Some helminth parasites of Nevada bullfrogs, Rana catesbiana Shaw

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(1)Rev.. Bio\.. Trop., 2 1 ( l ) :. 207-220,. 1974. Sorne helrninth parasites of Nevada buIHrogs, Rana catesbiana Shaw by. Bert B. Babero·. Katharina Golling*. and. ( Rcceived lor publication May 1 7,. ABSTRACT: of. In a survcy o f tbe helminth par:::. s ites of bullfrogs i n the area. Ash ,Meadows, Nevada,. Thc. 1 97 3 ). helminths. recovered. 12 specíes comprising 7 genera were collected. are. as. follow5:. ronia prol·ilella,id,. GIYIJJhelmins quield,. Euslro ngy/ides. ( Nematoda ). rrellrichi, S/,ir0I1011f(1 (alesbitwae ane! A bbret';ata sp.;. ( Trematoda). G. sub/Topirtl,. LAnge. proximus1 G .. G.. Jera'l HaemaloloechllJ but/el/si.r, H, brer,i/,/eXIIJ, and H. /hl'Tip/exlIs; (Cestod a) Ophiotaenj(l. magl/a. Brief discussions on each of t he preceding parasites. are presented. EusJro1'1/',ylides wellrichi, i n its encystment i n the musculature, "iscera, and. egg· mass, was lound to be highly pathogenic to bul l lrogs .. The bullfrog is an introdueed animal in Nevada, although the precise date of introduction is not known.. STE)NJ,GER ( 3 5 ). does not list. among the anurans collected in his Death V.lley expedition.. R. ca¡esbeia�la. However, accord.. ing to Norman Woods, Nevada Department of Fish and Game (personal como munication ) ,. a. recent article in a local newspaper refers to the presence of. bullfrogs in the MorOlon Fort in 1 9 1 0 .. Notwithstanding, the animal is n<YW. widel y distributed throughout the sta te, being present in few instances, it is even raised for commereial purposes.. of "frogging". was indiscriminate; however, since. all counties.. In . a. In the past, the sport. 1947 the bullfrog has been. on the protected list, being c1assified as a gaOle animal.. 1970, Dale Lockard of the Nevada D.epartment of Fish and. In June, Game. brought to the writers' laboratory for identification. infected bullfrog County) .. several helminth·. legs taken from animals colleeted at Ash Mead ows. Because of the. obvious. to the musculature of these Jegs,. and. extensive pathoJogical. damage. (Nyc done. the writers were persuaded to initiate an. investigation of these amphibians.. •. Department. of. Biological. Sciences,. University. Nevada, U.S.A.. 207. of. Ne\'ada,. Las. Vegas. 89 J H. ..

(2) REVISTA D[ !HOLOGIA 'f1{()I'ICAL. 20R Ash. Me1 dows,. con si. clevation 2 , 1 7 :, feet, is. dcrt d. oE. a portion. tü be. thz. Death Vall ey Systc-m; it consists of a largc vJ1ltr oc plain lying c::ast of. and 50 miles Ilorth of tbc grcat bend of the Amargosa b(:callse of a sm;t!l descrt ash (fraxilllfS cOri({Ccd ) \vhich was formerly abundant (PAUIFR, 2B ) . Thc boundary hne bctwccn California and Nevada passes through Ash l\ícadows. Thc rcg