1. Porostsot.. 93(5). 2007, PI' 999-1005 © American Society of Parasitologists 2007

HABITAT AND HOST SPECIFICITY OF TREMATODE METACERCARIAE IN FIDDLER FROM HABITATS IN FLORIDA

Nancy F. Smith, Gregory M. Ruiz*, and Sherry A. Reedt Galbraith Marine Science Laboratory, Eckerd College, 4200 54th Avenue South, St. Petersb urg, Florida 33711. e-meit: smilhnf@eckerdedu

ABSTJ

Trematodes target a diverse suite of second intermediate elevations or soils within mangrove and salt marsh habitats hosts both taxonomically (e.g., , molluscs, annelids) (Teal, 1958; Macnae. 19(8). Such habitat selection is influenced and ethologically (benthic, pelagic, sessile) (Combes et al., by their sediment preferences and their ability to osmoregulate 1994). Although trematodes often use many different species (Teal, 1958; Hartnoll, 1987; Thurman, 20m; Ribeiro, 2(05). as second intermediate hosts, some host species are infected Furthermore, parasitism by trematodes varies among fiddler more frequently, or at higher intensities than other host species, crabs, with some Uca spp. more readily parasitized than others or both (Bush et al., 1993). This pattern may occur because (Heard, 1976). In mangrove habitats of Florida, differences in some hosts are more frequently in contact with the infective parasitism also exist among Uca spp. (N. Smith, pers. obs.), stages than other hosts, they behave in ways that can increase Such differences may reflect their ecological or physiological or decrease their risk of parasitic infection, they vary in their preferences to occupy certain microcnvironments within man­ ability to provide metabolic resources necessary for parasite grove habitats, thereby affecting their risk of infection. Differ­ development, or they vary in their immunological ability to ences may also arise from the specificity of parasites to infect eliminate their parasitic infection (Adamson and Caira, 1994; certain species of Uca more readily than others. Combes, 200 I; Kirchner and Roy, 200 I). To address the issue of ecological or host specificity, we ex­ The role of habitat and habitat structure on the distribution amined populations of 3 species of fiddler crabs tU. speciosa, of parasites among and within intermediate host populations U. rapax, U. thayeri) for trematode metacercariae across a hab­ can play an important role in influencing the probability of con­ itat gradient. These populations overlap in their distribution OIl tact between the parasite and potential host (Sousa and Grosh­ the banks of mangrove-dominated swamps, a habitat that varies olz, 1991). For example, Lafferty et al. (2005) showed that in elevation, tidal influence, and soil composition. Here, we prevalence of trematodes in snail intermediate hosts was higher present data on the d istribution of the syrnpatric fiddler crabs in habitats with vegetative cover, compared with mudflats. sug­ within this habitat gradient, and the prevalence and abundance gesting that parasite transmission is higher in habitats that sup­ of their trematode rnetacercariae. We found that U. speciosa port more final hosts (Hoff, 1941; Robson and Williams, 1970; was more frequently and heavily parasitized by Probolocoryphe Sousa and Grosholz, 1991; Esch et al., 1997; Smith, 200 I; lanceolata compared with other species tU, rapax, Hechingcr and Lafferty. 2(05). Similarly, Skirnisson et al. U. thuveri). To better understand these differences in parasitism, (2004) found that trematode infections in mud snails were at­ we conducted a field experiment to test whether U. speciosa, tributed to the habitat use of salt marsh ponds by bird final which inhabits the lower intertidal zone, has a higher risk of hosts. Physical factors such as turbulence and storm events can trematode infection than U. rapax, which lives relatively higher also influence the temporal and spatial distribution of infective in the intertidal zone. For this, U. speciosa and U. rapax were stages in the water column, thereby affecting patterns of infec­ exposed to shedding cercariae while raised under identical en­ tion in subsequent intermediate hosts (Fingerut et al., 2003). vironmental conditions. In subtropical coastal communities, the zonation of man­ groves, which is linked to changes in elevation, tidal influence, MATERIALS AND METHODS and environmental factors (Macnae, 1968; Lugo and Snedaker, Study system 1974), has the potential to affect parasite transmission by af­ Our study was conducted at 2 mosquito impoundments, Impound­ ... fecting the spatial distribution of potential hosts. For example, ment 12 (21-ha marsh), Indian River Co. (2r33'45"N, 80020'W), and certain species of fiddler crabs (Uca spp.) dominate particular Impoundment 23 (In-ha marsh), St. Lucie Co. (2r32'30"N, 80020'W), Florida. both located on North Hutchinson Island. a barrier island lo­ cated between the Indian River Lagoon (IRL) and Atlantic Ocean. Both Received 17 November 2006; revised 9 April 2007; accepted 10 April impoundments were constructed in the 1960s to control populations of 2007. the marsh mosquito (Aedes taeniorhvnchus, Ae. sollicitans) and sandtly "' Smithsonian Environmental Research Center, 647 Contees Wharf (Culicoides jurens) (Rey and Kain, 1989). Impoundments were created Road, Edgewater, Maryland 21037. by excavating and depositing sediment around the perimeter of the t Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort marsh and then enclosing the marsh with a channel (1-3 m depth) and Pierce, Florida 34949. earthen dike (3-5 m wide). Culverts placed at various locations under

