Are Humans Parasitic Or Free Living Animals Explain

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Front Ecol Environ. Author manuscript; bachelor in PMC 2017 Jan 9.

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A world without parasites: exploring the hidden ecology of infection

Chelsea L Wood

¹Section of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI

²Michigan Guild of Fellows, University of Michigan, Ann Arbor, MI

^threeDepartment of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO

Pieter TJ Johnson

³Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO

Abstruse

Parasites take historically been considered a scourge, deserving of annihilation. Although parasite eradications rank among humanity'due south greatest achievements, new enquiry is shedding light on the collateral furnishings of parasite loss. Here, we explore a "earth without parasites": a thought experiment for illuminating the ecological roles that parasites play in ecosystems. While there is robust evidence for the effects of parasites on host individuals (eg affecting host vital rates), this exercise highlights how little nosotros know about the influence of parasites on communities and ecosystems (eg altering energy flow through food webs). Nosotros present hypotheses for novel, interesting, and full general effects of parasites. These hypotheses are largely untested, and should exist considered a springboard for future inquiry. While many uncertainties exist, the available evidence suggests that a earth without parasites would be very different from the globe we know, with effects extending from host individuals to populations, communities, and fifty-fifty ecosystems.

What would happen if all parasites disappeared? This intriguing thought experiment, recently posed in BBC World'due south "Strange & Cute" series (Jones 2015), is a useful practice for considering the ecological roles of parasites in ecosystems. Then far, humanity has managed to bulldoze merely one of its parasites to extinction: Variola, the viral genus that causes smallpox (Panel ane). Until it was eradicated in 1980 through global-scale public health efforts, naturally occurring smallpox was i of the near ascendant drivers of bloodshed in recorded history, killing 500 million people in the 20th century alone (Koplow 2003). By many metrics, the emptying of viruses, bacteria, protozoa, and parasitic arthropods and worms (here, collectively referred to as "parasites") would contribute to reduced rates of man mortality, less disability, improvements in quality of life (Murray et al. 2012), and even reduced poverty (Bonds et al. 2010). The disappearance of parasites would also substantially benefit livestock production (Perry and Randolph 1999) and wildlife conservation (Daszak et al. 2000), especially in developing countries.

Panel i

Controlling, eliminating, and eradicating parasites

Humans have been attempting to manage the transmission of parasites for hundreds and mayhap thousands of years. For case, variolation – an early vaccination technique by which recipients were intentionally exposed to scabs, fluids, or article of clothing of smallpox patients, ordinarily those who had lived through a mild form of the disease – was good in Republic of india equally early as the 16th century (Plotkin and Plotkin 2008). Efforts to manage parasite manual accept met with varying levels of success. Studying the outcomes of such attempts may offer opportunities for understanding the ecological roles that parasites play in ecosystems.

Definitions

Here, we adopt the following terminology, after Dowdle (1999):

• – Eradication: worldwide incidence of infection is reduced to zilch

• – Elimination: incidence of infection is reduced to zero in a defined geographic area, simply manual continues in other parts of the world

• – Control: prevalence of a parasite is reduced to a level that is locally acceptable

Parasites of humans

Although humanity has succeeded in eradicating only one human parasite – the smallpox virus (Variola spp) – countless attempts to control other parasites accept been fabricated, some highly successful (Centre for Global Development 2004). International efforts to eradicate polio (Aylward and Tangermann 2011) and guinea worm (Al-Awadi et al. 2014) are nearing completion. Numerous other diseases – including lymphatic filariasis, onchocerciasis, Chagas disease, and leprosy – take been the focus of international efforts. These are considered by the World Health Organization (WHO) to exist potentially "eradicable" (Dowdle 1999), and for many of these diseases, elimination has been achieved in some regions (Center for Global Development 2004). Co-ordinate to the WHO, a central feature of "eradicable" diseases is their specificity to the human species; it would be much more than difficult to eradicate a parasite species that could "bide its time" in a reservoir host or as spores or eggs in the surroundings (Center for Global Evolution 2004).

Although strides have been made toward eradication, elimination, and command of many human parasites, there have also been many failures. Malaria – the affliction responsible for more deaths over the class of human history than whatever other (Garnham 1966) – has been intensively targeted for eradication since 1955, with merely local or regional progress toward elimination (Alonso et al. 2011), despite substantial investments ($630 million invested in malaria research and development funding in 2011 alone; Moran et al. 2013). These failures are largely due to the development of resistance to pesticides among mosquitoes and anti-malarial drugs among Plasmodium parasites (Alonso et al. 2011). The Schistosoma spp, causative agents of schistosomiasis, have proved similarly recalcitrant to control (Chitsulo et al. 2000). Despite many national-level control programs (Rollinson et al. 2013), schistosomiasis remains very prevalent – information technology currently infects near 240 million people, generally in sub-Saharan Africa (WHO 2013).