ion contaills llumerous isolateJ warm springs and a fc-w disconncctcd SW-LlCC f l ows, "\vhich according tú MILL.ER ( 2 6 ) , are remnants of the Amargosa River system. During periods uf hcavy rain in s p r ing and summer, the headwatcrs of this rÍver pOllr their flood waters onto lhe great Dcath Valle), salt Ha!s. Thc: numerous warm springs oL" the Death Valle), region have tcmperatures that vary fcom 22 e to 43 C (average 23.8-24.1 C. ) ; howevcr, according to Millcr, temperature the Amargosa R:u\�c:. It was so namecl. River.. very. is. springs. indiv idual. in. fluctuation. (21). mostly. of. adult-size,. BL\TLEY ( 3 ) . 1feadows. Ash. at. bul1frogs. cites collections made in. 95 bullfrogs,. total of. of. oCCurrence. The LINSDALI:. vegetation. prevalent. The. narrow.. which covers thc arca is discussed in det"ail by. is. 1933 and 1936. were collected by. of. long. duration.. area,. From this. Collection sites included a Jarge isolated pand, marshy meado\\' areas, and. Tubb's. drainage ditch on the lodgc, and. a. 1 97 1 ,. 1970,. 50 animals.. 35. possibJe been. that the population of. decimated. dut. lo. and. tr ips. Spring.. Forest. M:ay <lne!. June, 1 972,. was. bul lf rogs in. exceptionalIy dr)',. the Ash 1-feadows arca ma)' have the. or. predation,. parasitism,. BUNNELL, 9; LITTON, 2 2 ) .. drainage. of. marshcs. uf irrigation agriculture (DEACON frogs were captured by hand at night. with thc aid of a searchlight,. l\1nst. bllt a. He1minths wcre rccovercd. and and. few "\Vere taken with lhe use of a ' "frog gig". from. frogs by. routinc pantsitological proce. In many instances blüod smears v.'ere made, ho"\'\" ever no helminths were. obseryed.. A total oE eleven spccics \Vere obtained, inc1uding Huee of Ncmíl.. toda, stven of Trematoda,. and. alcohol-¡tn:tic acid-formalin. ( A FA ). were. la. highly. i t is. associated with cxtcnsin; dcvelopment. dures.. From. froro Aprif to August,. to the arca in. 1 97 2. a. Meadows. Howc\'cr, in July of this btter year wc coJkcted. the spring of. Although. of. about a mile wcst. animals were cxam ined. Despile several. no frogs \Vere collected. animals.. ranch ; t\\'o small ponds near the Ash. arca. vast meado",. June to August,. a. the present writers.. stained. Semichon's. with. for study i n lactophenol oc disnlssions o f e;;¡ch parasite. one. AH parasites were fixed i n. of Cestoda. solutions.. Acid. The. Carminc,. gl}'ccrin and. studied. latter tWQ. parasite. groups. were. c!eared. whi J.e ncnutodes. from tcmpnrary mounts.. Brief. collected follow :. NEMATODA. l:.·IISI/"()}/f?y!ides. }iigerskiijld,. 1909. EJlJ/rOllfolideJ U'ellrirbi Ca navan , (Figs. 1 This. helminth. reddish. collected. larval. from. dioctophyrnid. bullfrogs, beinS. 1 929. 3) nematode. recovcted in. was. the. most. 53 animals.. COfllmQn. The ,,"orms.

