ERI C J. WETZEL AND GERAL D W. ESCH · within Charlie's Pond, a 2-hectare pond in the Pied-mont...

J. Helminthol. Soc. Wash.63(1), 1996, pp. 1-7

Influence of Odonate Intermediate Host Ecology on theInfection Dynamics of Halipegus spp., Haematoloechm longiplexus, andHaematoloechus complexus (Trematoda: Digenea)

ERIC J. WETZEL AND GERALD W. ESCHDepartment of Biology, Wake Forest University, P.O. Box 7325, Winston-Salem, North Carolina 27109

ABSTRACT: The prevalences and relative densities of Halipegus spp., Haematoloechus longiplexus, and Hae-matoloechus complexus metacercarial infections in anisopteran (dragonfly) and zygopteran (damselfly) odonateintermediate hosts were examined. These measures of infection were compared in relation to the ecologicalhabits of the host species. Also, the extent of second intermediate host specificity was compared between the 2species of Haematoloechus. Eighteen species (N = 934) of odonates were dissected and examined for metacer-cariae. Halipegus spp. generally had the highest prevalences and relative densities of infection when comparedwith Haematoloechus spp. in this system. Except for 1 host species, no significant differences in levels of infectionwere found between the 2 species of Haematoloechus in anisopterans. Haematoloechus longiplexus was a secondintermediate host specialist, being found in anisopteran odonates only. In contrast, Haematoloechus complexuswas a generalist and was found in both anisopteran and zygopteran hosts. Differences in infections among hostspecies suggest that variations in odonate ecology are sufficient to influence the suitability of larval odonates toserve as intermediate hosts for these frog trematodes.

KEY WORDS: Halipegus spp., Haematoloechus longiplexus, Haematoloechus complexus, odonate, host spec-ificity .

Bush et al. (1993) argued for the increased con-sideration of invertebrate intermediate hostswhen investigating parasitic helminth commu-nity dynamics. Traditionally, vertebrate defini-tive hosts have received most of the attention inthese analyses (Esch et al., 1990), although com-munity studies of intramolluscan trematodeshave received considerable attention recently(Kuris, 1990;Sousa, 1990, 1993; Fernandez andEsch, 199la; Williams and Esch, 1991; Snyderand Esch, 1993; Esch and Fernandez, 1994; Laf-ferty et al., 1994). Few studies have concentratedon parasites in invertebrate second or third in-termediate hosts, i.e., those that have a closerecological association with the definitive host,because the parasites rely on predator-prey path-ways for transmission.

Halipegus occidualis Stafford, 1905, is a hem-iurid trematode that uses odonate (Insecta: Odo-nata; i.e., dragonfly and damselfly) naiads as thirdintermediate hosts. Naiads infected with meta-cercariae are ingested by the green frog, Ranaclamitans, in which the parasites mature in thebuccal cavity under the tongue (Goater et al.,1990). Halipegus eccentricus Thomas, 1939, issimilar to H. occidualis, except that adults ma-ture in the eustachian tubes of the ranid definitivehost. The lif e cycle of H. eccentricus has tradi-tionally been thought to include only 3 hosts,with tadpoles ingesting infected microcrusta-

ceans (the second intermediate host) (Thomas,1939). Thomas concluded that metacercariaewould then reside in the host's stomach until thetadpole metamorphosed into an adult frog, atwhich time the worm would migrate up theesophagus to the eustachian tubes, where it wouldmature and live as an adult (Thomas, 1939).However, unpublished field data from our lab-oratory on the recruitment of this parasite intoits definitive host (R. clamitans) suggest that H.eccentricus metacercariae also can be found inodonates, which presumably act as third inter-mediate hosts. This would make the lif e cycle ofH. eccentricus similar to that of its congener, H.occidualis. Thus, in habitats such as Charlie'sPond, where both congeners could be presentwithin larval odonates, and because they aremorphologically indistinguishable, they are re-ferred to as Halipegus spp. for the purposes ofthis study.

Haematoloechus complexus Seely, 1906, andH. longiplexus Stafford, 1902, are frog lung flukesthat use odonate naiads as second intermediatehosts. A number of previous studies have ex-amined odonates for infections with Halipegus(Willey, 1930; Krull, 1935; Rankin, 1944; Macyetal., 1960; Kechemir, 1978; Goater, 1989; Fer-nandez, 1991) and Haematoloechus (Krull, 1930,1931, 1932, 1933, 1934; Ingles, 1933; Grabda,1960; Dronen, 1975, 1978; Bourgat and Kulo,

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Copyright © 2011, The Helminthological Society of Washington

2 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 63(1), JAN 1996

1979). However, these efforts predominantly havebeen surveys of odonate naiads as intermediatehosts in lif e history studies. Recently, Snyder andJanovy (1994) examined the second intermedi-ate host specificity for 2 species of Haematoloe-chus and provided experimental evidence of im-portant differences in host specificity between thespecies. However, field evidence for specificityof Haematoloechus spp. in odonates is lacking.