Parasites of non-human animals

Substantial efforts accept besides been invested in eradicating or eliminating the parasites of non-human animals, including domestic animals and wild fauna. To engagement, the only animal illness to be (purposefully) globally eradicated is rinderpest. When the success of this eradication endeavour was announced in 2011, it was simply the second intentional eradication to have been accomplished in human being history – subsequently smallpox (Roeder et al. 2013). Native to Central Asia, rinderpest was introduced into Africa in 1887 with Indian cattle (Scott 1998). The morbillivirus devastated populations of cattle, buffalo, antelope, giraffe, wildebeest, and warthogs throughout the African continent (Dobson et al. 2011). Long-term monitoring of wildlife in and around Serengeti National Park revealed the ecological outcomes of this eradication: in the absence of rinderpest-induced mortality, plant eater abundance increased several times over, triggering increases in the abundance of their predators (lions and hyenas), reductions in the frequency of fire (due to more efficient grazing and less unconsumed, flammable grass), a shift of grassland ecosystems to Acacia-dominated woodland and bush, and a shift of the Serengeti from a source of atmospheric carbon to a sink (Figure 1; Holdo et al. 2009; Dobson et al. 2011). These considerable ecological changes were among the start demonstrations of the of import role that parasites can play.

Although the example of rinderpest on the African continent is one familiar to ecologists, the disease was non native to Africa and its eradication was therefore akin to ecological restoration. Back in its indigenous Indian range, rinderpest's ecological function – and the ecological effects of its removal – were poorly documented. Bharat was alleged rinderpest-free in 2004 (Global Rinderpest Eradication Program 2011) and the last recorded instance of rinderpest in Southward Asia occurred in 2000 (Roeder et al. 2013). Eradication has undoubtedly benefited the subcontinent: the economic benefit–toll ratio for rinderpest eradication in India has been estimated at >60, primarily because livestock can now exist freely exported (Roeder et al. 2013). Prior to its eradication, the disease also affected wild mammals in the region, including threatened gaur (Bos gaurus; Ashokkumar et al. 2012) and Asiatic wild buffalo (Bubalus bubalis; Choudhury 1994). Whether any regional ecological impacts accept resulted is unknown.

An additional beast disease has been globally eradicated, although this came not every bit the result of a purposeful campaign, just equally an unintended consequence of conservation. In a final-ditch endeavor to rescue the California condor (Gymnogyps californianus) from extinction, the surviving few birds were removed from the wild into captivity and de-loused with pesticides. This deed eradicated the condor louse (Colpocephalum californici), a species that has been found on no other bird host and is presumed to be extinct (Dunn 2009), although its host has since rebounded. Whether there have been whatsoever ecological impacts of the louse's extinction is as well unknown.

Why consider the ecological outcomes of parasite eradication?

Eradication efforts – which tin can be plush – usually target only those parasites of major public health, economic, or conservation business concern (Stringer and Linklater 2014). Each successful eradication effort outlined above was an unmitigated triumph for humankind – in our opinion, no ecological argument tin overshadow the benefit of, for example, ridding humanity of the scourge of smallpox. However, nosotros believe it is worth considering the ecological functions that are lost when parasites are eliminated from an ecosystem, specially parasites of ecologically influential wild fauna species. Here, we identify several priority research areas:

1. Identify opportunities to experimentally assess the ecological function of parasites: Exclusion experiments – those in which a taxon is excluded from an area and ecological effects of this exclusion are quantified – have driven tremendous progress in environmental (Lubchenco and Real 1991). Parasite eliminations tin can serve as "natural experiments" that reveal the functional roles of parasites in ecosystems, providing disquisitional data that would otherwise be difficult to obtain. Indeed, some of the most informative studies of parasites' ecological roles to appointment have used control programs as "natural experiments" (eg Holdo et al. 2009) or have experimentally manipulated the presence of parasites (eg Hudson et al. 1998).

2. Conceptualize unintended consequences of parasite eradication: Collateral ecological impacts can arise from the eradication or elimination of an brute parasite. For example, the eradication of rinderpest and subsequent abeyance of vaccination may have led to contempo upticks in the prevalence of another ungulate morbillivirus in Africa, peste des petits ruminants (Libeau et al. 2011). The potential for such unintended consequences should exist assessed in a risk-do good assay earlier attempts at parasite command are made (Stringer and Linklater 2014).

3. Identify opportunities to reap economic and conservation benefit from parasite eradication: Conversely, parasite eradication or elimination may have important economic and conservation benefits. An accurate assessment of potential benefits is also a key component of gamble–benefit analyses (Stringer and Linklater 2014).