(3) HEU...llI\'TH PARAS1HS OF NEVADA BUU,FROGS. ¡¡ti/lUlO & (,'OUINC: werc l1S11al1y occurred. coiled. singly. single c)'st.. but. and. encysted. somctimes. within. two. peritoneum, along the. mesent('cy. of. che eg�·nuss uf gravid remales. single host. was. 2 5 ; the. the. Jead.. Most. prcsent within. \Vere observed on �nd. t..e:. (x.'c;lsionalIy. on. fron'!.. The maximum l1ull1ber of cysts obtained. in. a.. thc musculature-, especially. digestivc tract,. aver:ól.gc nurnber was. September, most cysts by the. on. membrane.. \Vere. a few instances, cysts werc seen within. worms decreasecl as the sUl11mer progrcssed. partial ly resorbed. whitish. wonns. However, they. In. the surface of the liver and lungs.. .1lld cul)'. tilin. CySt3 occurrect more frequently in and. of the append;lges and stomach \Vall.. .l. a. oc three. 209. five.. TI1C. of viable. munber. August. During t11c bUcr part of. the musculature appeared compressed and. surrounding tissue.. Coiled unencysted worms were. Worms with in. such cysts. \Vere:. In several hosts, such. encountered.. a lso. worms were found under the skin of the abdominal and thoracic regioo s. C"N"VAN stream. pike,. (6). n.. reported. wt?llrichi. brook trout, calieo bass,. eoelomic. from the. and the. ni ne.spined. cavity. sunfish.. of. He also. coJIected �neysted \yoflns from the mesentery, peritoneum, and liver of bull·. fish-eating. frogs, and suggesteJ that the primary hosts foc the roundworm are birds and that fish may be secondary hosts. llim to be an aberrant host. Thc. Dwarf cyprinodonts,. bull frog. wa.s considered by. CyprhlOdoll nevadens;s were. (25). aIso fcund in the streams and marshes of the Ash Meadov.rs anea; MrLLER offcrs. an. account o f. of. None. thcse. f ishes .. the fishes \Ve examined harborcd E.. u;enrie!;;;. theie sOla'!l sizc,. usuallr not mor� than 20 mm i n length, seemingly ne,gates infection. number of. infected frogs collected. ind icates. that these. anjrn�ls,. The large at l east. in. the areas studied, are truc secondary hosts for E. UJtllr;c!Jj. (43) rcports 1 6 species as comprising the genus EIIstl'ong)'·. YA1'.IAGUTl. lideJ, ho\vever, only two have been reported from the U.S.A. : E. ;gllotNJ ]iigersk., 1909, and E. Il'enr;c!;;. :Morphologically, tlle Nevada species firs the description of the. latter as presented. by Canavan.. The. species. large muscular bursal cup of males, in which. is recognizable. by. the. is a protrusile terminal cloacal. orificc, another smalJer bursal cup, and by the lattral rows of papillae extend· ing thc cupo. reported 123. length. of the body.. Such papilJae also sllrroun d the. larger. The lengths of the "\vorms are variable, depending upon the age. males. being. as. mm long by. measurements given. 1 0 6 mm mm wide.. 0.96. Canavan,. by. long. by 0.86 mm wide and. buesal. Canavan.. females. The Nevada specimens approximate. as. the. however, the length of worlTIS obviously 1S. dept'ndcnt upon 1ge and development.. f.lIJlrol1!!,)üdes org,lns - i.e.,. vital. J iver. lS highly pathogenic and. lungs,. metabolic fUllction,. Since. the parasite. to frogs.. In. attaching. conceivably could. itself. to. in terfere with. some cysts were also observed in egg·masses. within gravid females, there (ouId be increased reproductive morbidity. Extensive damage du c to cncystment within thc soma tic musculature was the most obvious pathological, damage obscrved. rnay even burrow. its ,�ay. JAGERSKIÓLD ( 1 6 ) rcported tbat E/lJlrollg)'lid,j. throush the stomach. wall..

