asite literature.

These papers also became the

10.1 I Background modern standard for parasite community ecology.
Ten years later. Crofton (1971a. b) established a
If the study of the ecology of parasitic organisms similar standard for a quantitative approach in
is considered in its broadest form, then it has a the study of parasite population dynamics.
long history. extending back to the middle of MacDonald (1965) was the first to extensively
the nineteenth century when fue connection employ mathematical modeling in the study of
between cysticerciand adult taeniid cestodeswas host-parasite relationships. Over the last 30-35
identified by Dujardin in 1845,when the life cycle years.investigations on the ecologyand epidemi-
of the canine tapeworm, Taenia pisifonnis,was ology ofparasitic organisms and their hosts have
experimentally completed by Kuchenmeister in expandedsignificantIy.
1852. or when the life cycleof Fasciolahepaticawas -

mostly elucidated by Leuckart and Thomas in

10.2 I General definitions
1882/3(Box 1.1).Thesediscoverieswere matched,
if not exceeded. by Sir Patrick Manson who
described the life cycle of Wuchereliabancrofti in Ecology can be considered within the context of
1877 and by Rosswho reported the life cycle of two. quite different methodologies.Autecology is
avian malaria in 1895; Sir Ronald Rosseventually concerned with the study ofindividual organisms
was to receive one of the first Nobel Prizes in or species.The approaches taken here can be
physiology in recognition of this exceptional varied but. plainly. population biology is auteco-
researchachievement. logical in character.A population can be defined
Modern parasite ecology can be traced to V. A. as a group oforganisms ofthe samespeciesoccu-
Dogiel and bis colleagues(Dogiel, 1964).Many of pying a given space in time and comprising a
these early studieshad a decided 'natural history' single gene pool. Each population can be
flavor, but they were nonetheless ecological in described by severalparameters. Some of these
their scopeand approach.The researchtrends in include birth rateo death rateoage distribution.
parasite ecology and epidemiology have contin- biotic potential (reproductive potential). disper-
ued to becomemore and more complexwith time sion. growth pattern. and density. Investigations
and the development of new technologies. on the population biology of human parasites
However,it was not until Holmes (1961.1962a,b) contribute to the discipline of epidemiology.
published bis now classicalstudies on the inter- whereasstudies on the population biology ofpar-
specific competitive interactions betweenthe rat asitesin other animals are in the realm of epizoo-
tapeworm Hymenolepis diminuta and the acantho- tiology. Synecologydealscollectively with groupS
cephalan Monilifonnis dubius that a quantitative of organisms of different species that live
perspectivebecamesolidly entrenched in the par- together. For synecology.the approach is at the
 community level. A community of organisms is by those working in the area ofparasite commu-
defined as a group of populations of different nity ecology(seeBush & Holmes, 1986;Holmes &
speciesoccupying a similar habitat or ecosystem. Price, 1986; Eschetal.. 1990a;Bush et al., 1993).
An ecosystem encompassesthe community of It should be noted here that a terminology
organisms,plus their physicalsurroundings. issue for parasite ecology was precipitated by
Mostofthese conceptswere developedfor free- severalofthe earlierworks and the initiaI resolu-
living organisms, but there are certain problems tion was provided by Margolis et al. (1982).
when the concepts are applied to parasites. For However,with the increase in ecological research
example, do all members of a given parasite in the following years. the need to revisit the
specieswithin a single host constitute a popula- issue becameapparent. Toward this end. Bush et
tion? Or, do all members of a given parasite al. (1997)re-examined the use of terms and con-
specieswithin all hosts in an ecosystemrepresent cepts as they applied to the community ecology
a population? Another difficultywith the concept of parasitic organisms. They attempted to clarify
as applied to parasitesis that populations offree- some of the old questions and to raise ~ome new
living organisms increase in number through issues as well. Students are advised to refer to
birth, or immigration, or both, whereas most both the Margolis etal. (1982)and Bushetal. (1997)
adult helminth parasites in a host increase only papers,as they will be useful in providing a pre-
through immigration, or recruitment. In an amble to the terminology employed in ecological
effort to clarify theseissues.Eschetal. (1975a)pro- parasitology.
posed that parasites within a single host and The conceptualization of parasite population
those within all hosts in an ecosystembe separ- structure can be viewed in terms of a nestedhier-
ated and .considered independently. They devel- archy (Fig.10.1).Consider,for example. the three-
oped the concepts of the infrapopulation and host life cycleora hypothetical digenean.one that
suprapopulation to addresstheseissues.An infra- involves a snail as the first intermediate host, a
population was describedas one that includes all fish asthe secondintermediate host. and a bird as
of the parasitesof a single speciesin one host. A the definitive host. Forthis parasite,active recruit-
suprapopulation was defined to include all ofthe ment (solid lines in Fig. 10.1)is associatedwith
parasitesof a given species,in all stagesof devel- free-swimmingmiracidia (asterisks)and cercariae
opment, within all hosts in an ecosystem. (plus signs).The transmission ofmetacercariae to
Margolis et al. (1982)reiterated this terminology the definitive host is a passive process, almost
and expanded on it. always depending on predator-prey interactions
Subsequently,Bush et al. (1997)modified the (dashedline in the figure). A spatial aspectto the
terminology and applied the term component transmission processis introduced with the posi-
population to describe all of the infrapopula- tioning of the symbols for miracidia and cercar-
tions ora speciesofparasite within all hosts ora iae. The large box that circumscribes the system
given species in an ecosystem.The numbers of represents the suprapopulation; observe that it
studies on infrapopulation and componentpopu- includes all of the component and infrapopula-
lations are substantial and far exceedthose at the tions, aswell asthe free-living stages.The large tri-