999 1000 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO.5, OCTOBER 2007

the dike allow free exchange of water between the IRL and impounded Field experiment: Host specificity of metacercariae marshes . The ha nks along the exc avated channel are dominated by a thick stand mixture of red mang rove iRhizophora mangle ) and black Differenc es in prevalence and intensity of metacercariae among fid­ mangrove (A vicennia germinuns), The substratum near the shoreline is dler cra b speci es from o ur surv eys prompted us to test whether host loose and mudd y, anti it becomes more compact and sa ndy tow ard the speci ficity was largel y respon sible for the diffe rences obse rved. Specif­ upper intertidal. Fiddl er crabs arc abunda ntly distributed in the sediment reall y, V . speciosa. which is more abundant in the low anti mid intertidal amo ng the mangrove prop roots and pncu rnaroph ores. zo ne, exper ience d higher prevalence and intensity of P. lance olatu Th ree spec ies of fiddler crabs were ex amined for trem atode mctacer­ mct ucercariac than the other fiddler nabs species (see Result s). We curiae. including the lougfinger Iiddler, U. spccioso ; the Caribbean fid ­ co nducted a tran splant ex periment to determine whether U. sp eci os« dler. U. rapax: and the mangrove fiddler, U. thaveri. In Florida. U. has a higher risk of trematode infection to P. lan ccolata than U. rapax sp cciosa occ urs from Yen> Beach to the Florida Keys, U. rapax OL'CurS as a result of its habitat preference for the lower half of the intertidal from Dayton a Beach to the Flo rida Keys. anti V . thuvcri occurs from zo ne. To control for habitat hetero gen eit y (elevation. tidal gradient, soil St . Au gu stine to Sarasota (Tas hia n and Vcmbcrg. 195 H; Salmon, 190 7). co mpos itio n) and ex pos ure to shedding cercariae, tiddler cra bs we re Man y species o f fiddler crabs of the Caribbea n anti North America have transplant ed to another site within Im poun dm ent s 12 and 23 . whe re the bee n shown to he parasitized by lar val trem atodes (Heard, 197 0; Dunn first inter medi ate host, C. scalarifo rm is, is known to occur; et al.. 1990 ). Of 8 species of tidd ler cra bs ex amined by Hea rd ( 1976) Enclosu res were constructed to co ntine and ex pose V. sp eciosa and in sa lt marshes along the north ern Gul f o f Mexico , 6 were naturall y U. ,:apax to sheddi ng cercariae from the surro unding infected snai l pop ­ infected with I to 5 species of trematodes. In addition to trem atodes. ulatio ns anti to standardize their habi tat environme nt so that tida l ele ­ fiddler crabs (V. rapax) from the cast coast of Florida have also heen vation and sediment composition wer e identical amo ng enclosures . Par­ sho wn to be infected by 2 species of larv al acunthoccpha lans (Ni ckol allel studies on parasitism in C. scalurijonnis showed that prevalence ct al.. 2002). ~ f P. lan ce olata was 26 and I C/r at Imp oundments 23 and 12. respcc­ T he ladder hom snai l. Cerith idca scalarifo rm is (Say, 1(25 ). co -oc­ tivcly. Enc losures we re con structed of 4-mm Vcxar ny lon mesh walls. curs with fiddler crab population s. where they inhabit the man grove suppo rted by woo den stakes. All enc losures we re co nstruc ted with bot­ frin ge of creeks and mudflats. grazing on detritu s and algae. Ceril /lidea tom s and covers (uu ached via cable ties) to prevent fidd ler crabs from scala ri jormis ser ves as the Ii I'S! intermediate host to several species of escaping and ente ring enclosu res. Th e enc losures we re buried to a depth larval trem atodes (Holliman . 1961 : McNeIT. 1978 ; Smith, 200 1), l of 01 15 em anti rose to a height of 62 em abo ve the sedime nt surface. which (P. lanceolata ) infe cts Uru spp. (Heard, J(70). Snails become providin g a surface area of 0.25 m- for burrowin g and feeding. infected after ingesting a P. lan rcolaia egg containing a miracidium. Five enclosures, plac ed 25 m apart, were placed at each site. On 8 The miracidium metam orphoses into a sporocyst and then und ergoes Augu st 1994. 50 (25 males and 25 fema les) U. speciosa and V. rapax ase xual rep roduction. producing a large population of sporocysts in the wer e co llected along the man gro ve intertidal in Impoundment 23 and gona d. Free-swi mming ce rca riae arc released from sporocysts and the transplanted to eac h site. Eac h enclosure was stoc ked with 5 individ ual sna il hos t, and then they ent er the bra nchia l cavity of fiddler cra bs. crabs of each species. rantloml y distributed with respect to size and sex. Mctacercuriac enc yst in the hepatopunc rcus. und trema todc deve lop me nt for a tota l of 10 crabs per enc losure . T his den sity is within the runuc is co mpleted when infec ted crabs are inges ted by a crab-eat ing mammal typicall y observed for tiddler cra bs that inh abit these sites. Two weeks or bini (Heard and Sikora, 1969: Heard , 1976; Mc Neff, 1(78). Ot her before the ex perime nt was initialed. prel iminary sa mples of fiddl er crabs potential first intermediate hosts were not exu mined in this study. from Impoundment 23 were colle cted to det ermi ne what size range sho uld be used for the ex perime nt. Fiddl er crabs with a carapace width under 13.0 n1l11 had low prevalence and mean intensity ( :!: SD ) of P. Fiddler crab distribution in the mangrove intertidal zone lan cc olata (V. sprciosa: prevalence 38'(,", mean intensity 2.30 :!: 3.7: L!'