(4) REVISTA nI-: IlrOJ.OG1A TROPICM.. 2JO. SpirOIlOllrtl Leidy, 1 8 5 6 S}i/'OIlO1ll'd ctttesbialldc (\XIa l ton, 1 92 9 ). (Figs. 1 Species of t he. -. 7). SpiroJ1(jlifrl primarilr occur in. amphibia by WALTON (39) from the bullfrog, R(Il1{/ ((/Iesbial/{I, from Ill inois, Oklahoma, and 'Louisi· aoa, Walton stated that' th e species \-vas the most common intestinal ncmatodc occurri ng in bullfrogs. He late r fouod the species in the same host in the state oE Georgi a. YA]I-{AGUTI (43) ci tes othcr hosts for thc specics as follows: Rana gry/;o, R .rpben(){epha1(I, HJftl grtíÚI)J{/: H. úncrtt, Gá.ftrophfyne (moli· nensis, PsellddC'/'iJ OCHltI/'iJ, aod Sirell {aeNtina, all of the U.S.A. Nevada cons ti tutes a. ncw locality record for this nematode species. genus. and reptiles. S. (ctlesbúl!l(/c. W<lS. fishes,. d escribed as FalrtlJ//'{1 caJeJhi.lIlcle. .. the second most common p aras i tc recovered in this intestine of 44 anirnaIs, with a range of infection from. 1 to ove r 1 0 0 parasites per host. GeneraI ly, the Nevada specirnens fitted the origi na l dcscri ption as gi vcn by Waltol1, however, both male and female specimens seemed to be longer thao those reported by Walton This size d ifference, however, does not seem to be sufficient fo! justifying a dif ferent identification. Although often prevalent in large numbers in bullfrogs, patl\Ülogical darnage duc to S. cr1leJbidllae was not discerned. S. calesbicmae was. study, occurring in the l a rge. .. A b brevi"la Travassos, 1 91 9 Abbrevirlta sp. This gen us. ""'¡tS e nco untereJ only once. A single remate worm was tbc l arge !ntestine wherein it was d etected pa rti ally extending through the serosa of the intest i n al \\'al1. 1" ,Iil/l . the worrn appeared rcdd ish however, this color disappeared upon fixatiol1. Members of Abbrel!i(tta normalIy are found in the stomarh rather than the intestine, so it is possible that the worm may have m igrated to the i ntesti nc. found i n. ,. .. TREMATODA LfllIgeroilia Caballero & Bravo-Hollis,. 1949. Lrlllgerollia /,rol'ite!!,,¡-itl Sacks, 1 9 5 2. (Fig. 8). Lmgerotlút pfol/iteJldlú was dcsceibed by. SACKS ( 3 1 ). {eom the small. lotestine of e ight leopard frogs Rál1fl PiPiem JpbcJJocepha/a, coHccted in Florida. ,. A total. of only. present Shldy.. three specimens. from two bullfrogs. were. recovere d ilT the. The· Nevada specimens werc slightJy smaller with ptoportionately.

(5) BABERO. &. GOLLlNG:. HEfMINTH PARASÍTÉS. 01'. NEVADA BULLFROGS. 211. reported by Sacks. Notwithstanding, they are con side red to be of this specíes. Langeronia prozJitellaria is not a coromon parasite oCbullfrogs, as evidenced by the few times it has been collected. snialler organs than tbose. '. Glypthelmins Stafford,. 1 905. There .has been much controver.sy co,ncerning the validity of species assigned . to Jhe . genus Glypthelmins and numeroJls investigators have attempted too str¡¡ightc;;n out the syste�natics oí . this group (M11.LER, 24; FRJ;lTAS, 1 0 ; RANK;rN, 29.; �UIZ, 3 0 ;.. BYRD, 4 ; BABERO, 1 ; CHENG, 7 ; BYRD anq 1-L\,PLEs, 5 ; NASIR, 27; TRAVASSOS e t al., 3 8 ; YAMAGUtI, 44) . Thus, members o f G/ypt he/mins have been variousl1 assigned to different genera lvIargeana Cort, 1 9 19; Microdermá' Mehra, 1 9 3 1 ; Cboledoc)'Jl1lJ Pereira and Cnocola, 194 1 ; Rauschiella Babero, 195 1 ; Reynoldstre.ma Cheng, 1 9 59 ; Repandllm By rd and Maples, 1963. BA�ERO (2) suggested that the genus: Glypthelmins couid be divisable into two groups : "a.) species with peripharyngeal glahds and without ute.rine coi15 developed. .in th,e pretesticular zone; b. ) species without peripharyngeal glands and with uterine coils developed in the pretesticular zone." CHE NG ( 7 ) painted out that since Margeana was described as a new genus because of the absepce of peripharyngeal glands that the erection of another genus as sug gested was not necessary. He, therefore, proposed the reestablishment of lI1argeana as a valid genus. MILLER (24) synonymized this genus with Glypthelmins . Subsequently eleven species previously assigned to G!ypthelmins were. -removed to Margeana, and G. quieta ( Stafford, 1900 ) , G. Sllbtropica. Harwood; 1932, and G. festina Cordero, 1 944, were retained. G. palmiPedis ( Lutz, 1928) was considered a synonym of M. lingllatula (Rud., 