suprapopulation level.This is mainly because the angle represents the component population of
logistics are far too complex in the latter caseto parasitesin snail hosts that. in turno is composed
coverall stagesof a parasite'slife cycle in a single of a series of individual snails (smaller triangles),
ecosystemat the same time. Severalinvestiga- each with its own infrapopulation of parasites.
tions have been attempted on suprapopulations The same kind of nesting is associatedwith the
(Hairston, 1965;Dronen, 1978;]arroll, 1979,1980), large rectangle and the large circle. The latter rep-
or atleast partially attempted (Riggset al., 1987; resent component populations of metacercariae
Marcogliese & Esch, 1989),and these will be dis- in fish secondintermediate hostsand the rectan-
cussed subsequently. Since the development of gles are definitive hosts. Infrapopulations within
this scheme for parasite population ecology. a individual fish are smalIer circles and individual
similar hierarchical approach has been adopted birds are the smalIer rectangles. In considering~
 are, however, influenced by a range offactors both
external and internal to the host (seealgo Chapter
13). Recruitment into a host can be passive, requir-
ing no expenditure of energy by the parasite, or
it can be active in which case an expenditure
of energy is required. Table 10.1 provides an idea
of the wide-ranging tactics that parasites have
evolved in achieving recruitment success, by
either active or passive means. The list is some-
what distorted, however, since the process of
active recruitment is almostentirely restricted to
8 parasites that reqtiire water to complete their life
8 cycles. Exceptions here would indude certain
Suprapopulation Componentr¡;;;;;:1
~ nematode species and, even then, their free-living
larvae require special soil conditions (moisture,
A schematic representation for the hierarchical shade, etc.) in which to survive. The turnover of
organízation of parasite infra-, component, and parasite infrapopulations will result from natural
suprapopulations. Whereas it represents a hypothetical host and parasite mortality, inter- and intraspe-
digenean, the scheme applies to virtually any host-parasite cific interactions, and from the effects of host
system. The small asterisks represent miracidia in the viciníty immune responses. In some cases, fue turnover
of snails; the small triangles are infrapopulations within
processeswill be directIy affected by external as
.molluscs; the large triangle represents a component
well as internal environmental factors.
population of several molluscs. The small + signs are
cercariae in the vicinity of the second intermediate host; the
small cirdes are infrapopulations in second intermediate
10.3.1 External environmental factors
hosts. The large cirde is a component population of Free-living stages are direct1y affected by abiotic
metacercariae. The small rectangles are infrapopulations of environmental factors. For helminth parasites,
the parasite in the definitive host; the large rectangle is the such stages would include, among others, mira-
component population of the adult parasite. Salid lines cidia and cercariae of digeneans, coracidia of
represent active transmission and dashed lines are passive many pseudophyllidean cestodes,and the rhabdit-
transmission. The large box circumscribing the entire figure
iform and filariform larvae of some rhabditid and
represents the suprapopulation of parasites.
strongylid nematodes. The eggs ofhelminth para-
sites and the cysts of many parasitic protozoans
are also affected by the external environment. If
the suprapopulation as a nested hierarchy, the terrestrial, then photoperiod, temperature, and
ideas of parasite flow, and of recruitment and humidity, are but a few of fue environmental
turnover, can algo be visualized. More impor- factors that will affect their development, survi-
tantly, even though the nature of fue processes vorship, etc. In freshwater habitats, temperature
that impact on the dynamics of the system have and water current are important elements in fue
not been illustrated, the idea of gene flow within biology of ectoparasites, e.g., copepods. In marine
the suprapopulation is algo implicit. environments, salinity and temperature have been
shown to affect the biology of ectoparasitic organ-
isms. In terrestrial, freshwater (Jokela & Lively,
1995), and marine (Curtis, 1997) habitats, a prime
feature affecting the risk of infection is fue spatial
distribution of infective agents and 9f hosts shed-
The diagram in Fig. 10.1 is a simplifiedwayofillus- ding infective agents.
trating theidea ofparasite transmission through Consider the host-finding capability of free-
a series ofhosts within the framework of a supra- swimming miracidia _and the combination of
population. Parasite recruitment and turnover physical and chemical factors that influence this
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transmission dynamics (Esch et al., 1997).The life-
cycle pattern of this hemiurid digenean is much
more complicated than that of most other dige-
neans as it has three obligate hosts, and a para-
tenic host (Goater et al., 1990; Zelmer & Esch,
1998a).Adults live under the tongue ofthe green
frog Rana clamitans, throughout temperate afeas
of North America. Eggs are swallowed and then
shed by the frog when it defecates.The snail inter-
mediate host Helisoma ancepsmust then eat the
eggs.Once inside the snail gut, the eggs batch and
a motile larval stage penetrates the gut wall and
migrates to the hepatopancreas where sporocysts Q)
.~
develop. Mter a sporocyst generation, rediae are
~
released from the sporocysts and eventually spill ~
o
ayer into the gonads. These voracious larvae
consume the gonads and cause host castration.
Cercariae are then produced by the rediae and are
released from the snail. One of the unique charac-
teristics of this parasite is the unusual cystophor-
ous cercaria, algo called a cercariocyst. These
cercariocysts are non-motile, but they have a rela-
tively extended life gran (Fig. 10.2). It has been
speculated that long-term survival by the cystoph-
orous cercariae has evolved as a temporal mecha-
nism for dispersal in time as opposed to the
spatial dispersal strategies employed by free-
swimming, but short-lived, cercariae of most
other species.Studies byWetzel & Esch(1995)have
shown that infectivity of the cystophorous cer- of cercariae of Ha/ipegus accidua/is at

caria for the next host (an ostracod, a microcrus- constant temperature. Values are percent and 95%