.rapax: preva.lencc O'ii.) . Because future infecti ons and host suscep­ . To exa mine the spati al distributi on of fiddler crabs alone0 a man0 arove- line d ba nk, 5 para llel transect s (20 m apart, 2 m long) were established tibility may be influenced by the presence of existing parasites. using perpen dicular to the shore line along a channe l in Impoundment 23 . At crabs that are likely to have a low abundance of meta cereariae can eac h tra nsect, 0.25- m' quadrats were taken at 3 elevations (low inter­ reduce these con foundi ng effects. T hus. we used tiddler crabs with a tidal , mid interti dal, hig h intert idal). spread approxi mate ly 0.25 m apart, carapace width of R.O-12.9 mrn for our experime nt. After 2 mo, so me of the fiddler crabs tran spl anted to the 2 sites had died from drown inu during a neap tide on 29 August 1994. Co llec tions were made by plac­ ~ ing a metal frame over the marsh surface and excavating all burrows due to the unexpected high tides that occurred that summe r. forcing within the quadrut. Fiddler crabs were identifi ed anti kept"separated by to termi nate the ex periment. After 72 days of bein g raised under iden­ quadrat until examined for trem atodes (sec trematode survey below). tical held conditions. fiddler crabs were co llected from the enclosures Fiddler cra b abunda nce (meas ured as number of crabs per 0.25 m-) was and assayed for P. lan ceolat a . Becau se the number of live cra bs varied com pared am ong the 3 intert ida l zones by a Kru skal-Wallis test (esti­ among enclosures, we randomly se lec ted 12 crab s of eac h spec ies from mated by a chi-sq uare). because data did not mee t ass umptions for each site . We calcula ted prevalence (pe rce ntage of infected cra bs in eac h parametric tests. sampl e) and mea n intensity (mea n nu mber of metacercuriae per infected cra b host in eac h sample) for each trem atod e species and field site (Margolis et al., 1( 82 ). Parasiti sm data did not meet the ass umptions Trematode survey ot parametric tests . c.g .. normality or homogeneity of variance; thu s. the Wilcoxon signed rank test was used to test for differences in prev­ Three species of fiddler crabs co llected from the mangrove habitats alence and intensity of P. lan ccolatu infe ction between V. sp cci osa anti we re assayed for trematode rn ctuccrcariue. inc ludinu cra bs co llec ted U. 1'''1'11.1". Sample sizes wer e too low to a llow us to co mpare difference s from Impoundment 23 (as de scr ibed above) and Impoundment 12. At in parasitism by sex. A ll statis tica l analyses were co nducted using Sta­ Impoun d ment 12, tidd ler crabs were collected by pitfall traps over 4 tistical Ana lytica l Software, vers ion 8.0 (SAS Institute, Ca ry. No rth consecutive days in August 1994 by placi ng appro ximately 25 .5-cm Carolina). plastic co nta iners in the gro und so that the upen end of the co nta iner was flush with the marsh surface. Here, co llec tions were co nducted in a mudflat with sca ttere d ma ngro ves, near the impoundment channe l RESULTS with all pitfall traps positioned at the sam e elevation. For both sites, the carapace width (millimeters) of each fiddler crab was me asured to ex­ Fiddler crab distribution in the mangrove intertidal zone am ine the relationsh ip between host size and para sitism , becau se size may influ ence infection ri sk . Fidd ler crabs were kept alive unt il dis­ Uca speciosa s ig n ifican tly varied in a bu ndanc e among the 3 sected for metaccrcuriac. All so ft tissue s we re thoroughl y ex am ined, zone s (X' = 7 .6 2, P < 0 .(5 ), w ith m ore c ra bs in th e lo w a nd and mctucercariac from infec ted crubs were counted and ide ntified. We m id intertidal zones c ompared w ith the hi gh int ertidal (F ig . IA). ass umed that metacerc ariac occu rring in large masses in the sa me tissue , seeming morphologicall y identical. represent ed the sa me spec ies. For Add itionally . U. speciosa represented a g reate r proportion of identifi cation purposes. metu cercariae wer e excystcd by incubating cys ts quad rat sample s in the lo w and m id inte rtidal zones rel ative to In a saline water bath at 40 C for several hours. the o the r species (Fig. IB ). Howe ve r, there were no di fferences SMITH ET AL.-·-TREfvIATODE METACERCARIAE IN FIDDLER CRABS 1001