1 8 1 9 ) . BABERO ( 2 ) created the ge.nus RatlSchiella for a trematode species from a Mexican frog. Because . of certain morphological similarities with the genotype R. tineri, G. ¡'epan(/tI1n (Rud" 1 8 1 9 ) was transferred to Ratiscbiella. In assigrring the latter species to ll1argeana, Cheng was unaware of the erection of Rtutschielia and the new position of repartdum. Also, apparently unaware of the erection of Rallschiella and the new position of repandum, BYRD and MApLES (5 ) established Repand¡¡m n.g., with Repandll1Jl repandum as genotype. These investigatots also rejected the separatióq of Glyptbelmins into Glyptbelmim and Márgeana for species described as lacking peripb.aryngeal glands, stating that these glarids seem to depend heavily on the methód u sed in handling and staining whole mou'ilted worms. Nasir studied both whole - mounts and sectioned specimens, and observed deeply stained structures in the peripharyngeal region. However, he fe1t that this character was too difficult to be worked out with certainty and, therefore, stated that .it .'. did not provide a sbund basis for generic separation. TRAVASSOS et al. ( 38 ) without discussion or reference to Cheng's division, r�tained most speCies of Glypthelmins previously assigned to the genus. -. ,.. '. Grfplhelmi¡'s 'elegam' Trávassos, 1926 was transferred te the genus- Choledocystus. YiAMAGUri:' (44) " lisldl twenty-thiee spedes as havins been assigned to Glypt..

(6) REVISTA D E BIOLOGIA TROPICAL. 212. betmtm and the genera Margealla, Cbolecloc)'Stlls and Repandu-m were cOl1sidered by him to be synonyms of Glyptbelmins. Cbolerlocystm, h owever, is considered by num€rous investigators as a valid genus. Gl)'ptbe/mim ra"fftest��ltl(fI'is Nasir, 1966 obviously does not be long in this genus. The h ighly branched testes and the extensive extracecal disposition of the u{erus are characters not consistent with other members of the genus. While it is tme that sometimc;;s the peripharyngeal gl an ds are not dist inctly stained, their presence usuálly is indicated by their faint appearance. However, in view of the gen eral consensus concerning the presen<;:e or absence of periph aryngeal glands as a cha'racter for generic separátion, the writers will employ the name Glyptbe/mim fár tbe following flukes obtained from the intestine of bullfrogs.. Giypthe/mi11J quieta (Stafford. (Fig. 9 ). 1900). Giyptb�¡m;!1S qlli�ta was the most prevalent trematode collected in this study, bei ng recovered from the small intestines of 32 bullfrogs. Infections ranged frOl11 1 to 97 specimens per host. Both mature and immatme worms were frequently collected from the same host. The morphology of the species fitted the redescription as presented by MILLER ( 2 4 ) and CHENG ( 7 ) Distotn1l1n quiet1l1n Staffo rd 1 900 was originally described b y STAFFORD ( 33 ) ; he later ( 3 4 ) removed the species to Gtypthelmins, stating' that it occurs in frogs - Rana catesbialla, R. 1J¡'l'e.rcem, and Hyla pickeri71gii. G. quieta has since been found to be a common trematode of frogs and has been reported numerous times from the bullfrog, incIuding reports by MANTER ( 2 3 ) , RANKIN (29) and WALTON (40 ) . The life cycIe of the species has been reported by RANKIN (29) and lEIGH ( 19, 20 ) . ,. Glypthelmins subt1'opica Harwood,. 1932. This species was also a common trematode of buIl frogs. It i.s easí1y confused with G. quieta, since both have peripharyngeal glands. In fact MANTER. ( 2 3 ) , RANKlN ( 2 9 ) and NASIR ( 2 7 ) considered the species to be synonymous with G. qttietr¡.. However, Cheng fe1t "that the distinct pattern of the viteIlaria of G. sltbtropicd, plus its reduction to approximately half the size oE G. pÚeI8, ( are of sufficient significance to separate it from the genotype. Employing the character cited by Cheng and by HARWOOD ( 1 2 ) re1ative to the viteIlaria, species of G. subtropica were uncertainly identified. Eight frogs harbored thfS parasite, with the number per host ranging from 2 to 1 2. ". GLypthe/mins pt'oximus Freitas,. 1 94 1. Five slides contai n ing spec imens of this species were identified. by Dr. Pi! N a sir Oriente University, Venezuela. This species lacks peripharyngeal ¿¡lands and uterine coils developed in th� pretesticu)ar zone and, therefore, was ,.

