants in the community in the upper and middle zones of the marsh and the interactions between them (solid lines: direct effects; dashed lines: indirect effects). Salicornia (the relatively low-growing plant in the figure) is most attacked by, and most affected by, dodder (which is not itself shown in the figure). When uninfected, Salicornia competes strongly and symmetrically with Arthrocnemum at the Arthrocnemum-Salicornia border, and is a dominant competitor over Limonium and Frankenia in the middle (high Salicornia) zone. However, dodder significantly shifts the competitive balances. (b) Over time, Salicornia decreased and Arthrocnemum increased in plots infected with dodder. (c) Large patches of dodder suppress Salicornia and favor Limonium and Frankenia. (After Pennings & Callaway, 2002.)

Figure 12.15 The number of buds produced by resistant and susceptible genotypes of two cultivars of lettuce, (a) and (b). Error bars are ±2 SE. (After Bergelson, 1994.)

a compensatory fashion - for example, loss to parasites may lead to a weakening of density-dependent mortality at a later stage in the life cycle. The effects of rare, devastating epidemics, whether in humans, other animals or plants, are easy to see; but for more typical, endemic parasites and pathogens, moving from the host-individual to the host-population level offers an immense challenge.

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