tacean) is not related to the ability ofthe parasite confidente limits. Salid and open circles show results from
two experiments. (Modified from Shostak & Esch, 1990, with
to excyst. Excystment is a purely physical phenom-
permission, /nternatiana/ jaurna/ far Parasita/agy, 20, 95-99.)
enon apparently related to rupture of the outer
cyst wall, followed by changes in the internal
osmotic pressure which forres eversion of a deliv-
ery robe from the body of the cercariocyst, then by bridge the ecological, or trophic, gap (Zelmer &
the forceful ejection of the body of the parasite Esch, 1998a). If development of the metacercaria
through the delivery robe (Zelmer & Esch, 1998b). is incomplete when the ostracod is consumed by
Infectivity of the parasite is a strictly temporal the odonate, development will continue inside
factor. fue midgut of the naiad until it becomes infective
The cystophorous cercariae are accidentally for the frog.
ingested by benthic ostracods in which the para- The distribution of Halipegus-infected snails
sites penetrate the gut wall and develop into infec- was examined from a microhabitat perspective in
tive metacercariae within the hemocoel. However, a small, 2-ha pond in the Piedmont afea of North
transfer of the metacercariae from an ostracod to Carolina, USA(Williams & Esch,1991). They found
a frog definitive host is unlikely to occur since that infected snails were not randomly distrib-
frogs do not normally feed on ostracods. Instead, uted in the littoral zone of the pond, but were
an alternate host, the odonate naiad, is used to concentrated in very shallow water, < 5.0 cm,
 FACTORS AFFECTING PARASITE POPULATIONS 317

The prevalence of Ha/ipegus accidua/is in the

pulmonate snail He/isoma anceps, with respect to the
substrate from which the snails were captured. (Modified
from Williams & Esch, 1991, with permission,journa/ of
Parasitology. 77. 246-253.)
immediately adjacent to the shoreline (Fig. 10.3) l -
and were found significantly more often on leaf
substrata in the shallow waters (Fig. 10.4).These were primarily associatedwith afeaSof the pond
observationson the microgeographic distribution which favored all facetsofthe parasite'stransmis-
of H. occidualisserve to emphasize the concept sion success,i.e.. the frog's predatory and repro-
of 'scale' in considering the overall population ductive activities. an appropriate substratum
dynamics of different species of digeneans and conducive for the life histories ofsnails, ostracods.
probably other parasites as well. They explained and odonates. and emergent vegetation which
the distribution ofthe infected snails by correlat- would permit odonate naiads to successfully
ing it with the behavior of the definitive host. crawl out of the pond and onto the vegetation.
Creenfrogs are ambush predators,spendingmost then transform from an aquatic to an aerial stage.
of their time submerged in very shallow water The concept of landscape ecology/epidemiology
along the pond's edge.It is here that they defecate has broad implications for the transmission
and shed eggsin high concentrations. Snails such dynamics of a wide range of protozoan and hel-
as H. ancepsgraze the leaf litter and other sub- minth parasites,including many of those infect-
strata in the littoral zone.As they do,theyencoun- ing humans. and will be discussed.asappropriate.
ter aggregations of parasite eggs, primarily in in other sectionsofthe texto
shallow water and on leaf litter that, in effect, Of the external factors affecting infrapopula-
function as enhanced transmission foci, or 'hot tion biology of endoparasitic organisms, diet is
spots', for the parasite. probablythe mostbasic.Forexample,manyof the
The idea of these enhanced transmission foci enteric parasites within a definitive host are
was extended to encompassthe concept of land- present because the host ingested an infective
scapeecology/epidemiology.Accordingto Beeby& stageofsome parasite.Dogiel (1964)madea strong
Brennan (1997),landscapeecologyis the 'study of casefor the importance of diet in influencing the
the spatial arrangement of ecosystemsand the parasitefauna within hostswhen he said. 'the par-
large-scaleprocessesthat unite them'. Landscape asitological indicators of diet are among those
epidemiology would include application of the clues that allow us to make deductions from the
sameideas of scaleprocessesto the transmission type of parasitefauna about various aspectsof the
ofparasites. Zelmer etal. (1999)examined the dis- ecologyof the host'. In other words, parasitologi-
tribution of infected green frogs in the North cally. you are what youeat! He illustrated his point
Carolina farm pond mentioned above.Theydeter- by noting that herbivorous cyprinids within an
mined that these so-called 'hot spots' (Fig. 10.5) aquatic systemwere virtually devoidof enteric hel-
318 POPULATION CONCEPTS

45

40

35
.
1996
o
1995
+
1994
...
o 1993

o+,¡..
o

o.
" .

18 20 22 24 26 28 30

the herbivorous diet that in reality causesthem to

becomeinfected with speciesof Neoechinorhynchus.
Horsesare herbivores and they also often harbor
rich faunas of strongylid nematodesin their gut.
Theseparasitesare accidentally acquired as filari-
form larvae while the horsesgraze. Somedetriti-
VOTessuch as mullets (Mugilidae) have rich
minths, whereascarnivorous cyprinids within the digeneanfaunas that are acquired as the fish feed
same systempossessedrich helminth faunas.The on the benthos of estuarine and marine coastal
implication is that carnivory is more likely to afeas,accidentally ingesting metacercariaeof the
result in recruitment of parasitesthan herbivory, parasites present in the detritus (Paperna &
but there are many exceptionsto this pattern. For Overstreet, 1981; Fernández, 1987). Bush et al.
example, slider turtles Trachemys smpta are typi- (1993)describe what they can 'source communi-
rally omnivorous. but feed extensivelyon aquatic ties' in intertidal crabs. In these cases,the crabs
vegetation. It is the herbivory that results in the havebeenshownto recruit severalspeciesoflarval
recruitment of an extensive acanthocephalan parasitesand then, when ingested by appropriate
fauna of the genus Neoechinorhynchus (Eschet aJ., predators, the infective larval forms are trans-
1979a, b; jacobson, 1987). These parasites use ferred to the new hosts where they establish as
various speciesof ostracodsas first intermediate adults. As described by Lotz et al. (1995),'these
hosts.The ostracodsare part ofthe epiphytic fauna sourcecommunities are transmitted in packetsof
associatedwith aquatic vegetationand are acciden- infective propagules to target communities in
tally consumedasthe turtles feed.Whereasturtles definitive hosts'. They went on to note that such
are accidentallyexposedto infected ostracods,it is transferswould result in greaternumbers of posi-