10 A c::::::J { 'e ll .'l}('C/(!SI/ in the density of U. rapax or U. thayer! among zones (U. rapax: "!- t :C1J rllplJX X2 = 4.52, P > 0.05; U. thayeri: X2 = 1.49, P > 0.05; Fig. lA), C tca ';/(/\'('1"/ on although U. rapax was the most abundant species in the high N 8 0 -"til - intertidal relative to U. speciosa and U. thayeri (Fig. IB). When .De all 3 species were pooled for each zone, there was no significant u difference in fiddler crab density among the three zones (X2 = ~ 6 -0 3.29, P > 0.05). "0 I.i: 0 4 Trematode surveys '-0 'Vi c 0) Three species of mctaccrcariac were observed among the 3 -0 C 2 species of fiddler crabs that were collected from the 2 localities ee ;;;:0) and field experiment: P. lanccolata occurred in the hepatopan­ creas and it was observed in all 3 fiddler crab species; Mari­ 0 trenia prosthometra metacercariae were found in the thoracic low mid high musculature of U. speciosu and U. rapax, but they were not observed in U. thayeri; and metacercariae of Gynuecotyla adun­ ox B ca were found encysted in the antennal gland of all 3 fiddler N = 35 N = 37 N = 16 ('I crab species, but they usually occurred in low abundance (Table E 'n I). "! 0 0.6 Prevalence and intensity of P. lanceolata was higher in U. Vi .D speciosa than in the other fiddler crab species (Table I), with 13'" infected crabs harboring between I and 103 cysts. Uca rapax ~ experienced relatively higher levels of parasitism by M. pros­ "0 0.4 -0 thometra compared to the other 2 species at both sites (Table I.i: "- 0 I), with infected individuals harboring 1 to 61 cysts. Of the 3 § fiddler crab species, U. tltaycri experienced low prevalence and ·c 0 0.2 intensity of metacercariac (Table I). eD- For U. speciosa, there was a significant posruve association c, between host size and intensity of P. lanceolata (R2 = 0.46, P < 0.01) and M. prosthotnetra (R2 = 0.17, P < 0.(1) (Fig. 2), 0.0 but not for U. rapax (P. lanceolata: R2 = 0 .0 I, P > 0.05; M. low mid high prosthomctra: R2 = 0.06, P >. 0.(5) (Fig. 2), nor for U. thayeri Intertidal Zone (P. lanceolata: R2 = 0.07, P > 0.05) (data pooled across the

