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Proceedings of the NationalAcademy of Sciences, India Section B:Biological Sciences ISSN 0369-8211 Proc. Natl. Acad. Sci., India, Sect. B Biol.Sci.DOI 10.1007/s40011-013-0241-3

Parasite with Multiple Roles: Are TheyReally Beneficial?

U. R. Zargar, M. Z. Chishti & MudasirA. Tantray

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REVIEW

Parasite with Multiple Roles: Are They Really Beneficial?

U. R. Zargar • M. Z. Chishti • Mudasir A. Tantray

Received: 20 February 2013 / Revised: 2 July 2013 / Accepted: 19 August 2013

� The National Academy of Sciences, India 2013

Abstract Parasites represent a major portion of biologi-

cal diversity of earth because they show high diversity and

abundance. They play an important role in ecological

functioning as they form important links in food web,

which are vital for regulation of host abundance and toxic

pollutants. However, it is also a fact that parasites are

detrimental for living organisms. In recent years, the

importance of parasites has been acknowledged thanks to

ecologists who are searching for new and potential envi-

ronment service providers. Parasites can be useful in a

number of ways which include assessment of environ-

mental health, disease therapy, understanding biodiversity

and ecological principles, etc. The present review critically

highlights the important roles of parasites, envisages the

speciality of parasites in an ecosystem and also examines

the potential of different parasitic species acting as positive

agents. This review will entice more studies on different

aspects of parasites so that major roles of parasites are clear

in future. However, caution is to be taken while consider-

ing a particular parasite for a positive role because positive

potentialities differ from parasite to parasite depending on

the nature and position of these tiny creatures in an

ecosystem.

Keywords Biological diversity � Parasites �Ecological principles �Environment service providers (ESP) � Disease therapy �Positive role

Introduction

Parasites previously considered as infection agents, have

now been considered useful in different aspects thanks to

researchers involved in ecological studies of parasites. For

a layman it is awkward to say that parasites are useful

because word Parasite itself means deleterious organism,

but for an ecologist Parasite is an essential part of an

ecosystem. Past attitude towards parasites was due to the

fact that parasites possess low biomass and were thus

considered unimportant in ecological terms [1]. However,

with the advancement in parasite ecology, more informa-

tion is now available on different aspects of parasites.

Ecologists have predicted different hypothesis with

regards to diversity and ecosystem functioning. Although,

there had been various studies in the past to find the rela-

tionship between parasite diversity and ecosystem func-

tioning, but till date there is an ambiguity about this

relationship [2–5]. It has been stated that &75 % links in

food webs involve parasitic species and these links are vital

for host regulation and for maintenance of ecological bal-

ance [6] thus it is felt that these tiny creatures are vital sign

of health of aquatic ecosystems [7–9].

In this review article, important roles of parasites are

discussed which they play at different levels. The aim is to

acquaint researchers about the beneficial aspects of para-

sites which were previously neglected due to dearth of

information. This article is against the general perception

about parasite i.e. they are only infecting agents.

U. R. Zargar (&) � M. Z. Chishti

Centre of Research for Development (CORD), University of

Kashmir (NAAC Accredited Grade ‘A’ University),

Srinagar 190 006, Kashmir, India

e-mail: uzssummer2@gmail.com

M. A. Tantray

Coy Waller Laboratory, National Centre for Natural Products

Research, School of Pharmacy, University of Mississippi,

Oxford, MS 38677, USA

e-mail: mudaek@gmail.com

123

Proc. Natl. Acad. Sci., India, Sect. B Biol. Sci.

DOI 10.1007/s40011-013-0241-3

Author's personal copy

Parasites can be Used in Solving Health Related Issues

Parasites have catched the media attention in past for their

possible role in disease cure. On 26th May, 2006, there was

an interesting article on Medical News Today (MNT) [10]

entitled Parasitic Worms Used To Fight Bowel Disease

focused on the role of parasites in treating inflammatory

bowel disease (IBD) in humans. The concept of parasite

therapy stems from the hygiene hypothesis according to

which early exposure to infections is necessary in order to

develop full immunity [10]. It has been further stated that

increased occurrence of allergic and autoimmune diseases

in advanced countries is due to absence/exposure of hel-

minth infections [11–13]. However, there are also counter

arguments which state that there is negative relationship

between helminth occurrence and allergic reactions [14].