.
.
 FACTORS AFFECTING PARASITE POPULATIONS 319

tive associations among parasite species within and parasite genetics. natural and acquired resis-
some definitive hosts than what might otherwise tance, ontogenetic factors associated with the
be expected. aging process,and host sexmar be involved; more-
Also of course, a strong case can be made for the over, several of these frequently act in concert.
relationship between diet and parasites in humans. Inter- and intraspecific interactions among infra-
Many ofthe enteric protozoans ofhumans are, for populations of certain speciesmar also affect par-
example, acquired through the accidental inges- asite densities and fecundity. It is well known. for
tion of cysts that occur externally on contaminated example. that eggproduction by someenteric hel-
food or in water, e.g., Giardia lamblia, Entamoebahis- minths will rise with increasing parasite density,
tolytica, E. coli. Balantidium coli. The same route of but will reach a threshold or evendecline ifpara-
infection is used byeggs ofmanyenterichelminths. site densities increase abovea certain point (see
e.g., Ascaris lumbricoides,Enterobiusvermicularis.and Chapters11and 14 for a more extensivediscussion
Trichuris trichiura. Human parasites are acquired by of competition).
ingestion of a wide range of foods, e.g., Fasciola The two most complex internal factors affect-
hepatica (watercress), Diphyllobothrium latum (fish). ing parasite infrapopulation biology are asso-
Taenia solium (pork). Taenia saginata (beef), and ciated with the host's immune systemand with
Trichinella spiralis(pork). For a number ofthese latter the geneticsofboth the parasiteand the host.This
parasites. transmission depends on long-standing. complexity is compounded since the genetics of
local 'culinary' customs, e.g.. the consumption of the host also impacts directlyon its immune capa-
poorly cooked or raw fish, beef, and pork. or on poor bilities. One of the best-studiedcasesof such an
socioeconomic conditions, or a combination of diet interaction involves the deer mouse Peromyscus
and wealth (or lack thereof). Finally, there is an maniculatusand the tapeworm Hymenolepis citelli.
inextricable link between nutrition (not just diet) Wassom et al. (1973. 1974, 1986) reported that
and parasitic infection (Crompton. 1993); this will these tapeworms were aggregated within the
be discussed more fully subsequently. definitive host and that the prevalencewas low,
Only a few of the external environmental less than 5%.They attributed these observations
factors known to affect the infrapopulation to the heterogeneous distribution of infected
biology of parasites have been identified here. We intermediate hosts (camel crickets. Ceuthophilus
hope, however. that these examples will serve as utahensis)within the habitat of the deer mice.
an introduction. Other factors will be considered Moreover,they presentedevidencethat about 75%
more fully in subsequent chapters. These include of the deer mice are endowed with natural resis-
seasonal changes in photoperiod and light inten- tance. That natural resistance is related to a
sity, ecological succession, the many ramifica- single. autosomal dominant gene. The result is
tions ofnutrient loading and pollution in aquatic rejection of the tapeworms before they can
habitats, ecosystem stability. dispersion, and become sexually mature and this contributes to
other spatial distribution patterns such as those both the low prevalenceand the aggregateddistri-
discussed above for H. occidualis. The zoogeo- bution ofthe parasite.
graphic factors intluencing the global distribu- Host behavior, age, and sex are factors that
tion of both parasites and their hosts will be mar influence the infrapopulation biology of
considered as well. someparasitic organisms. In a few cases,all three
factors canbe inextricably linked. A good example
10.3.2 Internal environmental factors of this linkage is associatedwith aspects of the
The range ofinternal environmental factors affect- infrapopulation biology of the cestode Proteoce-
ing the infrapopulation biology of parasites is phalusambloplitis.Definitive hosts for this parasite
probably not as great as the external ones, but. in are smallmouth bass Micropterusdolomieuiand
some ways. internal factors are more complex largemouth bassMicropterussalmoides. Mter eggs
than those external to the host. This is true pri- are released from the adult tapeworm, they are
marily because phenomena such as behavior, host shed in fue reces.Eggs are freed from the fecal
320 POPULATION CONCEPTS

