Faunal survey. II. The distribution of digenean trematodes within the New England Tablelands

2004·2.1 MB·English

FAUNAL SURVEY. THE DISTRIBUTION OF DIGENEAN TREMATODES WITHIN
11.
THENEWENGLAND TABLELANDS
MAREEKOCH
Koch,M.20040630.Faunalsurvey. II.Thedistributionofdigeneantrematodeswithinthe
NewEnglandTablelands. MemoirsoftheQueenslandMuseum49{2): 659-664. Brisbane.
ISSN0079-8835.
Trematode larval stages collected fromaquatic snails across theNew England Tablelands
were examined and identified through morphometric analysis and where possible,
transmissionexperimentsand28S(LSU)rDNAanalysis.Onemonostomeandthreedistome
digeneantrematodespecieswerefoundinpopulationsofGabbiavertiginosa(Bithyniidae).
OnedistomedigeneanwasfoundinthesnailGlyptophysasp.(Planorbidae).Theprevalence
ofalltrematodespecieswaslowandtheirdistributionslimitedtothecentral portionofthe
NewEnglandTablelands.Temporal andspatial heterogeneitywithinbothintermediateand
definitivehostpopulationsmaybeactingasisolatingmechanismsattimesofrecruitmentof
larvaltrematodes, limitingparasitedistributionalrangesthroughdisruptionoftheirnatural
transmissioncycles. Trematode,Notocotylidae,Echinostomatidae,Heterophyidae,distribution.
MareeKoch, SchoolofBiological, Biomedical& MolecularSciences, UniversityofNew
England, Armidale2351, Australia (email: [email protected]); 1March2003.
METHODS
Aquaticsnails collectedduringasurveyofthe
New England Tablelands, New South Wales,
between February 2000 and 2003 (Koch, 2004)
The Australian Biogeographical Integrated
were examined for larval stages oftrematodes. Grid System (ABIGS) was used to map all
Typically, such parasites utilise molluscs as species, in accordance with Brook (1977) and
intermediatehostsin twoorthree-hostlifecycles Simpson & Stanisic (1986). Aquatic snails were
(Ginetsinskaya, 1988). Sporocyst, redia, cercaria collected as described by Koch (2004). Snails
and metacercaria stages of trematode were dissected within 24 hours ofcollection by
developmentcanbefoundinbothterrestrialand crushingoftheshellandthetissueexaminedina
aquatic snails, with adult parasites maturing cavity block under a dissecting microscope for
withinadefinitivevertebratehost(Rohde,2001; live trematodes. Trematode specimens were
Haas & Haberl, 1997). Traditionally trematodes fixed in either 10% hot formalin or hot saline
havebeenidentifiedtogenusandspecieslevelby (8.5g NaCl per 1 litre distilled water), stained
obtaining a mature adult worm either by with either Grenacher’s carmine alum or
dissection out ofa natural vertebrate host or by acetocarmine, dehydrated in an alcohol series,
andmountedinCanadabalsam. Slideswerethen
completing life cycle experiments utilising the dried in an oven at 66°C for 14 days (Conn,
larval forms obtainedfrom snails collectedfrom DNA
1946). Specimens required for sequencing
a natural habitat (Gibson, 1998; Wright, 1971). were dropped immediately upon dissection into
Wheneverpossible,suchtransmissionexperiments absolute alcohol (Jousson et al., 1998).