There have been various clinical studies where

researchers have found medicinal value of helminths

(Table 1) [15–28].

Reddy and Fried [19], for example, reviewed the use of

helminths to treat Crohn’s and other autoimmune diseases.

Various issues are discussed in this review like the use of

Necator americanus larvae to treat autoimmune and other

related diseases. Recent clinical trials have shown great

promise for using live helminths as a novel alternative for

curing wide range of allergies and other autoimmune dis-

eases [29]. This has further opened new areas in immu-

nology and could lead to unravel hidden enigmas [29].

However, ambiguity still prevails regarding the proper

mechanism of helminth immunity paradigm. Two theories

have been used to explain the mechanism of helminths to

cure the autoimmune diseases and allergies. The classical

helminth immunity paradigm underpins the role of Th2

responses and induction of regulatory cells, whilst

emerging new helminth immune regulation paradigm

stresses key roles for the resident epithelia and innate cells

[29]. Researchers also believe that helminths can be useful

for curing different inflammatory reactions (allergies) [30].

Published data from previous decade show that more

clinical trials on helminths have been carried out on

experimental model animals (EMA) in comparison to

humans (Figs. 1, 2). More studies have been carried out on

IBD (five diseases) in humans, whilst more efforts have

been made on Allergy and IBD in case of EMA. All these

studies have shown promising results and can become a

base for disease therapies in future though it may take a

while from now. It is also clear from the published data that

more number of studies and species have been worked out

in case of EMA. Furthermore, IBD has been used both in

EMA’s and humans (Fig. 3). This analysis further envis-

ages the importance of helminths in disease therapies.

Morphological features of parasites which were previ-

ously considered worth for resolution of taxonomic status

are now showing extraordinary roles. The hooks in

Table 1 Medicinal value of different parasite groups/parasite species

Parasite group/species Can be helpful against References

Helminth Allergy [15, 16]

Intestinal worms Allergy [17]

Helminth Autoimmunity [18]

Helminth Inflammatory bowel disease [19]

Helminth Malaria antigens [20]

Helminth Epilepsy and poliomyelitis [21]

Pomphorhynchus spp. Surgical wounds [22]

Trichuris suisa Multiple sclerosis [23]

T. suisa Inflammatory bowel disease [24]

Trichuris trichiuraa Inflammatory bowel disease [25]

T. suisa Allergic rhinitis [26]

Necator americanusa Allergic rhinitis [27]

N. americanusa Celiac disease [28]

a Adapted from Khan and Fallon [29]

0

1

2

3

4

5

6

MS IBD AR CD

Num

ber

of s

tudi

es

Fig. 1 Helminth therapy against human diseases (study years:

1994–2011). More studies have been carried on IBD. Figure is shaped

on the basis of Khan and Fallon [29]. MS multiple sclerosis, IBD

inflammatory bowel disease, AR allergic rhinitis, CD Crohn’s disease

0

1

2

3

4

5

6

7

EAE T1 D RA Allergy IBD Obesity

Num

ber

of s

tudi

es

Fig. 2 Helminth therapy in experimental model animals (study years:

2002–2011). More studies have been carried on IBD and allergy.

Figure is shaped on the basis of Khan and Fallon [29]. EAE

experimental autoimmune encephalomyelitis, T1 D type 1 diabetes,

RA rheumatoid arthritis, IBD inflammatory bowel disease

U. R. Zargar et al.

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Acanthocephala, considered as an insertion organs as they

allow Pomphorhynchus spp. to get firmly attached to the

host gut without too much damage to the host tissue, have

inspired medical researchers to built super-grip plaster for

surgical wounds [22]. This recent innovation i.e. a bio-

inspired swellable micro needle adhesive for mechanical

interlocking with tissue, is an efficient and durable way to

heal up the surgical wounds.