material, float in the water column, and are con- copepodsand those acquired through predation
sumed by severalspeciesof planktonic copepods. on small fishes and fingerlings infected with
An oncosphereemerges from the egg and pene- plerocercoids that were obtained from copepods
trates the gut wall of the copepod; it enters infected with procercoids.
the hemocoel and develops into a procercoid. The final step in the cycleinvolves severalphe-
Planktivorous fishes then eat the copepods. It nomena about which not much is understood. In
should be emphasized that, for the most part, the spring of eachyear,when water temperatures
only speciesof smaller fishes and fingerlings that rise, adult tapeworms begin to accumulate in the
will grow to much larger sizeswill normally feed pyloric ceca of sexually mature bass (all adult
on copepods.We thus have an example of an age- worms are lost each fall and are replaced the fol-
related or, perhaps more precisely,a size-related lowing spring by a new infrapopulation). Under
transmission tactic. Within the gut of the small laboratory conditions, Fischer & Freeman (1969)
fish, the procercoid is freed from the copepod by were able to demonstrate that rising temperature
digestion and the liberated parasite penetrates was apparently the stimulus for migration of
the gut wall where it developsinto a parenteric parenteric plerocercoids from sites within the
(outside the intestine) plerocercoid. The plerocer- abdominal cavity into the lumen of the pyloric
coids of P.ambloplitisare able to migrate through- ceca.However.this migration also coincides with
out the visceral mass, e.g., liver, gonads, and increasesin the level of circulating spawninghor-
spleen, of infected centrarchids using a metallo- mones released from the gonads and pituitary
proteinase for digestion of host tissues,and are gland in the spring. The spawning act in small-
capable of inducing considerable tissue damage mouth bassis preciselydetermined by water tem-
in the process (Esch & Huffines, 1973; Coggins. perature. An interesting feature in this processis
1980a,b; Polzeret al., 1994). that, when sexuallymature bassbegin to acquire
Another age-related component of the para- new plerocercoids from plerocercoid-infected
site's life cycle is also involved. In arder to com- fishes as the summer progresses.the new plero-
plete the cycle,the plerocercoid must first reacha cercoidsmigrate into parenteric sites and do not
parenteric site within the definitive host, almost developinto adult tapeworms until the following
always a sexually mature smallmouth or large- spring. In other words, all plerocercoids appar-
mouth bass.This can be accomplished in one of ently must spend at least part of one annual cycle
two ways. First, a larger basscan eat the plerocer- in parenteric sites within a sexually mature bass
coid-infected small fish or fingerling. If this before migrating back into the pyloric ceca and
happens,the plerocercoid will be digested from developing into adults within that bass. This
the flesh of the intermediate host and then could be interpreted asa mechanismto minimize
migrate through the gut wall of the bassinto the competition betweenan alreadyestablishedadult
body cavity. Once inside, it will migrate into infrapopulation and new. potential adults. It may
various organs such as the gonads, spleen, and alsobe a way to separategene pools on an annual
liver. Apparently, it continues to wander in these basis. Plerocercoids occurring in other centrar-
organs,growing in size until an appropriate stim- chid speciessuchas the bluegill. Lepomismacrochi-
ulus is received. rus, will not migrate out of parenteric sites after
In the second route, the copepod containing the fishes become sexually mature even though
the procercoid is consumed by a fingerling bass, subjected to rising spring temperatures. This
in which casethe parasite migrates into a paren- clearly implies that the stimulus for migration
teric site within the fingerling and changesinto a from parenteric sites in bassis not rising temper-
plerocercoid. It wanders through various abdomi- ature alone, but is something specifically asso-
nal organs,growing in size until the bassbecomes ciated with the appropriate definitive host.
sexually mature. The infrapopulation ofplerocer- The precise nature of the stimulus in small-
coids within a bassthat becomessexuallymature mouth bass is not known. Fischer & Freeman
for the first time will thus consist of a mix ofpar- (1969)and Eschetal. (1975b)suggestedthat it was
asites acquired directly from procercoids in a combination ofrising temperaturesand increas-
 THE DISPERSION CONCEPT

ing levels ofhormones since migration coincided treatment with sexhormones. In these cases.the
with the spawning act and becausejuvenile bass uninterrupted reproductive activity of the para-
are not infected with adults even though they site is in some manner related to the continuous
usually possessplerocercoids.The problem with availability of its aquatic host (Tinsley & Owen,
this hypothesis is that in South Carolina (USA), 1975).
adults of P. ambloplitisare present in largemouth One ofthe most unusual sequencesofinternal
bassduring winter and disappearin the spring at migration and responsiveparasite adaptation is
about the time of spawning (Eure,1976).This is associatedwith the monogenean Pseudodiplorchis
opposite to the pattern that occurs in the north. americanus. This parasite passesthrough a wider
Whatever the migration cues, this systemis an range of external and internal habitats and is
elegant one to highlight the complex relation- exposedto more diverse physiological conditions
ships between parasite infrapopulation biology than any other monogenean (Cable & Tinsley,
and host behavior, age,and sexualmaturation. 1992). It reaches sexual maturity in the urinary
Another excellent example of a hormonal bladder of the desert toad Scaphiopuscouchii.
effect is associatedwith the synchronization of Following a very brief. free-living oncomiracid-
the life cyclesofthe monogeneanPolystoma integer- ium stagein an ephemeral desert pond. the para-
rimum and its frog host Ranatemporaria.Polystoma site enters the toad's nares and migrates to the
integerrimumenters the frog bladder before the lungs. Within the lungs, there are ontogenetic
tadpoles metamorphose and juvenile frogs changesin morphology that. presumably,prepare
becometerrestrial. Therefore,transmission of the the worms for migration through the entire
parasite to new hosts can occur only when frogs length of the intestine. The majority of the para-
invade temporary bodies of water to reproduce. sitesmigrate through the gut when their hostsare
When frogs are preparing to enter fue water prior gorging themselvesin arder to replenish bodyfats
to copulation (after 3yearson land),the reproduc- necessaryto withstand the upcoming estivation.
tive system of the monogeneandevelops.As the This migration presentsa formidable barrierwith
frog spawnsfor the first time, maturation ofP.inte- which to cope. e.g..the parasitesare subjected to
gerrimumoccursand eggsare released.In this way, radical changes in pH, secretions of bite acids
the synchronized mechanism ensures that when from the liver, digestiveenzymesproduced in the
the monogenean eggs batch, tadpoles will be stomach and pancreas. and anaerobiasis. In
available for infection. The high correlation partial response to fuese conditions, the pre-
betweenthe host's and the parasite'sreproductive adults in the lungs accumulate PAS-positivevesi-
cyclessuggeststhat reproductive developmentin des in the tegument, which are then releasedto
Polystoma is controlled by the hormonal activity of form a carbohydrate-rich glycocalyx as the para-
the frog. Indeed, experiments havedemonstrated sites enter the gut. Presumably,the glycocalyx
that maturation and stimulation of gamete pro- servesto isolate the surface ofthe fluke from the
duction in P.integerrimumcanbe elicited by inject- extremevagariesofthe gut during migration. The
ing the frog host with a pituitary extracto entire gut migration lasts for about 30 minutes,
However,it is not known yet whether the effect is afterwhich the production ofthe PAS-positiveves-
a direct one through the injected pituitary hor- icles stops; they are then repIaced by vesides that
mones,orvia the host gonadalhormones that are are morphologically distinctive ofthe adult stage
produced in responseto those releasedfrom the that now occupies the urinary bladder. and the
pituitary. A similar synchrony in life cycles has glycocalyxdisappears.
been demonstrated for Polystomastellai and the
--
tree frog Hyla septentrionalis(Stunkard, 1955). In
contrast, however, polystomatids parasitic in
IlóATThe dispersion concept
more aquatic amphibians, e.g., Protopolystoma
xenopodisin Xenopusspp., exhibit development Beforeconsidering further anybasic ideasregard-
that is not influenced by seasonofthe year,repro- ing parasite population biology and regulatory
ductive condition of the host, or by experimental~ interactions. it is first necessaryto identify and
322 POPULATION CONCEPTS