Just while the eradication of affliction agents is critically important for ensuring homo well-beingness, parasites often play important notwithstanding underappreciated roles in nature. Every ecosystem on Earth contains parasites; indeed, virtually every metazoan hosts at to the lowest degree one parasite species (Poulin and Morand 2000). Parasites represent ∼40% of described species (Dobson et al. 2008) and are at least twice as rich in species every bit their vertebrate hosts (Poulin and Morand 2004). Considering but viruses in the sea, a projected ∼4 × 10³⁰ species be, with the continuing stock of carbon in viral biomass estimated at ∼200 megatons (Suttle 2005). Despite this ubiquity and abundance, the diversity of parasites is poorly known (Poulin and Morand 2000) and our understanding of parasites' ecological influence remains rudimentary (Gomez et al. 2012; Hatcher et al. 2012).

Hither, we explore a "earth without parasites" every bit a vehicle for identifying the ecological changes that accompany the elimination or loss of infectious organisms. The elimination of all parasites is improbable and perhaps impossible, only as Holt (2010) noted, "it can exist illuminating to ponder all kinds of implausible and radical scenarios, in effect bracketing the real world with visions of possible worlds". We limit our give-and-take to parasites of animals, focusing on empirical and theoretical inquiry on parasites' influence at several levels of ecological organization (private, population, community, and ecosystem), posing hypotheses for general mechanisms by which parasites may be ecologically influential, and identifying attributes of parasites, hosts, and ecosystems that may predict a strong ecological influence of parasites (Panel ii, run across p 433–434). We focus on ecological effects of parasites, simply evolutionary effects are besides likely to be important (Holt 2010; Stringer and Linklater 2014). We emphasize those cases where parasites' effects are likely to be consistent across contexts, excluding impacts of parasites that are probable to exist highly context-specific. The studies reviewed below propose that the influence of parasites, though ofttimes subconscious, can be substantial.

Panel 2

Hypotheses for general roles of parasites in ecosystems

Here, we nowadays some full general, novel, and interesting hypotheses regarding the roles of parasites in ecosystems. These accost broad questions: which ecological processes are about likely to change equally the result of parasite removal? Under what conditions will parasite effects exist strongest? Which parasite effects might be general across ecosystems? For each hypothesis, nosotros sketch a brief caption or example, and define conditions nether which nosotros expect the hypothesis might concord. These hypotheses await testing.

Individual level

Elimination of i parasite species might atomic number 82 to increased abundance of other parasite species

Explanation

Well-nigh complimentary-living organisms – including humans – host numerous species of symbionts, including viruses, bacteria, fungi, worms, and arthropods. These symbionts tin can interact with ane another directly (eg through predation or interference competition) or indirectly (eg via immunity-mediated credible contest; Stringer and Linklater 2014). Non all of the symbionts that alive on and in humans are parasitic, but even those that are may still confer a internet benefit if they deter other, more deleterious pathogens (Costello et al. 2012).

Example

Anti-helminthic treatment increases hazard of Giardia infection in humans, and anti-protozoal handling increases the risk of hookworm infection – probably the issue of competitive inhibition (competition between parasites) or cross-immunity (susceptibility of 1 parasite to the immune response provoked past the other) between worms and protozoans (Martin et al. 2013).

Weather

• When there are parasites in the system that are ecologically similar to the parasite targeted for eradication (and therefore probable to engage in intra-host competition)

• When there are parasites in the organisation that are closely related to the parasite targeted for eradication (and are therefore likely to exist affected by the same component of host immunity), but are unaffected past the eradication effort (eg Libeau et al. 2011)

• When parasite interactions (directly or indirect) are an important determinant of parasite community composition (ie when intra-host interactions matter), as may exist true for highly abundant parasites, those with stiff cross-reactive immunity, or when priority furnishings are potent

Removal of one parasite species might lead to reduced affluence of another parasite species

Case

Infection with the parasitic worms that cause man urinary schistosomiasis (Schistosoma haematobium) increases the risk of contracting HIV for women in sub-Saharan Africa (Rollinson 2009). Emptying of schistosomiasis through distribution of anti-helminthic drugs has been suggested as an approach for controlling the African HIV epidemic (Hotez et al. 2009).

Atmospheric condition

• When the parasite removed depresses the efficacy of host immune defenses

• When the parasites in question are less likely to compete (eg are ecologically or phylogenetically distinct) or trigger different branches of the host's allowed defenses (eg Ezenwa et al. 2010)

• When host immune function is an important regulator of parasite abundance or manual potential

Population level

Removal of "keystone" parasite species or groups will influence host populations

Explanation

"Keystone" species have stiff trophic links to many other species, and extirpating them can take important effects on food webs. Bully theoretical progress has been made in predicting the event of a species' extinction. This work demonstrates that – for free-living taxa – outcomes of extinction are variable from species to species, with many weak interactors and a few "keystone" species (Wootton and Emmerson 2005). Do parasites follow the same pattern? If so, can we predict which parasitic species are likely to be "keystones"?