In this paper, we examine the prevalences andrelative densities (as defined in Margolis et al.,1982) of Halipegus spp., H. complexus, and H.longiplexus metacercarial infections in severalspecies of anisopteran (dragonflies) and zygop-teran (damselflies) odonates in relation to thedifferent ecological habits of these hosts. We alsocompare the prevalences and relative densitiesof 2 species of Haematoloechus to investigatewhether strong second intermediate host speci-ficity can be observed in samples of field-col-lected hosts.

Materials and Methods

Odonate naiads were sampled from several siteswithin Charlie's Pond, a 2-hectare pond in the Pied-mont area of North Carolina, U.S.A., from June 1992to June 1993. Because this study was associated witha more extensive investigation of trematode popula-tion dynamics in the definitive host, Rana clamitans,naiads were not sampled in the winter months (No-vember-March) when frogs were inactive and not re-cruiting parasites. Odonates were collected using anaquatic sampling net and a 2-mm2 mesh screen, placedin jars of pond water, and returned to the laboratory.Individuals were isolated at room temperature in 65-ml plastic jars filled with pond water. Naiads wereexamined under a dissecting microscope within 2 daysof capture and identified to species according to Hug-gins and Brigham (1982). All parts of the odonate bodywere examined for metacercariae. Halipegus spp. werealways found in the midgut of the naiads. Haemato-loechus complexus was found in all parts of the body,occurring in a thin, hyaline cyst in the abdominal cav-ity, legs, and head. Haematoloechus longiplexus wasunencysted and was always found associated with thebranchial basket/respiratory structures of anisopteranodonates. Specimens of parasites are deposited in theU.S. National Parasite Collection, Beltsville, Maryland20705, as follows: Halipegus spp. (USNPC 85276),Haematoloechus longiplexus (USNPC 85277), andHaematoloechus complexus (USNPC 85278).

Data used to calculate prevalences were analyzedusing chi-square (Zar, 1984). Relative density data wereanalyzed with an analysis of variance (ANOVA) usingSystat (Wilkinson, 1989). Differences between groupswere determined using Tukey's honestly significant dif-ference (HSD) test. Probability values less than 5% (P< 0.05) were considered statistically significant. In afew instances, relative density data were distributednonnormally and were analyzed with a Kruskal-Wallis

nonparametric ANOVA. Due to the robustness ofANOVA, results from the nonparametric and para-metric tests were consistent; thus, results are reportedonly from the parametric ANOVA for consistency.

ResultsEighteen species of odonates, representing 5

families, were examined (7Y = 934). Those spe-cies with sample sizes adequate for statisticalanalysis are shown in Table 1. Other anisopter-ans that were examined, but not included in Ta-ble 1, were Boyeria vinosa (TV = 6; 4 infected withHalipegus spp., 1 infected with H. complexus)(Aeschnidae), Neurocordulia alabamensis (N =1) (Corduliidae), Cerithemis monomelaena (N =1), Libellula deplanata (N = 2), and Perithemisseminole (N = 2) (Libellulidae). Additional zyg-opterans included Enallagma exsulans (N = 15;4 infected with Halipegus spp., 2 infected withH. complexus), En. signatum (N = 1), and Isch-nura verticalis (N = 1; 1 infected with Halipegussp.) (Coenagrionidae).

Halipegus spp. generally were the most prev-alent of the 3 trematode species (Table 1). Prev-alences ranged from 55% in Epitheca cynosurato 3% in Gomphus exilis, which was significantlylower than in all other hosts (%2 = 47.9, df = 1,P < 0.001). There was no significant differencein Halipegus spp. infection among Ep. cynosura,L. luctuosa, En. traviatum, En. basidens, or Er-ythemis simplicicollis (x2 = 2.28, df = 4, P >0.05); infection with Halipegus spp. in this groupwas significantly higher than in other hosts.Within individual host species, the prevalenceof Halipegus spp. was significantly higher thanthe 2 species of Haematoloechus (P < 0.05) ex-cept in G. exilis (x2 = 1.24, df = 2, P > 0.05)and I. posita (x2 = 0.27, df = 2, P > 0.05), forwhich there were no differences in prevalence ofall 3 trematodes. Likewise, for L. luctuosa therewas no difference between the prevalences ofHalipegus spp. (54%) and H. longiplexus (41%)(X2 = 1.43, df= 2, P> 0.05).