discuss several additional population terms and further efforts in this afea are clearly warranted.
concepts.The sample mean, X, is defined as the Wetzel & Esch(1996),for example,observedlarge
sum of all measurementsin the sampledivided by and rapid increasesin infrapopulation densities,
the number ofmeasurements in the sample.It is reminiscent ofthe 'sourcecommunity' structural
one ofthe most important measuresofwhat sta- changesalluded to by Bushetal. (1993)and Lotz et
tisticians refer to as measures of central tenden- al. (1995). These increases were frequently fol-
cies. The variance, (S2),of a sample mean is a lowed by suddenand sharpdeclines in infrapopu-
measure of mathematical variability within the lation densities, not unlike those reported by
population. It is important to note that the mean jackson & Tinsley (1994)for Gyrdicotylus gallieni,a
and variance, as we use them here, represent monogeneanthat occupiesthe buccal cavity and
values derived from a sampleas opposed to the pharynx of Xenopuslaevis.Both Wetzel & Esch
entire population. They are estimatesof the true (1996)and jackson & Tinsley (1994)ascribed the
population mean (J.L) and variance (0:2). swift infrapopulation declinesto host reactions in
Sincethe sample mean and the variance for a responseto high parasite densities.
given population are only estimates, it becomes The component parasite population's vari-
critical that sampling be conducted both accu- anceis an important estimate when assessingdis-
rately and randomly. Some species are clearly persion of parasites among th"e hosts. Consider
more difficult than others to enumerate and, the six distinct component population frequency
accordingly, a variety of sampling protocols have distributions in Fig. 10.6. In each of these cases,
been developed for various plants and animals the mean is identical, but note how the compo-
(Tanner,1987). nent populations differ in their dispersion char-
Parasiteinfrapopulations present specialprob- acteristics. If an assessmentis made regarding
lems. For all but a tew species,hosts must be killed the degree to which dispersion pattems of
beforeparasitescanbe counted.The problem with various component populations differ from each
this approachis that by killing the hosts,both the other, then substantially more information
hosts and the parasites they carry are removed about the component populations could be gen-
from both their overall populations and gene erated. Such a measurewould provide an idea of
pools. In some cases,this does not createa serious the spread, or variability, within the component
problem becausethe population sizeofthe host is population, which, in space,typically occurs in
sufficiently large that the removal of a few indi- three distinct patterns called random, aggre-
viduals will not significantly affect the reproduc- gated (or dumped) , and uniform (or regular)
tive capabilities of the remaining hosts or their (Fig.10.7).(SeeBox 10.1 for semantic issuesasso-
parasites. It is, therefore, necessary to obtain ciated with these terms in the fields of ecology
certain basic information on the population and parasitology.) Random distributions occur
biology ofboth the host and the parasiteand eval- when the position of one individual is completely
uate it carefully before undertaking a 'kill and independent of any other individual and when
count' procedure. each segment of the habitat has the same prob-
We might note here that Halipegusocddualis, ability of being colonized. Stated differently,
the hemiurid fluke that occupiesthe buccal cavity random distributions suggest that no interac-
ofthe green frog Ranaclamitans,is unusual in that tions occur among organisms. As such, random
it is one of the few endoparasitic helminths that distributions are the appropriate 'null model'
can be enumerated without killing the host and against which to test observed patterns.
therefore offers a number of unique advantages Aggregatedpatterns of distribution, on the other
over other species.Halipeguseccentricus occurs in hand, indicate possible socialinteractions, a need
the eustachian robe of the same host and is also to be together for some reason (mutual defense,
readily enumerated without killing its host. cooperative feeding, mating purposes), or the
Extensive studies using these two parasiteshave presenceof a suitable resource.Aggregateddistri-
shown that the dynamics of infrapopulation butions are the most common patlern found in
recruitment and turnover mar be more volatile nature. In uniform distributions the organisms
than previously expected or shown, and that are evenlydistributed or spacedin an area,imply-~
 THE DISPERSION CONCEPT 323

o
(/)
(/) x=3
-
o
(/)
(/)

.!:
'+-
o
.. ..c:
O+-
o
L- '-
a> Q)
.D .o
E E
:J :J
Z Z

2 3 4 5 6 7
Number of parasites

8
x=3
-o (/)
(/) 6
.t:
+
--
o
'- 4
Q)
.D
E
::J
Z

1 2 3 4 5 6
Number of parasites

l. An example of the variability with which different

Table 10.2. For each, the mean (x), the variance (52),
populations can be dispersed around the same mean. In each
case. the mean is the same (x = 3). but the distribution of the
and the variance/mean (52/X)ratio, or coefficient of
dispersion has been calculated. Note that for each
observed numbers is quite different.
-I
component population, the mean (x) is the same (x
= 6.0). The statistical significance for goodness offit
ing the existence of strong antagonistic interac- can be assessedusing a simple K test. In component
tions between them. population 1,the variance (52)is not significantly dif-
The importance of knowing the variancesand ferent from the mean (x); thus, 52~ x). In this case,
meansofparasite componentpopulationsis appar- the component population is randomly distributed.
ent when thesetwo estimatesare computedfor the Whenever the variance/mean ratio is clase to 1, a
three hypothetical componentpopulations givenin component population is randomly distributed. In

7
324 POPULATION CONCEPTS

."