Fj(;lIJ{J' I. Abundance and distribution of 3 species of fiddler crabs intertidal). along an elevation gradient in a mangrove intertidal zone in the Indian River Lagoon. Florida. (A) Mean density (::: SD) of fiddler crabs per Field experiment: Host specificity of metacercariae 0.25 m-, (B) Proportion of each fiddler crab species that occupied the intertidal zone. N represents the total number of fiddler crabs collected Fiddler crabs transplanted to the 2 localities (Impoundments from each zone. 12 and 23) exhibited different patterns of parasitism (Fig. 3). Specifically, all individuals of U. speciosa became parasitized with P. lanceolata, but no U. rapax became infected with P. lanceolata from either site. Intensity of P. lanceolata was sig­ nificantly higher in U. speciosa than U. rapax at Impoundment 12 (Wilcoxon signed rank test, P < 0.001) and at Impoundment

TABLE I. Prevalence and mean intensity of parasitism in 3 species of fiddler crabs (Uca speciosa, U. rapax, U. thayeri) collected from Impound­ ments 23 and 12.

Prevalence (';lr) Mean intensity (:t: SO)

Probolocoryphe Gynaecotyla N lanceolata prosthometra adunca P. lanccolata M. prosthometra G. adunca

Impoundment 23 U. speciosa 48 45.8 4.2 0 4.2 :+: 10.7 O.l :': 0.5 0 U. rap"X 18 5.6 77.8 16.7 0.1 :': 0.2 11.2 -.. lO.7 4.3 :t: 7. t U. thuyeri 22 22.7 0 4.5 0.5 ::: 1.3 0 4.2 :!: 4.5 Impoundment 12 U. speciosa 21 85.7 52.4 0 36.0 :': 33.3 5.1 :': 7.9 0 U. rapax 21 14.3 66.7 0 3.0 :t 10.2 10.7 :!: 16.1 0 1002 THE JOURNAL OF PARASITOLOGY. VOL. 93. NO. 5. OCTOBER 2007