How Important are Parasites in Understanding

Biodiversity and Ecological Principles?

At this time people are concerned about the changed trend

in biodiversity due to habitat alteration and global warm-

ing. The more concern is about the extinction of species

which is going at a faster pace. Under such circumstances

there is a need to recognize the role of parasites by non-

parasitologists so that there is a joint consensus to look into

ways by which parasites drive the biodiversity pattern.

Parasites can help to revise ecological theory which will

have great implications for research workers and veterinary

health managers [31]. It has been proposed by different

researchers that parasites play an important role in driving

the biodiversity and ecosystem functioning [32]. It is stated

that half of the biodiversity is composed of parasitic worms

[33]. They are believed to shape the communities and

enhance the ecological functioning [34, 35].

Parasites can give new insights about diversity patterns

can be useful for the promotion of biodiversity [32]. There

is a link between biodiversity and parasitism which is

partly due to host-parasite interaction. It has been stated

that generalist parasites reduce the biodiversity through

competition, whilst specialists tend to increase the biodi-

versity [32]. In addition, variation in species diversity can

be used in predicting the community structure and also

predicting disease risk for conservative targets.

There are many ecological patterns which are mediated

by parasites. In the past there was hardly any consensus

about the criteria which could be laid down to describe the

healthy ecosystem. Hudson et al. [32] argued that healthy

ecosystem is one which is rich in parasite species as many

important bottom-up and top-down processes are mediated

by parasites.

Helminths also show altitudinal gradient in their distri-

bution i.e. with the increase in altitude, species richness

and abundance of helminths decreases. This has been

proved by Zargar [36] while testing the prediction that

diversity and abundance of helminth species will decrease

with the increase in altitude due to variation in temperature

regime and adaptability of particular species of helminth.

Altitude can serve as a proxy for temperature [37] and can

play an important role in predicting the species pattern of

helminth parasites of fish in different altitudinal zones.

Quilchini et al. [38] also supports the view that altitude,

hydrographic network and season could have an impact on

the species richness of parasites. However, it needs to be

seen whether all parasites show same response to the alti-

tude. Kennedy [39] and Hartvigsen and Halvorsen [40], for

example, showed that altitude correlated negatively with

the species richness in British and Norwegian water bodies.

The reason could be that the unfavorable conditions could

favour colonization of less competitive or less abundant

parasite species [41].

Role of Parasites in Environmental Monitoring

Environmental parasitology is being debated and discussed

at different levels in recent times [42]. There are many

reasons why parasites should be preferred for biomonitor-

ing over other organisms and modern probes. There are two

ways by which parasites can be used as bioindicators:

(i) they can be used as an effect indicator, or (ii) can be

used as accumulation indicator. Different researchers have

used different approaches to assess the effect indication

with parasites. Some have analyzed individual organisms

[43], whereas others have focused on parasite populations

and communities with respect to environmental pollution

[44]. It has also been shown in literature that conventional

effect indication have been less promising [42] than effect

indication by population or community structure [45] as

latter is more holistic approach than the former.

The occurrence of infectious diseases in natural popu-

lations is a consequence of interaction between pathogens,

their hosts, and the environment in which they live [46–

48]. Several studies have appreciated the importance of fish

parasites as a biological tag [45, 49, 50], and many authors

have attempted to analyse parasite-contaminant associa-

tions [45, 51–53]. Under eutrophic conditions, parasites

tend to be host generalists, favouring trematodes in par-

ticular [54]. A positive relationship has been reported

between eutrophication and fish parasitism [55–58].