". "

Random
ti) "(;;'
Q) "'iií
"5. o..c
E
(ti
ti)
(/) ro
o
'-"C
'- ro
Q) ;:¡
.D o-
E
::J O>!}j,
Z

Number of individuals in a sample

Distributional patterns in space (above) for Uniform frequency distributions are un-
populations that are random. regular and aggregated. Below common among parasite infrapopulations.
are the frequency curves that describe these distributions; Cestodarians ofthe genus Gyrocotyle,the digenean
the dashed line is the same random distribution for Deretrema philippinensis. and the copepod
comparison. Leposphiluslabrei are among the few exceptions.
Studies of different species of Gyrocotyle in holo-
component population 11,the variance/mean ratio cephalan hosts such as Otimaera monstrosa.
(52/X)is greater than unity (52>> X)and it is aggre- Hydrolagus colliei. Callorhynchus millie, and C. callo-
gated. In component population 111,the vari- rhynchus,reveal some striking similarities. In most
ance/mean ratio (52/X)is les s than unity (52<< x) and instances. prevalence is very high (90%-100%)and
this component population is uniformly distrib- parasite densities are low, with infrapopulations
uted. In other words. the distribution of values composed mostly oftwo individuals (Halvorsen &
around the mean in each component population is Williams, 1967; Dienske. 1968; Simmons & Laurie,
quite distinct and each distribution can be 1972; Allison & Coakley. 1973; Fernández et al.,
described mathematically; they will be random, 1983; Williams et al.. 1987; Donnelly & Reynolds.
aggregated, or uniformo The significance of under- 1994). Four possible mechanisms have been pro-
standing the &equency distribution of parasite posed to explain why uniform distributions occur
component populations will become more appar- among these species of parasites. The first sug-
ent when Crofton's (1971a. b) definition ofparasit- gests a reduction in the probability of infection
ism is discussed in greater detail. Since Crofton 's caused by ontogenetic changes in host biology,
seminal work, the concept of aggregation (he used e.g., in food selection or habitat. The second pro-
the term overdispersion) has become a central com- poses that parasite recruitment rates are equal to
ponent for paradigms involving parasite popula- death rates, thereby maintaining constant popu-
tion biology and of models employed in describing lation size. A third explanation suggests that
regulatory interactions between host and parasite heavier infections are lethal for the host. Finally.
populations (Anderson & May, 1979; May & it is also possible that further infections are pre-
Anderson, 1979). vented through intraspecific competition, or the
 THE DISPERSION CONCEPT 325

Box 10.1 Patterns of distribution: a matter of

terminology and tradition

Since the early nineteenth century, 'free-living' ecologists have recognized that
organisms are, for the most parto not randomly distributed in space. Most sci-
entists now recognize that the distributions of both free-living and parasitic
organisms follow one of three basic pattems. Random pattems can be
described mathematically by the expression S2=x. A second pattem, variously
called regular, uniform, spaced, negative contagian, or overdispersed can be
defined mathematically by the expression s2< x. The third pattem has also
been variously described as aggregated, clustered, clumped, contagious, patchy,
positive contagian, or underdispersed. This distribution is described mathe-
maticallyas S2>x.
The difficulty with some of these terms is that 'free-living' ecologists and
parasitologists use 'overdispersion' and 'underdispersion' to describe opposite
pattems of distribution. Unfortunately, when Crofton (1971 a) first looked at
the distribution of parasites, he used the mathematical term 'overdispersed' as
a synonym for aggregated or clumped distributions and 'underdispersed' as a
synonym for uniform or regular distributions. exactly the opposite to the
accepted manner in which most 'free-living' ecologists had applied the same
term1nolo~ Some parasitologists. including one ofthe most oft-cited papers
in parasite population ecology, i.e., that of Anderson and May (1979). follow
Crofton's lead and continue to use overdispersion to describe aggregated or
clumped distributions.
To avoid further confusion, and in an attempt to Standardize the usage of
these terms, we will use the more intuitive terms random, aggregated (or
clumped), and uniform (or regular) to describe the pattems of parasite distri-
bution. Because the terms 'overdispersion' and 'underdispersion' have had
general acceptance among some parasite population ecologists, we think that
any student, new to parasitologr; should be aware of this semantic problem. In
short, much of the primary literature in parasitology refers to aggregated or
clumped distributions as overdispersed. and to uniform or regular distributions
as underdispersed. Beware!

host's immune response,or both. Although not (Crenilabrusmelops)in Mulroy Bay,on the coast of
much is known about the biology of either hosts Ireland, were infected with a single individualof
or parasites.the evidenceavailablefavorsexplana- the copepod Leposphilus labrei,and that the other
tions based on the last mechanism. with regula- two hosts had just two copepods.Again, however,
tion mediated by antagonistic, parasite-parasite the mechanism responsible for these highly
interactions (Williams et al.. 1987). Another remarkable uniform distributions has not been
exampleora uniform distribution is Deretrema phi- determined.
lippinensis.a gallbladder digenean in the flash- Neither random nor uniform frequency distri-
light fish, Anomalopskatopron.Burn (1980)and butions are common in nature. By far, the most
Beverley-Burton& Early (1982)consistentlyfound common form of frequency distribution is one
two digeneans per gallbladder. with a prevalence that is aggregated.This pattern is as common for
ofalmost 100%.Donnelly & Reynolds(1994)found parasite component populations as it is for free-
that 1922 of 1924 infected corkwing wrasse living organisms. Several different theoretical
326 POPULATION CONCEPTS

Population Population 11 Population 111

Xj=3.1.1"0.5..8,1,2 Xj=10.11.2,3.'I1..3,2N=7 Xj=6.s.e.7.6.S.5N=7

N=l
x=6.0, x=6.0 x=6.0
52=8.0 sZ= 19.3 52= 1.33
S2/X= 1.33 s2/X=3.22 s2/X= 0.22
s2=x S2>x 52<X
Random diStribution Aggregated distribution Uniform distribution