Example

In some common salt marsh ecosystems of western Due north America, trematode biomass exceeds that of whatsoever other parasite group (Kuris et al. 2008). Continuing trematode biomass and trematode production of infective stages (cercariae) each exceed the biomass of top predators (Kuris et al. 2008). Therefore, the influence of trematodes on free energy flow in these ecosystems is probably substantial.

Conditions

Ecologically influential ("keystone") parasites should tend to be:

• Those that infect ecologically influential ("keystone") hosts

• Those that commandeer a substantial proportion of host biomass (eg parasitic castrators, Kuris et al. 2008; behavior manipulators, Sato et al. 2011)

• Those that tin behaviorally manipulate their hosts, considering these parasites might affect energy flow by strengthening predator–casualty links (eg trophically transmitted trematode metacercariae in killifish; Lafferty and Morris 1996) or causing the host to move into a novel habitat (eg nematomorphs that induce "water bulldoze" in cricket hosts; Sato et al. 2011)

Removal of a parasite species might lead to loss of regulation of the host population

Example

Hudson et al. (1998) administered anti-helminthic drugs to red grouse and observed a dampening of the population's boom-and-bust cycles.

Conditions

• When parasites are highly host-specific

• When parasites are pathogenic

• When ecosystems are stable and where abiotic factors (eg drought, desiccation, fire, wave activity) do non limit host populations

• When hosts are high trophic-level species, and the likelihood of control by predators is therefore lower

Community level

Removal of a parasite species may change community composition

Examples

Parasites have variable effects on communities: for instance, they can either increase (eg Thomas et al. 1995; Mouritsen and Poulin 2005) or decrease (eg Tompkins et al. 2003) coexistence and customs-level species diversity.

Atmospheric condition

While there may be few full general means in which parasites change community composition, we predict that the weather condition that favor a strong effect of parasites on community composition include:

• When hosts are abundant and/or ecologically influential

• When hosts vary in their tolerance to parasitic infection

• When parasites are highly host-specific, and the magnitude of parasite impacts is therefore highly divergent amongst species in the gratis-living assemblage

• When parasites are highly pathogenic

• When ecosystems are stable and where abiotic factors (eg drought, desiccation, fire, wave action) practise not limit host populations

• When the host community is strongly influenced by interspecific interactions rather than other forces (eg dispersal, stochastic effects)

Removal of a parasite species may change a community'south invasibility

The removal of parasites might make communities more difficult to invade (because release from parasitic enemies puts natives and invasives on "equal footing" or removes the "biological weapons" that might otherwise facilitate invasion) or easier to invade (because removal of parasites removes the "biotic resistance" of native communities).

Possible tests

• Experimentally assembled parasite-rich and parasite-costless communities

• Comparison the number or proportion of invasive species beyond habitats that naturally vary in the number of parasites they back up

• Experimentally manipulating the number of parasite species or individuals (eg using anti-helminthic drugs) in a habitat experiencing an ongoing or progressive invasion

• Identifying the cause of failure in intentional introductions

Removal of parasite species that regulate populations may increase predation rates

Explanation

Parasites drain the resource of their hosts. In the absence of parasites, this energy tin be exploited past other natural enemies, including predators.

Example

Before its eradication, rinderpest devastated populations of cattle, buffalo, antelope, giraffe, wildebeest, and warthogs throughout the African continent (Dobson et al. 2011). Afterward Africa became rinderpest-free, the abundance of lions and hyenas increased, probably due to increased availability of prey (Figure one; Holdo et al. 2009; Dobson et al. 2011).

Conditions

• When parasites strongly regulate the host/prey species and removal of parasites releases this regulation

• When the host/prey species is abundant and ecologically influential

Removal of manipulative parasite species may reduce predation rates

Explanation

Manipulations of host behavior or morphology that increase susceptibility of an intermediate host to a downstream host are amidst the near common manipulations known and – in many cases – the behavioral manipulation is accompanied by an increase in the lipid and glycogen content of the intermediate host (Lefevre et al. 2009). By making prey easier to grab and more valuable as food resources, manipulative parasites may functionally increase predation rates and, by extension, the corporeality of resources accessible to predators.

Conditions

• When manipulation drives a large modify from host'south uninfected state

• When parasites are arable and manipulation is common amid casualty individuals

• When the host is abundant or ecologically influential

Ecosystem level

Removal of regulating parasite species may increase flow of energy to higher trophic levels

Caption

Parasites drain the resources of their hosts. In the absence of parasites, this energy can exist exploited past other natural enemies, including predators, with additional downstream effects on energy flow.