0

5

10

15

20

25

Diseases Species

Tot

al n

umbe

r

Humans

Experimental diseasemodel

Fig. 3 Number of helminth diseases and species studied in humans

and experimental disease model. Figure is shaped on the basis of

Khan and Fallon [29]

Parasite with Multiple Roles

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The helminth parasitic fauna can be used to assess the

environmental quality of aquatic ecosystems showing

altered environmental gradient [7, 8, 59]. The data on the

prevalence and abundance of helminth parasites in fish can

provide supplementary information on the pollution status

of a water body [7]. The increase in nutrient enrichment

can enhance the helminth infections in fish and data has

shown that eutrophic and hypertrophic habitats were

favourable for the monogenean gill parasite [8]. In addi-

tion, monogeneans can show both antagonistic and syner-

gistic response to the combined effect of pollution and

eutrophication [8]. It is further felt that the environmental

features of aquatic ecosystems play an important role in

shaping the pattern of fish parasites [60].

In recent past some researchers have used meta-analysis

to determine possible statistical interactions between

environmental impact variables and parasites. Notable

contribution is from Martinez et al. [61] and Blanar et al.

[62]. Martinez et al. [61] in their meta-analysis compiled

relevant studies published in the previous years and dem-

onstrated significant effects and interactions between par-

asite levels and the presence and concentration of various

pollutants and/or environmental stressors. It was found that

the 52 studies and their 242 comparisons, as well as the

field studies subset, revealed no significant overall effects

or interactions. All the experimental and accumulation

study subsets showed significant overall effect sizes for

both factors and the interaction. It is further suggested that

environmental impacts have significant effects on parasites

[61]. There are mounting evidences from the literature that

parasites play an important role in assessing contamination

level in an ecosystem (Table 2).

Role of Parasites in Ecosystem Energetics and Food

Web Topology

The role of parasites have been discussed and debated by

some authors from time to time. Amundsen et al. [74]

introduces his paper by giving an exciting example of Carl

von Linnes expedition to subarctic Lapland, where he

refused to eat heavily infected fish and advocated to

unravel the role of parasites in the food web. In recent past

researchers have put their effort to see the role of parasites

in food web [74–79]. Kuris et al. [79] made an attempt to

assess whether parasites contribute any biomass to the

ecosystem. Thompson and Townsend [80] assessed the

degree to which food webs display patch-scale variation,

and the consequences for emergent properties at the larger

scale of the stream reach and concluded that reach-sum-

mary food webs were consistently different from patch-

specific food webs in each stream. The majority of food

web topology studies based on parasitic worms have been

used to test ecological theory [80]. Thompson and Town-

send [80], for example assessed the degree to which food

webs display patch-scale variation and reach-summary

food webs were consistently different from patch-specific

food webs in each stream. They can alter the topology of a

stream food web across seasons [81].

Other Roles

Two new dimensions came into existence in the second

half of last decade, one explaining the role of parasitism

on sex and another stating the role of parasitism on

human behavior. Weeks [82] explains how a parasite

(Wolbachia) which was initially bad for the host later on

evolve in such a way that it increased the reproductive

potential of host.

Parasites can also influence the human culture by

manipulating individual behavioral traits in human beings.

This is explained by Lafferty [83] while carrying out a

survey in different countries who are hit by Toxoplasma

gondii. He adds that people who have association with cats

are more prone to neuroticism characterized by high levels

of anxiety. This may also show cross cultural differences as

some societies are not prone to T. gondii as they don’t keep

cats as pets.

What Will Happen if Parasitic Species are Removed

or Their Eradication Programmes are Launched?

As parasites can regulate the host communities and shape

the parasite communities, it is important to think that the

removal of parasite species may alter the whole community

[1]. It has already been suggested in past that removal of

any organism may have detrimental impact on an ecosys-

tem. The mass scale eradication of mosquito’s, which are

carriers of malarial parasite, is not recommended because

of the contribution of mosquitoes in making substantial

biomass in aquatic ecosystems [84]. Stronger argument for

keeping organisms like mosquitos on earth would be if they

provide some sort of services to human beings. The fact

remains that nature has not created organisms to provide

services only to humans as there are other roles which an

organism can play for the betterment of an ecosystem.

Currently, there is a debate to understand how relationships

are interwoven among organisms, processes and their sur-

roundings. More stress is given to species or populations

that provide specific ecosystem services [environment

service providers (ESPs)] and parasites in this sense show

great promise.