wereattemptedthroughoutthissurveyperiod. In Identification oftrematodes was done primarily
additiontothetraditionalidentificationmethods, by obtaining adult worms through life cycle
partialsequencingofthe28Slongsubunit(LSU) experimentswheneverpossible, and secondarily
rDNAtakenfromlarvaltrematodesfoundduring throughpartialsequencingofrDNA28S LSU by
dissections of snails was undertaken at the OlsonandLittlewood.Inallothercases,cercarial
Natural HistoryMuseum, London), (Olsonetal, andrediallifestageswereusedtoidentifyspecies
2003; Littlewood & Olson, 2001). to family and/orgenus using publishedresearch
papersandkeys(Yamaguti, 1971, 1975;McDonald,
Theaimsofthesurveyweretoidentifytrematode 1981)- Intensity was defined as the number of
species across the New England Tablelands; to cercariae observedwithin the snail tissues atthe
establish their distributional ranges; and to timeofdissection(high:>100cercariaepersnail;
identifythe aquatic snails beingparasitised, and medium: 50-100 cercariae per snail; low; <50
thereby determine intermediate hostspecificity. cercariae per snail). Prevalence was defined as
MEMOIRS OF THE QUEENSLAND MUSEUM
660
FIaGGua.sbtbr1ai.laCisovmenr.ptasiprg.ii;nsEoo,snaA.socAfo,ccoGu.tryrvelenerttsipd.giisnntoorvsi.abu(;tAiBoB,n—IaCGlatSraastnrygoseptsiesmoifgnrdtiirdceusmsua;pteCor,diePmshpiwolisotephdthotavhaletmruotshfestpNh.eeinrwovi.En;ntgDel,ramEencddhiraietngeoiposannarwiyilpthhhoitsuhtm,e
surveyedareaenclosedbythesoliddots seeKoch,2004)
the percentage of snails collected that were oftheLSU28SrDNAofadultwormsagainst 150
infectedby treniatode larval stages. digenean taxa confirmed the identity ofEchino-
PhotographsweretakenusinganOlympusBH2 pacacreyspsihoinunmumabuestrraAlYi3s95s5p.77n)ova.nd(GC.enienbdiacnuks
cameraattachedtoastereomicroscope,orusinga (Genebank accession numbers AY222114,
digital camera attached to a Nomarski contrast AY222220). PCR products could not be
microscope.Digitalphotographsweredownloaded generated for any other trematode species.
intoAdobePhotoshopprogramforediting. Body Attempts to obtain adults ofPhilopthalmus sp.
parts were measured with a calibrated eyepiece nov. ?indAscocotyde sp. nov. failed.
graticule.Measurementsaregiveninmillimetres.
The rediae and cerctiriae ofC indicus always
RESULTS occurred alone within the gonad tissue of G.
vertiginosa. However, the otherthree trematode
Twosnailspecieswerefoundtobeparasitised. species were found as concurrent interspecific
TlieprosobranchGabbiavertiginosa(Bithyniidae) doubleandtripleinfectionswithin G vertiginosa,
washostto 1 monostomeand3distomedigeneans: all utilising gonad and digestive gland tissues.
Catatropis indicus (Notocotylidac), Echino- Philopthalmussp. nov.establishedinfectionfirst
paryphiumaustralissp. nov. (Echinostomatidae), withinthesnail.RecruitmentoiEchinoparyphium
Philopthalmus sp. nov. (Echinostomatidae), and australis sp. nov. and Ascocotyle sp. nov.
Ascocotyle sp. nov. (Hcterophyidac) (Figs 1-3). followed inthatorder.
AdultwormsofC. indicus2LndEchinoparyphium
australis sp. nov. were obtained from life cycle Glyptophysa sp. (Planorbidae)washosttoone
experiments(Koch,2003).Phylogeneticanalysis distome digenean, Echinostoma sp. nov.
.
DIGENEAN TREMATODES OF THENEW ENGLAND 661
Morand, 1999). Seasonal
migrationandothermovements
across and between habitats by
final hosts such birds can re-
moveoraddhostsfromortothe
specific preferences ofparasite
species. By adding to the
habitat, the opportunity for
completionofalifecycleinone
or more final hosts by one or
more parasite species is greatly
enhanced. Conversely, the
departure ofa final host from a
particularhabitatmaycausethe
loss(seasonallyorpermanently)
FIG 2. Comparison ofcurrent distributional ranges ofEchinostoma sp. of one or more parasite species
nov.with thatofits intermediatesnail host, Glyptophysasp. due to the interruption of the
natural cycle of transmission
(Echinostomatidae) with rediae and cercariae between intermediate and definitive hosts
occurringin digestive gland andgonadtissue of (Combes et al, 1994; Kuris & Lafferty, 1994).