The relative density of Halipegus spp. in Er.simplicicollis was significantly higher than in allother hosts except En. traviatum and Ep. cyno-sura (Table 1; Tukey HSD, P < 0.05). Halipegusspp. generally had the highest relative densitiesof the 3 trematodes within individual host spe-cies as well. There were no significant differencesamong relative densities of any parasite for A.fumipennis, G. exilis, and /. posita. Only in L.luctuosa was the relative density of Halipegusspp. significantly lower than H. longiplexus (t =


Table 1. Total prevalence, relative density, and range of infection of odonate naiads infected with metacercariae.

Halipegus spp.

Odonate (habit*)

Suborder AnisopteraGomphidae

Gomphus exilis (B)Corduliidae

Epicordulia princeps (C, S)Epitheca cynosura (C, S)

LibellulidaeErythemis simplicicollis (S)Libellula cyanea (S)Libellula luctuosa (S)

Suborder ZygopteraCoenagrionidae

Argia fumipennis (C, S)Enallagma basidens (C)Enallagma traviatum (C)Ischnura posita (C)

N

301

6831

9020037

54334150

No.infected

(%)

8(3)

21(31)17(55)

38 (42)76 (38)20 (54)

19(35)15(46)20 (49)10(20)

Relativedensity ± SE

(range)

0.03

0.91.5

2.70.60.9

0.71.01.70.3

± 0.01 (0-2)

± 0.2 (0-9)± 0.4 (0-9)

±0.6 (0-40)± 0.06 (0-4)± 0.2 (0-5)

± 0.2 (0-9)± 0.3 (0-5)± 0.4 (0-10)± 0.08 (0-3)

Haematoloechus longiplexus

No.infected

13(4)

9(13)5(16)

3(3)36(18)15(41)

0000


(range)

0.05

0.20.4

0.080.61.0

± 0.02 (0-2)

± 0.08 (0-4)± 0.2 (0-5)

± 0.05 (0-3)± 0.2 (0-19)±0.3 (0-9)

0000

Haematoloechus complexus

No.infected

11(4)

5(7)5(16)

9(10)32(16)8(22)

7(13)5(15)4(10)8(16)


(range)

0.04

0.70.3

0.30.30.6

0.50.30.30.3

± 0.01

± 0.3± 0.1

± 0.6

(0-2)

(0-1)(0-4)

(0-7)± 0.06 (0-7)± 0.3

±0.2±0.1±0.2±0.1

(0-9)

(0-7)(0-3)(0-7)(0-4)

Ecological habits of odonates: B = burrower; C = climber; S = sprawler.

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JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 63(1), JAN 1996

Table 2. Prevalence and relative density of infection of odonate naiads grouped by the ecological habit of thehost. Only those species having a singular ecological habit designation are included.

Halipegus spp.

Ecologicalhabit

Burrower*ClimberfSprawler̂

N

301124327

Prevalence(%)

2.736.341.0


0.03 ± 0.011.0 ± 0.21.2 ± 0.2

Haematoloechus longiplexw

Prevalence(%)

4.30

16.5


0.05 ± 0.020

0.5 ±0.1

Haematoloechus complexus

Prevalence(%)

3.713.715.0


0.04 ± 0.010.3 ± 0.90.3 ± 0.06

* Burrower = Gomphus exilis.t Climbers = Enallagma basidens, Enallagma traviatum, Ischnura posita.t Sprawlers = Erythemis simplicicollis, Libellula cyanea, Libellula luctuosa.

2.25, df = 72, P < 0.025). There was no signif-icant difference in densities of Halipegus spp. andH. longiplexus within L. cyanea (t = 0.1, df =398, P > 0.05).

Haematoloechus longiplexus infected anisop-teran odonates only (Table 1). For anisopteranhosts, there were no significant differences in ei-ther the prevalence or the relative density of in-fection with H. longiplexus and H. complexusexcept in L. luctuosa. In the latter host species,the prevalence of H. longiplexus (41 %) was sig-nificantly higher than that of//, complexus (22%;X2 = 3.1, df = 1, P < 0.05). Similarly, the relativedensity of//, longiplexus was significantly higherthan for H. complexus (t = 6.11, df = 72, P <0.001).