Conditions

• When parasites strongly regulate the host/prey populations and removal of parasites releases this regulation

• When the host/casualty species is abundant and ecologically influential

Removal of manipulative parasite species may reduce catamenia of energy to higher trophic levels

Explanation

We hypothesize that manipulative parasites are responsible for subsidizing populations of predators, shunting free energy that would otherwise fail to period to college trophic levels; this is accomplished through host behavioral manipulation to improve the odds of trophic transmission. If the loss of predator fitness due to parasitic infection does not outweigh this gain, this could correspond a subsidy that lifts resources constraints on predators (Lafferty et al. 2000). Therefore, a globe without manipulative parasites may besides be a world with fewer predators (Figure 3). Given the commonness of behavioral manipulations that facilitate trophic transmission, this could be a general result beyond ecosystems.

Weather condition

• When manipulation drives a large alter from host'southward uninfected state

• When parasites are abundant and manipulation is common among prey individuals

• When host is abundant or ecologically influential

• When parasite has high biomass / secondary product

Removal of a parasite species may alter across-ecosystem subsidies

Explanation

Some parasites induce their hosts to movement from habitat preferred past the host to habitat suitable for the parasite (eg Hanelt et al. 2005), increasing the exchange of energy and materials (in the form of host and parasite biomass) beyond ecosystems. Others may reduce host movement by sapping host resource, by suppressing overall activity levels, or by reducing the affluence of a host that otherwise might traverse ecosystem boundaries (eg Dobson et al. 2011). Is there any consistency in the result of parasites on beyond-ecosystem processes? We anticipate that these will be extremely context-dependent effects.

Meet Web References for all references in Panel 2

Individuals and populations

The fitness effects of parasites on host individuals, although negative past definition (Combes 2001), vary strongly among species. A parasite may reduce its host's growth, prevent it from reproducing, or change its behavior. Parasites may even accept positive collateral furnishings on a host (eg past competing with other, more virulent parasites inside the same host [Panel two, see p 433–434]). When individual-level effects accrue, parasites may also influence host populations in a variety of means.

Parasites influence host immunity

A growing body of inquiry illustrates the ecological importance of within-host interactions among parasites, too as interactions between parasites and the host'south immune organisation. Although co-infections would exist impossible in a world without parasites, nosotros address interactions amongst co-infecting parasites in Console 2 (see p 433–434). Fifty-fifty without co-infecting species, the absence of parasites can drive unexpected outcomes in host wellness, through effects on host allowed role. Some chronic illnesses of humans – including allergies and autoimmune diseases – take been linked to a lack of exposure to parasites, particularly worms (the "hygiene hypothesis"; Okada et al. 2010). Paradoxically, parasites may have net positive fitness benefits for hosts if the immunologic upshot of parasite absence takes a sufficiently high toll on host fitness (Holt 2010; Stringer and Linklater 2014). In the absence of parasites, hosts should shed costly – and useless – allowed defenses. But nature abhors a vacuum. Hosts that initially lost their immunity would later be susceptible to re-infection by newly evolved parasites (Stringer and Linklater 2014; Jones 2015).

Parasites affect the dynamics of host populations

Many parasites affect the charge per unit of host population growth and total population size. Indeed, at that place are numerous examples demonstrating regulation of wild host populations past parasites, including both "micro-parasites" and "macro-parasites", whose fitness furnishings on hosts are independent and dependent, respectively, on the number of initial infecting transmissive stages (Lafferty and Kuris 2002). For example, crustacean parasites such as isopods and copepods (Effigy ii) can reduce growth, reproduction, and survivorship of coral reef fishes, resulting in population-level regulation of hosts (Forrester and Finley 2006). In British heathland ecosystems, experimental application of anti-helminthic drugs (which clear blood-red grouse of infections with the parasitic nematode Trichostrongylus tenuis) dampened the boom-and-bust cycles that characterize the population dynamics of infected bickering (Hudson et al. 1998). Merely parasites need non kill their hosts to exert regulatory effects on host populations; many parasites desexualize their hosts (eg the bacterium Pasteuria ramosa in Daphnia spp; Ebert et al. 2004), thereby regulating host populations (Decaestecker et al. 2005). Removal of such influential parasites may pb to loss of regulation of host populations and an increase in host affluence (Panel two, meet p 433–434).