There are two viewpoints regarding the eradication of

disease or a parasite. One is human centric approach i.e. to

U. R. Zargar et al.

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eradicate the disease or parasite because they pose great

threat to human welfare, though there are various issues

which should be taken care of while thinking of eradication

of any species [85]. Another is ecological approach i.e.

giving more stress to positive aspects than to negative

aspects. There is a need of consensus before embarking

eradication programmes against diseases or parasites as

there is dearth of information regarding the disease pattern

[86]. The health experts, for example, opine that global

warming may have effect on disease pattern, and this may

put halt on eradication programmes. One may also argue

that there exist mechanisms in nature which favour eco-

logical balance and the mutual co-existence of biological

organisms. So, permanently wiping out an organism

including parasite is unwise because this could lead to

ecological imbalance. It is therefore important for public

health authorities to consult epidemiologists and ecologists

to seek a broad scientific consensus [86].

Conclusion

So, where are the humans now? They actually are at

crossroads where they have to think both ways; one to have

a control over parasitic diseases which pose great loss to

animal life and second to propagate positive aspects of

parasites in ecological functioning among the general

public. Although majority of veterinary researchers are

concerned about the parasitic diseases, but there are some

who regard the multiple roles of parasite which they show

at various levels. However, more studies are needed

regarding the role of parasites at different levels. Studies

should focus on three issues:

1. To see whether parasites are only disease causing

agents or they have other major roles

2. Role of parasites in ecological functioning

3. Assessment of environmental quality by using parasites

Table 2 Evidence from the literature about the association between parasites and contamination level (adapted from Sures [42], with some

modification)

Parasites Host Pollution/

contamination

Effects Refs.

Component community Perca fluviatilis (perch) Acidification Reduced parasite diversity [63]

Trichodina sp. Hippoglossoides platessoides (American

plaice)

Contaminated

sediments

Higher abundance [64]

Component community Schizothorax niger Eutrophication Higher abundance, intensity and

diversity

[7]

Component community

and infra-community

Schizothorax esocinus Eutrophication Higher abundance, intensity and

diversity

[60]

Intestinal digeneans Hippoglossoides platessoides Contaminated

sediments

No effect [63]

Trichodinid ciliates Platichthys flesus Eutrophication, general

marine pollution

Increase in prevalence and density [65]

Component community Rutilus rutilus (roach) and Perca fluviatilis Eutrophication Increase in parasite richness [66]

Parasite community of

snails

Physella columbiana (rotund physa) and

Lymnaea palustris (marsh snail)

Heavy metals Lower diversity and intensity [67]

Acanthocephalans Tautogolabrus adspersus (cunner) Municipal and

industrial effluents

Increase in prevalence and intensity [68]

Trichodinid ciliates Gasterosteus aculeatus (three spined

stickleback)

Organic pollution Increase in density [69]

Component community Leuciscus cephalus (chub) Organic pollution Decrease in species richness [70]

Component community Sigmodon hispidus (cotton rat) Petrochemicals Decrease in number of helminth species [71]

Dactylogyrids Rutilus rutilus Pulp and paper mill

effluent

Reduced abundance and mean number

of species

[72]

Rhipidocotyle fennica

(Digenea)

Rutilus rutilus Pulp and paper mill

effluent

Higher abundance and intensity [73]

Diversity increased with the decrease of

pollution and water quality

Diplozoon kashmirensis Carassius carassius Eutrophication and

contamination

Antagonistic and synergistic effect [8]

Parasite with Multiple Roles

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In next 100 years, researchers may be able to find new

roles which are beyond imagination. There is great debate

on the use of model organisms in space and who knows

parasites may show great promise. Nematodes have already

been used as a model organism for space. Only time will

tell us whether parasites are really showing promise in

different aspects.

Acknowledgments U R Zargar highly acknowledge the discussions

with elite researchers of Parasitology during the preparation of this

review. The inputs from the National workshop held at Allahabad

University also helped the authors in great deal to shape up this

review. In addition, U R Zargar appreciates the facilities provided by

the Director CORD for carrying out research in the research centre.

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