In contrast to its congener, H. complexus in-fected both anisopteran and zygopteran odonates(Table 1). The prevalence of//, complexus in allspecies of zygopterans was lower than that ofHalipegus spp. except in /. posita (x2 = 0.27, df= 1, P > 0.05). There were no significant differ-ences in relative densities of infection with //.complexus and Halipegus spp. for /. posita (t =0.51, df = 98, P > 0.05) and A. fumipennis (t =0.88, df = 106, P > 0.05). However, there weresignificantly lower densities of//, complexus thanHalipegus spp. in En. basidens and En. traviatum(Table 1; Tukey HSD, P < 0.05).

There were no significant differences in theprevalence (x2 = 0.74, df = 1, P > 0.75) or rel-ative density (t = 1.48, df = 448, P > 0.5) ofinfection with H. occidualis between sprawlingand climbing odonate species (Table 2). Like-wise, there were no significant differences in theprevalence (x2 = 0.09, df = 1, P > 0.9) or relativedensity (t = 0.22, df = 449, P > 0.5) of infectionwith H. complexus between these groups. Whenthe sprawling and climbing habits were pooledand collectively compared with levels of infec-

tion of the burrowing habit (i.e., G. exilis), therewere highly significant differences in both theprevalence and relative density (respectively) ofinfection for H. occidualis (x2 = 133.0, df = 1,P < 0.001; t = 8.4, df = 750, P < 0.001), //.longiplexus (x2 = 32.1, df = 1, P < 0.001; t =5.3, df = 626, P < 0.001), and H. complexus (x2

= 24.1, df = 1, P < 0.001; t = 3.3, df = 750, P< 0.001).

Discussion

Halipegus spp. generally had the highest prev-alences and relative densities of infection whencompared with Haematoloechus spp. in this sys-tem. The prevalence of Halipegus spp. rangedfrom a high of 55% in Ep. cynosura to a low of3% in G. exilis, a species that consistently hadlow prevalences and relative densities of all 3parasites. Of all the species that were sampled,Gomphus exilis is the only burrower; i.e., thenaiads burrow beneath the surface of the pondbottom mud, sand, or sediment (Huggins andBrigham, 1982). This lif e style or ecological"habit" would seem to restrict predation by thisspecies on large numbers of infected ostracods(in the case of Halipegus spp.) or to reduce ex-posure of the host to the motile cercariae ofHae-matolochus spp., relative to the other species ofodonates. In contrast, all other odonate specieshad prevalences of Halipegus spp. that were atleast 20%. These species represent 2 other eco-logical habits: climbers (A. fumipennis, Enallag-ma spp., /. posita, Ep. cynosura) and sprawlers(Epi. princeps, Er. simplicicollis, Libellula spp.)(Huggins and Brigham, 1982). Climbers are ac-tive predators that stalk their prey when foraging.Sprawlers are ambush predators, sitting andwaiting for prey to move close to them (Hugginsand Brigham, 1982). Species representing theselatter 2 habits have relatively greater exposure


WETZEL AND ESCH-TREMATODES IN ODONATE INTERMEDIATE HOSTS

to the water column, including infected ostracodsand motile cercariae.

There were no significant differences in pat-terns of infection between climbers and sprawl-ers. However, when collectively compared withthe burrowing habit, the climber and sprawlerhabits had significantly greater prevalences andrelative densities of infection of all 3 species oftrematode. In light of this, we suggest that theecological habit of the intermediate host mayreflect real biological limits with respect to whichspecies may play an important role in the dy-namics of the parasite's lif e cycle. Given that allof these species were clearly susceptible to infec-tion (notwithstanding the absence of //. longi-plexus from zygopteran hosts), we feel that thedifferences in levels of infection among host spe-cies were primarily due to ecological/habitat de-terminants rather than patterns of host phylog-enies (Bush et al., 1990). Thus, because of thesometimes large differences in levels of infectionbetween hosts representing different ecologicalhabits, care must be taken when generalizationsare made with respect to a particular host "group."For example, Dronen (1978) examined severalanisopteran and zygopteran odonate species,treating them as a single group because they re-portedly served equally well as second inter-mediate hosts for H. coloradensis (=H. corn-plexus; Kennedy, 1981). However, inspection ofthe present data suggests there is substantial vari-ability in the suitability of a particular species asa host. Furthermore, much of this variability canbe attributed to simple differences in the ecolog-ical habits of the hosts. When considering //.longiplexus, for example, treating both anisop-teran and zygopteran odonates as a single groupwould have a serious impact on the assessmentof prevalence and relative density of infection,given the strong specificity of this parasite foranisopteran naiads. Clearly, ecological habits ofintermediate hosts must be considered when ex-amining patterns of infection at the level of thecomponent community.