An isopod parasite (Anilocra laticaudata) fastened to the cheek of its fish host, a coney (Cephalopholis fulva), in the Commonwealth of the bahamas

Communities

Parasites modify the composition of ecological communities

The effects of parasites vary among host species, and this can lead to customs-level furnishings (Console 2, see p 433–434). Many examples, most accumulated over the past several years, demonstrate that parasites can alter the limerick of communities through demographic (density-mediated) or morphological/physiological/behavioral (trait-mediated) indirect furnishings. Because these effects have been reviewed elsewhere (eg Gomez et al. 2012; Hatcher et al. 2012), we give only a few illustrative examples here. In a classic case of a density-mediated indirect issue of parasites and of parasite-mediated apparent competition (an interaction that looks like competition betwixt two species simply is really acquired past a third factor; Stringer and Linklater 2014), the invasive grey squirrel (Sciurus carolinensis) was able to supersede the native red squirrel (Sciurus vulgaris) throughout the U.k. considering the invader brought with it a parapoxvirus. Only the native scarlet squirrel experienced substantial parasite-induced mortality, assuasive gray squirrels to expand into the niche vacated by the natives (Tompkins et al. 2003). Parasites may too have trait-mediated indirect effects. In the rocky intertidal zone of New England, periwinkle snails (Littorina littorea) infected with a trematode parasite eat less algae than practise uninfected snails, probably due to infection-related changes in the digestive system; every bit a result, edible macroalgal species are more than abundant in the presence of infected snails than in the presence of uninfected snails, with implications for the other intertidal species that apply this macroalgae as habitat and nutrient (Forest et al. 2007). Finally, parasites may affect interactions among gratuitous-living species (Holt 2010; Mordecai 2011; Stringer and Linklater 2014); for example, the presence of larval trematodes increases intertidal diversity on New Zealand mud flats past irresolute interactions between host bivalves and the organisms that depend on bivalve shells for habitat (Mouritsen and Poulin 2005). Whether by effects on host density or traits, or on species interactions among hosts, the composition of free-living communities can exist radically reshaped by parasites.

In addition to affecting the composition of communities, parasites may also affect variability in composition (ie food web stability), but whether the presence of parasites generally increases or decreases such variability is controversial and may be context-dependent (Lafferty et al. 2008; McQuaid and Britton 2015). Parasites could increment stability in community composition past regulating host populations (Anderson and May 1978), contributing "weak links in long loops" (Neutel et al. 2002), or by producing credible competition (Dobson 2004). Alternatively, parasites could decrease stability by increasing the length of nutrient chains (Williams and Martinez 2004), overwhelming stable predator–prey links with unstable parasite–host links (Otto et al. 2007), or merely by contributing additional species to total community richness (Chen et al. 2011). While the presence of parasites is by and large thought to decrease the robustness of nutrient webs (ie the likelihood of secondary extinctions occurring after a primary species loss), this is primarily because parasites themselves are decumbent to secondary extinctions (Chen et al. 2011; McQuaid and Britton 2015). Whether there is a general role for parasites as a stabilizing forcefulness in free-living food webs remains an open question.

As suggested in the example of grayness squirrels, parasites may mediate the ability of not-native species to invade a community (Tompkins et al. 2003). According to the "enemy release hypothesis", when a species is introduced into a region to which it is non native, it experiences weaker population regulation by natural enemies (eg parasites, predators) than it would in its native range (Prenter et al. 2004). Indeed, host species of various taxa are infected by twice as many parasites in their native ranges than in their invaded ranges (Torchin et al. 2003). If parasites disappeared, native and invasive species might be placed on equal ground – that is, release from parasitic enemies would benefit both native and invasive species. Alternatively, if the parasites of invasive hosts facilitate invasion by infecting native hosts (the "biological weapons hypothesis", as in the example of the grey squirrel; Tompkins et al. 2003), parasite loss might effect in a disadvantage to invasive species and reduced rates of invasion. Native parasites also have the potential to tiresome the progress of invaders (the "biotic resistance hypothesis"; Torchin et al. 2002; Panel ii, see p 433–434); for instance, European settlers were repelled from large swaths of state in southern and key Africa by trypanosomiasis, so that patterns of early European settlement mostly matched areas that were trypanosomiasis-free (Ford 1971; Beinart and Coates 1995). Thus, whether the loss of parasites will increase or decrease invasibility of an ecosystem ultimately depends on the relative fitness effects of invasive parasites on native and invasive hosts, the propensity of native parasites to infect invasive hosts, and other factors.

Parasites alter trophic interactions and predation rates

In a world without parasites, energy should become bachelor to complimentary-living consumers that would otherwise take been siphoned away by parasitic consumers (Holt 2010; Jones 2015); this follows from the expectation that the loss of parasites should ameliorate individual-level fettle effects associated with parasitism (eg brand prey larger) and release some gratuitous-living species from regulation (eg make prey more numerous). But parasites can besides influence host individuals through sublethal furnishings, which affect their quality and availability equally prey (Holt 2010). Whether elimination of a parasite species will increase or decrease free energy period to consumers/predators will therefore depend on the balance between the regulatory and individual-level effects of the parasite.