Uca speciosa along the Indi an River Estuar y, including U. sp eci osa. U. ra­ 120 pax , and U. tha yeri . A fourth species, U. pugilator , the sa nd fiddl er crab, was frequently observed in adjacent san d and mud­ 100 • flats , but it was not found in our sur veys, because we did not • sample beyond the mangrove intertidal. We found that fiddler crab distribution along a mangrove bank, which vari ed in ele­ 80 vat ion and tidal influence , was not uniform; rather. ce rtain zones • • were dominated by cert ain species of Uca, which is consistent with oth er findin gs (Tea l. 1958; M acn ae, 1968: Montague, 60 • • • 1980; O 'Conner, 1993). Specifically, U. sp eciosa dominated the ..D ('j •• lower and mid-intertidal zo nes, and U. rapax was more abun­ I- () 40 • dant in the high int ertid al relative to the lower zo nes. Such l- • microhabitat preferences may reflect their ecological and phys­ V • 0 0.. I • iological adaptations to inhabit environments with cert ain biotic CIl ...... 20 •Q) and physical condition s, e.g., sediment composition. salinity. CIl • 0 >-. • vegetative cover. For exa mple, Thurman (2005) experimentally () • cc, • • V 0 showed that U. rapax had higher survivorship than U. sp eciosa .;::('j and U. thay eri at high sa ltwater co nce ntrations (>2,500 ('j 0 5 10 15 20 25 o mO sm ), potentially all ow ing U. rapax to inhabit and surv ive in l- V the high intertidal zone. () 70 Fiddler crabs ha ve been documented to host trematode meta­ ...... ('j Uca rapax V cercariae and larval acanthocephalans (A hmed and Khan , 1976; E 60 0 Heard , 197 6; Overstreet , 1983; Nickol et al. , 20(2), pro viding 0 a rich and ins tantaneous helminth co m munity to a variety of Z 50 vertebrates that feed on Uea (Hutton. 1964 : Heard, 1970; Bush and Forrester, 1976; Kin sella, 1988) . The present study repre­ • sents the first report of Probolocoryphc lanceolata (syn . Cer­ 40 CD caria caribbe a XXV, Cable, 1956; Cercaria lanceolata , Holli­ 0 man, 1961 ; Cercaria XXIII. Wardle, 1974 : and P. glandulosa. 0 30 6 Heard and Sikora, 1969 ; Heard , 1970: Bush and Forrester. 1976; Kin sella. 1988) in U. speciosa , Eight species of fiddler 0 0 20 crabs. including U. rapax. are known to naturally or ex peri­ 0 • 00 0 mentally serve as second intermediate host s of P. lanceolata 0 6 CD (Hea rd, 1976). Int erestingly, Heard (19 76) ex posed U. sp cciosa to 0 IS> 0 6 g6 0 to m ore than 200 P. lanccolat a ce rca riae, but no infecti on s re­ 0 0& CD sulted. Furthermore, no para sites were found in more than 30 0 spe cimens of U. speciosa collected from the Gulf co ast of Flor­ 5 10 15 20 25 ida, alth ough P. Ianceolata was pres ent in first intermediate hosts (Bus h et al. , 1993). These findings suggest that along its Carapace width (mm) geographic range, popul ations of U. sp eciosu ma y be ge neti­ FIGliRE 2. Numbe r of metacercari ae of Probolocoryphe lan ceolata cally diff erent, adapted to local condition s. or both. thereby in­ (closed circles). Ma ritrem a prosthometru (open circles), am] Gynaeco­ fluen cing its compatibility as a suitable host for parasite devel­ tyla adunca (open triangles) in Ura spcciosu and U. rap ax coliceted opment (Co mbes, 200 I ). Althou gh we obse rved P. lan ce olutu from Impoundments 23 and 12, illustrating relationships between trcrn ­ atode abundance and host size. Note that G. adunca was not found in in all 3 fiddler crab species during our surveys, onl y U. sp eciosa U. spe ciosa. bec am e infec ted with this parasi te when ra ised und er the same en vironmental condition s as U. rapa.x. Furthermore, our ex per­ ime nt sho wed that at even at a low prevalence ( I% ) of P. lan­ 23 (P < 0.00 I). Both U. specios a and U. rapax became infec ted ce olata in the first intermediate host (c. scalariformisi. all in­ with M. p rosthometra, with U. rapax exhibiting higher parasit­ dividuals of U. speciosa became infect ed, and at mu ch higher ism than U. speciosa at both Impoundment 12 (Wil cox on intensities relative to the parasite survey s. signed rank test, P < 0.001) and Impoundment 23 (P < 0.00 I) . R esults of the transplant experiment indicate that m icrohab­ Furthermore, both fiddler crab species become infected with G. itat prefe ren ces in the mangrove intertidal do not account for adunca, but there wa s no significant differen ce in intensity be­ differen ces in parasit ism between U. speciosa and U. rapax. tween both species at each site (Wilcoxon signed rank test, P Be cause U. speciosa and U. rap ax were presumably equally > 0.05). exposed to shedding ce rcariae , and they were co nfined to the same tidal height, factors other than host distribution may play DISCUSSION an important role in influ en cin g the nature or outco me o f their Of the 6 species of fiddler crabs that occu r along the Atl anti c interacti ons with larv al trem atodes. For example, diffe rences in coast of Florida (Salmon, 1967 ; Barnwell and Thurman, 1984), para sitism between U. speciosa and U. rapax ma y be att ributed 3 species were collected from the banks of mangrove swa mps to the deg ree of openness of the encounter and compatibility SMITH ET AL.-TREMATODE METACERCARIAE IN FIDDLER CRABS 1003