Differences in host specificity were observedbetween H. longiplexus and H. complexus. Hae-matoloechus longiplexus infected only anisop-teran odonates, whereas H. complexus infectedboth anisopterans and zygopterans. The appar-ent restriction of H. longiplexus to anisopteransin this system is in contrast to the work of Krull(1932), in which he described this species as oc-curring in the zygopteran Lestes vigilax. As wehave no reason to doubt the experimental infec-

tions of Krull (1932), this discrepancy suggeststhat levels of host specificity may be more finetuned than at the level of taxonomic suborders(i.e., anisopteran vs. zygopteran hosts). BecauseLestes sp. does not occur in Charlie's Pond, po-tentially susceptible zygopteran hosts may not bepresent in this system. These differences also im-ply that regional differences in invertebrate in-termediate host use may exist.

Except for 1 host species (L. luctuosa), therewere no differences in either the prevalence orrelative density of infection with H. longiplexusand H. complexus in anisopteran hosts. The sim-ilarities between the 2 congeners are interestingbecause the patterns do not reflect those seen atthe level of the first intermediate hosts. In Char-lie's Pond, H. complexus occurred in over 15%of Physa gyrina, its first intermediate host (Sny-der and Esch, 1993). In contrast, H. longiplexusinfected less than 1.5% of the snail Helisomaanceps for any given month (Fernandez and Esch,1991b). We recognize that differences of this sortcould be a result of different population sizes ofthe first intermediate hosts, but as populationdensities of the snail species have not been es-timated, no conclusive comparisons are possibleat this time. Instead, we suggest that despite thegreater prevalence of H. complexus in its firstintermediate host (P. gyrina), the similarity inthe levels of infection with H. longiplexus andH. complexus in their second intermediate hosts(odonates) is a function of differing host speci-ficities of these parasites.

Recently, Snyder and Janovy (1994) demon-strated that H. complexus is a second interme-diate host generalist; this trematode was able toinfect 9 arthropod species (representing 2 sub-phyla and 3 insect orders) exposed to cercariae.Whereas they did not test H. longiplexus in theirstudy, a pattern similar to H. longiplexus wasseen with H. medioplexus: it too infected onlyanisopteran naiads (Snyder and Janovy, 1994).They suggested that anuran definitive hosts mighthave a better chance of ingesting a food iteminfected by the generalist (H. complexus) becausethis parasite can infect a wider range of preyitems. Using this logic, we suggest that, given afinite number of cercariae shed by an infectedsnail, a generalist parasite species would be ex-pected to have a lower prevalence of infection inany particular second intermediate host specieswhen compared with a parasite that was a spe-cialist on that second intermediate host species.Assuming that H. complexus uses several other


JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 63(1), JAN 1996

aquatic arthropods in Charlie's Pond, we pro-pose that the similarities in infection of anisop-teran odonates with H. longiplexus and H. corn-plexus in this system are created by the "dilu-tion" of cercariae of H. complexus into othertypes of hosts (e.g., zygopterans). This would ef-fectively counterbalance the initially large dif-ference in prevalences of these parasites in theirfirst intermediate hosts. Thus, the anisopteran-specialist H. longiplexus may be as prevalent inanisopteran hosts as the generalist H. complexus,despite the cercariae being shed from a muchsmaller proportion of its respective snail host.

Despite the variable levels of infection amongodonate species, which, in this system, can beattributed primarily to different ecological hab-its, it does appear that a wide variety of the odo-nates could serve as suitable intermediate hosts.Al l of the trematodes in the present study areactively recruited by, and mature in, ranid frogs.Which odonate species act as the primary inter-mediate hosts in this system remains unknown.Presumably, species such as Er. simplicicollis andL. cyanea play an important role in the trans-mission dynamics of these parasites; they areabundant in the pond and have relatively highprevalences and relative densities of infection.For example, up to 40 metacercariae have beenobserved in 1 individual of Er. simplicicollis,which, if ingested by a frog, could represent an"instant" infrapopulation in the definitive host.On the other hand, the burrowing G. exilis, al-though abundant in the pond (representing 32%of individuals sampled), consistently had thelowest levels of infection of any host sampledand thus would not be expected to contributegreatly to the transmission dynamics of thesetrematodes. Nevertheless, given the potentiallylarge number of hosts that could be used, theseparasites may be successfully "hedging their bets"against barriers to transmission and local ex-tinction (Bush and Kennedy, 1994).

AcknowledgmentsWe thank S. Wetzel and 3 anonymous review-

ers for their comments on earlier versions of thispaper. Publication of this paper is supported bya grant from the Wake Forest University Re-search and Publication Fund.

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ERI C J. WETZEL AND GERAL D W. ESCH · within Charlie's Pond, a 2-hectare pond in the Pied-mont...

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