We suggest that the power of parasites to manipulate host behavior facilitates a substantial corporeality of energy menstruation from lower to upper trophic levels (Figure 3; Console ii, encounter p 433–434; Hadeler and Freedman 1989; Kuris et al. 2008). Host manipulation is a mutual strategy by which parasites alter their host'southward phenotype to increment their ain fitness, usually by inducing or exaggerating host traits that favor parasite transmission or dispersal (Dobson 1988; Poulin 2010). Adaptations for host manipulation have been documented in hundreds of parasite species beyond the tree of life – including platy-helminths, acanthocephalans, nematodes, nematomorphs, arthropods, protozoa, fungi, bacteria, and viruses (Hughes et al. 2012) – and have evolved at least xx divide times (Poulin 2010). Some manipulations increase the likelihood of parasite manual from prey to predator (trophic manual) by inducing changes in the prey host's phenotype that make it more susceptible to predation (Figure three). Other parasites induce behaviors that facilitate transmission among conspecifics; for instance, in infected vertebrates, rabies can increase assailment, promoting transmission of the virus via bite wounds (Klein 2003). Parasites may also cause their hosts to move from habitat preferred past the host to habitat suitable for the parasite as, for example, in nematomorph parasites that induce a "water drive" in their cricket hosts, causing the crickets to drown themselves in streams, where the nematomorph emerges to complete its aquatic life phase (Figure 4; Hanelt et al. 2005). Our understanding of the ecological effects of manipulation is notwithstanding limited (Weinersmith and Faulkes 2014), possibly because manipulations are diverse and tin have varying, context-dependent ecological effects. The net influence of parasite loss on consumer populations will depend on the balance betwixt loss of regulation on prey populations versus loss of manipulated prey individuals; but because many taxa in many ecosystems engage in host manipulation for trophic transmission, nosotros predict that a world without parasites could exist a globe with fewer predators (Panel 2, run into p 433–434).

In many second intermediate hosts (hosts of the second larval stage) of trematode parasites – like the California killifish (Fundulus parvipinnis) – the parasite induces behavioral changes to facilitate transmission to the concluding host (in this example, bird predators). (a) In the absenteeism of parasites, fish display evasive and camouflaging beliefs that minimizes the likelihood of bird predation. (b) When trematode metacercariae (larval phase) infect killifish, the fish perform behaviors that make them conspicuous to bird predators, effectively increasing the availability of fish resource to birds (Lafferty and Morris 1996). In this manner, parasites may provide a "subsidy" to predators. Such behavioral manipulations are common across the diverseness of parasite life.

Many parasites are capable of manipulating the beliefs of their hosts. Nematomorphs (also sometimes called Gordian or horsehair worms) induce a "water drive" in their cricket host, causing the host to drown itself in puddles, ponds, or streams, where the parasite can wriggle free and go on with the aquatic stage of its life cycle. In this way, nematomorphs drive across-ecosystem subsidies that have strong effects on the recipient ecosystem (Sato et al. 2011).

Ecosystems

Parasites alter the cycling of energy and nutrients

The means in which parasites affect the cycling of free energy and nutrients are only beginning to receive enquiry attention (Preston et al. in review), but because parasites can represent a big proportion of full biomass in some ecosystems (Kuris et al. 2008; Preston et al. 2013) and tin straight modify rates of host nutrient excretion (eg Bernot 2013), their influence on such cycles could exist substantial. Beliefs-manipulating parasites, in particular, may take strong effects on these cycles; we discussed above the influence of manipulation on the abundance of predatory species (which tin can exist thought of as the "nodes", architecture, or topology of a food web), but parasites tin likewise affect the movement of free energy and nutrients through food webs (Kuris et al. 2008). For instance, by inducing behaviors in intermediate hosts that increase their susceptibility to predation, parasites may intensify trophic interactions and strengthen predator–prey linkages (see above; Lefevre et al. 2009). Parasites may likewise alter the rates of other of import ecosystem processes, such equally grazing (eg rinderpest; Panel one; Sinclair et al. 2008), decomposition (eg nematomorphs; Sato et al. 2011), and bioturbation (eg trematodes; Mouritsen and Haun 2008), as well every bit carbon sequestration and cycling of other nutrients (eg marine viruses; Panel ii, see p 433–434; Danovaro et al. 2011). Whether energy flow to upper trophic levels is strengthened or weakened past parasite removal will depend on the relative influence of manipulative versus host-population regulating parasites.