Probolocoryphe lanceolata Probolocoryphe lanceolata 100 300

80 0' 250 o: + 1 200 60 '-' 150 40 100 20 50 o a

Maritrema prosthometra Maritrema prosthometra 100 40

80 0'rJ) 30 +1 '-' 60 20 40

10 20

a o

100 2.5 Gynaecotyla adunca

~ 80 Q 2.0 ir: +1 '-' 60 .c 1.5 '(1) c ...... v c 1.0 40 >---< c cdv 20 ~ 0.5

o 0.0 Uca speciosa Uca rapax Uca speciosa Uca rapax FIGURE 3. Prevalence (%') and mean intensity ( ::':: SO) of Probolocoryphe lanceolata, Maritrema prosthometra, and Gynaecotyla adunca metacercariae in Uca speciosa and U. rapax transplanted to Impoundments 12 (black bars) and 23 (white bars). Fiddler crabs experienced identical environmental conditions at each site over 72 days. Note differences in the mean intensity on the y-axis scale. 1004 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO, 5, OCTOBER 2007 filter (sensu Combes, 2001) for each species. For a parasite to which they must respond and survive the host defense system. successfully infect a host, it must both encounter the host and Signs of encapsulation by host cells have been observed as be compatible, operating as 2 consecutive stages, or stepwise early as 7 days after infection (Heard, 1976). Mctacercariae filters, that determine infection (Combes, 200 I; Kuris et al., begin to encyst 19 days after penetration, becoming fully de­ 2007), Specifically, the parasite must be able to locate and in­ veloped and infective after 50 days (Heard. 1(76). Indeed, en­ fect the potential host (encounter filter) and be able to develop cystment, or sequestration, may be an adaptive strategy to re­ successfully within the host after the encounter (compatibility duce or minimize its interactions with the host that would oth­ filter). Because P. lanceolata has been found to naturally infect erwise compromise its survival (Adamson and Caira. 1994). multiple species of Uca, including U. speciosa and U. rapax, Because the host defense system may respond differently to this trematode is compatible with several hosts, but it may pre­ parasitic infection as a result of genetic or physiological het­ fer certain species over others, When U. speciosa and U. rapax erogeneity within a species (Karp, 19(0), variation in compat­ were raised together under the same field conditions, cercariae ibility among host strains or species is likely to occur. were given a choice between potential hosts, and they chose to In sum, our study supports previous findings that fiddler infect U. speciosa over U. rapax, showing that U. speciosa is crabs often occupy specific microenvironments within coastal a relatively more preferable host. Over time, P. lanceolata cer­ marsh habitats. In mangrove marshes of Florida, their distri­ cariae may have evolved a mechanism to find and identify the bution varied across the mangrove intertidal, with various zones most compatible host (U. speciosai, thereby avoiding less suit­ dominated by different species of Uca. Uca speciosa occurred able hosts (Combes, 200l ). Furthermore, the presence of U. most abundantly in the low intertidal; therefore, it may be ex­ speciosa may close or reduce the encounter filter of U. rapax, posed to relatively high levels of P. lanceolatu cercariae. How­ causing U. speciosa to act as a population sink for cercariae. ever, the higher prevalence and intensity of this trematode in To determine whether the presence of U. speciosa influences U. speciosa compared with U. rapax, which occupied higher the probability of contact between cercariae and U. rapax, the regions of the intertidal, was shown to be driven by host selec­ encounter filter can be artificially widened in the laboratory by tion. Differences in their encounter and compatibility filters. gill exposing U. rapax to cercariae in the absence of U. speciosa. morphology, behavioral activities, and defense systems may If U. rapax was found compatible after experimental exposure, contribute to tbe significant differences in parasitism among then one can assume that the encounter filter is closed in nature host species. when in the presence of U. speciosa. Additionally, gill morphology and behaviors associated with ACKNOWLEDGMENTS respiration may play an important role during the encounter We are grateful to Bjorn Tunbcrg for assisting with identification and process, because P. lanccolata infects fidd ler crabs by entering collection of fiddler crabs, Camilie Sewell for field assistance, and Rich­ the branchial chamber with the respiratory currents. Specifical­ ard Heard for identifying trematode mctuccrcariac. We thank Armand Kuris, Kevin Lafferty, and the anonymous reviewers for input and com­ ly, the setae of the third maxilliped, which prevents sand and ments on the manuscript. Funding was provided by the Smithsonian mud from entering the branchial chamber, varies in morphology Graduate Fellowship to N.F.S. This article represents contribution 685 among Uca spp. (Macnae, 1968), which may allow or prevent of the Smithsonian Marine Station at Fort Pierce. cercariae from entering the host. The setae of the scaphognarh­ ite (gill bailer) and other setal lobes of the maxillae could also LITERATURE CITED prevent cercariae from entering the branchial chamber. Further­ AD,\~'IS()N, M. L., AND J. N. Ci\IRA. 1994. Evolutionary factors influ­ more, as water is pumped across the gills in the branchial cham­ encing the nature of parasite specificity. Parasitology 109: S85 ­ ber by the gill bailer, crabs may respond or behave differently 595. AHMED, M., AND R. A. KHAN. 1976. 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