thesnail(Figs2& 3E). Itwaspresentinthesnail Such temporal pulses in host populations will
population during all seasons, across all years. bring about pulses in parasite populations
Adultwormsofthisspeciescouldnotbeobtained actively associated with those hosts (Smith,
throughtransmission e.xperiments. 2001).Aninferencecanbedrawnfrommystudy
C. indicus waspresentinthesnailpopulations ofadegreeoftemporalvariation inbothparasite
at all seasons across all collection years. The and intermediate host populations between
three distome species specific to G. vertiginosa, seasons as indicated by the presence ofdistome
however,werepresentonlybetweenJanuaryand species in G. vertiginosa only in mid and late
April of all collection years. Intermediate host summermonths. Publishedrecords shownatural
specificity was high for all trematode species as final hosts ofthe Echinostomatidae and Hetero-
demonstrated by the use ofasingle hostspecies phyidae to be commonly waterbirds such as
and failure ofparasites to establish infections in ducks, herons, and egrets (Kanev et al, 1998;
other aquatic snail species during transmission Yamaguti, 1975). These species are mostly
experiments performed and described by Koch nomadic birds that are found abundantly across
(2003).Prevalenceandabundanceofalltrematode the Tablelands during the summer months,
species are summarised in Table 1 moving towards the warmer coastal or inland
Detaileddescriptions ofparasite anatomy and areasforwinter. Suchmigrationpatternscan link
habitats and thus parasite communities of
life cycles, andtransmissionexperiments canbe
found in Koch (2002, 2003). intennediate hosts creatingpulses in prevalence
in both parasite and intennediate host populat-
DISCUSSION ions across time (Smith, 2001). There was a
consistency in my study, however, of the
Many studies have presented data to support presence of all parasite species across years,
the hypothesis that temporal heterogeneity indicatingonlyseasonalisolationofspecieswith
within both definitive and intermediate host in habitats as opposed to complete removal of
populations can bring about the isolation and species.
even removal of a parasite species from the
environmentwhen the chronologicalpatterns of Spatial heterogeneity in parasite recruitment
activityofthe hostsare inopposition eitherwith due to geographical isolation of snail host
theparasiteoreachother(Al-Kandarietal,2000; populations and possible definitive host habitat
Kuris & Lafferty, 1994; Crews & Esch, 1986; preferences may be responsible for the patterns
Cort et al, I960). The trematode life cycle has and seasonality ofparasite distributionalongthe
evolvedaroundthisvariationinbothintermediate central sectionoftheTablelands. This areahas a
and definitive host habitat usage, and the inter- high concentration ofnatural watercourses that
playoftemporal behaviourpatterns ofboth host attract water bird species and provide suitable
and parasite (Poulin, 1999a; 1999b; Poulin & habitats for first and second intermediate hosts
662 MEMOIRS OF THE QUEENSLAND MUSEUM
FIG 3. Trematode species found during the survey of aquatic gastropods ofthe New England region. A,
Catatropis indicus adult(SEM); B,Philopthalmus sp. nov. Cercaria; C,Echinoparyphium australis sp. nov.
Aadu&lt;CD=, A1smcmo;coBtyAleEsp.=n2o0v.pmc.ercariawithclose-upoftailfinfold;E,Echinostomasp.nov.cercaria. Scalebars-
DIGENEAN TREMATODES OF THENEW ENGLAND 663
TABLE 1. Prevalences ofinfectionoflarvaltrematodeswithinaquatic snail populations oftheNew England
Tablelands.
Parasite Prevalence Intensity SnailHost
Catatropisindicus 3.5%(5240) high Gabbiavertiginosa
Philopthalmussp.nov. 0.90%(5240) high Gabbiavertiginosa
Echinoparyphiumaustralissp.nov. 0.30%(5240) medium Gabbiavertiginosa
Ascocotylesp.nov. 0.08%(5240) low Gabbiavertiginosa
Echinostomasp.nov. 85%(47) high Glyptophysasp.
suchassnails,fishandfrogs(Douglas&Douglas, infectionofapopulationofCerithideacingidata
1977). Therearealsomanyman-madedamsand by larval trematodes in Kuwait Bay. Journal of
swamps,someofwhichdonotsupportthediversity Helminthology74: 17-22.
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these habitats dry up for three to five months CONN,H. 1946. BiologicalStains: ahandbookonthe
every year, concentrating snails and final hosts nature and uses of the dyes employed in the
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mayactaspotentialisolatingmechanismsoccurring CORT, W.W., HUSSEY, K.L. & AMEEL, D.J. 1960.
attimesofrecruitmentofparasitesandpeaksnail Seasonal fluctuations in larval trematode
hostreproductiveperiods, inthesummermonths infections in Stagnicola emarginala angulata
of October through to April. All trematode from Phragmites Flats on Douglas Lake.
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