Note:
Xi= number ofparasites in individual hosts, N= number ofhosts sampled in each population.

models, including the lognormal, lag series, Speciesthat employ such a growth strategy are
Neyrnan type A, and the negative binomial, can also frequentIy describedas opportunistic in the
describe aggregated frequency distributions. The sensethat they tend to maximize their reproduc-
significance of some of these models and their tive capacities and do not direct their energies

~
application to parasite population dynamics will toward enhancing the survivorship of their off-
be distussed in Chapterll. spring.
Most species do not exhibit exponential
10.5 ~.
growth except under ideallaboratory conditions
Dynamics of population
or during initial colonization. Instead,they follow
'"I
growth a logistic pattern (Fig. 10.8B);only when these
speciesare colonizing a new habitat, or perhaps at
Generally speaking, there are two patterns of the beginning of a new reproductive season,will
growth exhibited by populations of free-living they approximate an exponential pattern of
organisms. In an ideal environment that has growth. Even then, however,it is not truly expo-
unlimited resources, growth may be exponential; nential becauseofthe resistancecreated by many
that is to say, numbers per unit of space will environmental factors. The logistic growth curve
increase 1, 2,4, 8, 16, 32, etc. (Fig. 10.8Aj. The curve can be describedby the equation:
in Fig. 10.8A that illustrates this growth can be
described by the following equation:
~=rN(T)
dN --
-'-- = rN where K = the carrying capacity of the habitat, or
dt
that point in time when dN/dt=O. The term
where N = the number of individuals at time t, [(K-N) I K] means that as N increases, dN/dt
and r=the per capita rate ofnatural increase,or decreases. It is a measure of environmental resis-
biotic potential. The per capita rate of natural tance or crowding. WhenN=K, the term will be
increase,r, is the difference betweenthe instanta- O and dN/dt also will be O. The term [(K -N) IK] is
neous birth rate and instantaneous death rateo the simplest method of expressing the manner in
Thus,r is said to 'represent in a single number all which a population can expand up to equilib-
of the physiological responsesof all members of rium K. If N exceeds K, the term will become neg-
a poptilation to a given set of environmental ative and N will approach K from the other
factors' (Hairstonetal.,1970).Specieswith growth direction.
curves that are exponential in character are said The shape of a logistic curve is characteristi-
to be r-selected (Pianka, 1970; Esch et al., 1977). cally sigmoid (Fig. 10.8B). When a population ini-
 DYNAMICS OF POPULATION GROWTH 327

is directly related to that of the hare, although

Q.ti= rN others have challenged this conclusion.
dt If limiting factors are increased, then the
initial phase ofthe growth curve maybe repeated
K
dN
until some new carrying capacity is reached and
then it willlevel off again. In some cases,the pop-
r ulation will undergo senescence and become
N (Avdt=rN~ locally extinct. In these situations, perhaps the
popula tion has become toa specialized for a chang-
ing environment, or perhaps a competitor enters
1/ the habitat and is more successful than the previ-
00 Time (t) --. ously established population. Speciesthat exhibit
a logistic growth curve are said to be K-selected.
Population growth curves. (A) Exponential In concluding this brief primer on population
growth; (B) logistic or sigmoidalgrowth. N = number of
biology, a number of questions regarding parasite
individuals;K = carrying capacityof the environment; r = rate
population dynamics should come to mind. For
of increase.
example, how do parasites lit into the exponen-
tial-Iogistic schemes of population growth, or do
tially colonizes a habitat, growth is slow. This is a they lit at all? Are parasite population dynamics
time for physiological adjustment to new sur- regulated primarily by abiotic factors or by
roundings, or perhaps new mates are being density-dependent forces? If fue latter, are they
sought. This period of time is followed by a near- consistent ayer time? If the former, are most
exponential increase in population size. The dif- parasite species of the 'boom-bust' variety? Are
ference between the shape of the growth curve at growth patterns of most parasite species influ-
this point in time and a true exponential curve is enced by the stability or instability oftheir physi-
said to represent the biotic resistance of the cal environment? At what point(s) is parasite
environment. EventuaIly, however, environmen- population growth most likely to be checked and
tal pressures begin to slow population growth. which factors are most likely to impact on this
Resources such as nutrients or space may become growth? Can these check points be exploited by
limiting, or toxic materials produced by members intervention of drug therapies for the control of
of the population may begin to accumulate. parasite population dynamics? Most parasite com-
FinaIly, the population growth stabilizes; at this ponent populations are aggregated within their
time, birth and death rates become equal. Once host populations, but what is the significance of
the carrying capacity is reached, population size this sort of dispersion pattern within the frame-
wiIl remain reasonably constant except for erratic work of parasite population dynamics? May &
or irregular fluctuations in response to short-term Anderson (1979)claimed that parasitic organisms
shifts in various resources. Competition, preda- are highly effective in regulating host popula-
tion, and parasitism may algo influence popula- tions. Indeed, they stated, 'parasites (broadJy
tion fluctuations. There are some populations defined) are probably as important as the more
that osciIlate afier reaching their carrying capac- usually-studied predators and insect parasitoids
ities; in these cases,there are regular changes in in regulating natural populations'. In general
density ayer fixed periods oftime. The classic case terrns, there may be some, but very little, validity
is the lo-year lynx/hare cycle recorded by the to this statement if one includes viruses and bac-
Hudson Bay Company since the middle of the teria as parasites (and they did). On the other
nineteenth century. In this type of osciIlation, hand, if one includes only what the traditional
population densities of the lynx lag those of the parasitologists consider as parasites (mostIy proto-
hare with a high degree of fidelity. Some have zoans, helminths, and arthropods), then this
speculated that the population density ofthe lynx proposition would be questioned.
//
328 POPULATION CONCEPTS

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