Parasites alter beyond-ecosystem subsidies

In many cases, parasites' manipulation of their hosts to move from habitat preferred by the host to habitat suitable for the parasite can result in a transfer of energy and nutrients from one ecosystem to another. To demonstrate this effect, Sato et al. (2011) showed that parasite-driven energy subsidies from terrestrial ecosystems in Nihon (where crickets were experimentally added to stream reaches at rates equivalent to the rate at which nematomorph-infected crickets enter stream habitats) are sufficient to set off a trophic cascade. In this cascade, fish predators switch to feeding on crickets, releasing their usual prey – benthic invertebrates – from predation pressure, and thereby decreasing biomass of benthic algae and increasing the leaf breakdown charge per unit. Thus, in the absence of parasites, we may observe weakening of across-ecosystem subsidies (eg nematomorph-infected crickets will no longer cross the boundary between terrestrial and aquatic ecosystems), but the extent of the contribution of manipulation or other parasite-mediated processes to across-ecosystem subsidies remains unknown.

Conclusions

A globe without parasites is impossible to achieve, and tin can be approximated only in specific circumstances (eg zoo enclosures, aquaria, and intensive agronomics), which – despite strenuous try – are ofttimes even so hotbeds of infection (eg hospitals). Even if parasites did somehow all disappear, other species would evolve to occupy the newly vacant niches (Lloyd-Smith 2013). Despite its improbability, imagining such a world tin can assistance expose the otherwise subconscious ecological roles of parasites. These roles are hidden considering the ecosystem of a parasite (ie inside the host) is oft nested inside the ecosystems that ecologists are accepted to considering (eg forests, grasslands, coral reefs). A better agreement of how parasites contribute to the communities and ecosystems in which they are embedded is a critical need as we consider how to make the world "less wormy" (Loker 2013).

The hypotheses outlined here (Panel 2, see p 433–434) posit several general furnishings of parasites on ecosystems, including on host community structure and energy flow. Parasites may be small and inconspicuous relative to their hosts, but information nerveless so far suggest that they are far from unimportant. Nosotros must begin to consider their influence within ecosystems, particularly when planning disease management interventions or conservation efforts.

In that location are some cases in which emptying of a parasite species is both possible and highly desirable. In these instances, potential benefits to human health and well-existence trump any other considerations. However, many of the contemporary illness challenges faced by society and imperiled wildlife involve more than complex bondage of manual – oft including multiple host species, multiple parasite species, reservoirs, or resilient environmental resting stages. As a result, eradication will oftentimes exist impossible, and "ecological surprises" associated with control efforts will probably announced with greater frequency. For instance, without an appreciation for the antagonistic relationship betwixt worms and protozoa living in the homo intestine (Panel 2, see p 433–434; Martin et al. 2013), a well-intentioned de-worming campaign could make people very sick. We do not debate that human parasites should exist conserved, merely rather we urge the importance of understanding the ecology of a parasite before attempting to control it. As Jones (2015) wrote, "Surprisingly, a world without parasites might not be a nicer one". Thoughtful planning will prevent the loss of ecologically important parasites and the processes they facilitate, as we progress slowly toward a parasite-free world.

​

African wildebeest (Connochaetes taurinus) were decimated by rinderpest in an 1889 outbreak and remained at low abundance for decades. When rinderpest eradication efforts were initiated in the 1960s, wildebeest affluence increased dramatically (a). Because wildebeest grazing reduces biomass of flammable grasses, thereby reducing burn down frequency and increasing woody institute abundance, the return of wildebeest increased the abundance of trees (b), increasing savanna carbon sequestration (c). These changes accept been very evident in the Serengeti ([d] through [g]). In (a), circles bespeak wildebeest population size, whereas squares and triangles indicate prevalence of rinderpest before and later eradication, respectively. In (b), solid and dashed lines indicate direct and indirect effects, respectively; the plus and minus signs signal direction of effects. In (c), columns bear witness means with 95% confidence intervals (fault bars). Panels (a) through (c) were adapted from Dobson et al. (2011), adapted from Holdo et al. (2009).

In a nutshell

• Since artifact, humans have tried to eliminate their ain parasites and those of their domesticated animals; what would happen if they succeeded?

• We explore the ecology of a "world without parasites" every bit a style to understand the roles of parasites in ecosystems

• What functions would be lost in a globe without parasites? Might there be unexpected ecological or epidemiological outcomes?

• This exercise highlights major noesis gaps about the ecological roles of parasites

• We shut by presenting hypotheses for novel, interesting, and general effects of parasites, positing that a world without parasites might be one with very different free-living communities

Acknowledgments

D Preston provided insights and suggestions that contributed to the development of ideas in this manuscript. Nosotros acknowledge support from NSF (DEB-1149308), NIH (R01GM109499), and the David and Lucile Packard Foundation.

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