(7) IJAW;RO & G'OUJNG :. HELMINTH. PARASITES OF NEVADA BULLFROGS. 213. placed by Cheng in the genus AIargeana. However, the present writers for the reason already explained, are regarding the species as a member of Glypthelmins,. GJypthelmins sera. Cordero, 1 944. G. s eTa) is primarily According to Cheng's redescription, .M. serd ( identifiable by its oval-elongated body, intestinal ceca reaching to one-third of the body and by i ts extracecal vitellaria, which consist of grouped foHicles extending from the leve! of the ovary to nea r the tip of the ceca, It also has testes which are obliquely arranged. Nasir (personal communication) identified as G. Jer,1 worms on a single slide sent to him by the writers. Apparently, these specimens were the only GileS collected. In making his i dentification, apparently Nasir no longer feels G. sera to be a synonym of G. lingtlat"la as previously stated (27 ) . =. HaematoloechuJ L0055,. 1899. Members of the genus Haematoloechtls are not uncommon parasites 1ll the lungs of bullfrogs. Accounts of the life cycle of several members of this group are presented by KRU LL ( 1 8 ) . YAMAGUTTI (41 ) lists five species of Haematoloechm as occurring in Rana catesbial7a - H. variegaftls (Rud., 1 8 1 9 ) , H. bret!iplexlIs Sta fford, 1 902, H. complex/Js ( Seeley, 1906 ) , H. f¡oedete Har wood, 1932 and H. longiplext'J Stafford, 1 902. Additionally, '\VALTON (40) Iists H. par'V·iple.'i..'ttS ( Irwin, 1929 ) . In the present study, members of the genus comprising three species have been collected nine times, with the number of specimens in a single host ranging from 1 to 17. Flclematolo(!(!JtlJ buttensiJ Ingleól, 1 9 3 6. (Fig. 1 0 ) Flukes clss i gned to this species were collected four times, both mature and immature specimens being rccovered . H. bttttensis was originally described from R. boy!i in California by INGLES ( 14 ) . The Nevada specimens, in addition to showing resemblance to H. bllttensis, also showed similarities to H. kemensis and H. oxyo rchiJ as described by INGLES ( 1 3 ) . However, organ sizes did not concur with either of these lalter species. The Nevada specimens also resembled to some extent H. floedae as described by HARWOOD ( 1 2 ) , however, they differed !rom this fluke by the presence of a. "distinct visible collar" that was described by INGLES ( 1 3 ) for the species. Although spines appeared to be absent from ¡he Nevada specimens and the average sizes of organs did not quite agree with those given by Ingles for H. buttemís, organ size did faH within the ranges given. Nevada bullfrogs, therefore, constitute a new locality and host record for H. buttenJis..

(8) 214. REVISTA bE BíOLOGIA TROPICAL. Haematoloechtts breviplexus Stafford, 1 902. ( Fig. 1 1 ) H. brellip/ex!IS i s one of the largest lung flukes occurring 111 North ' American frogs. From Nevada frogs it was collected five times. The morphology of the specimens fitted the description as presented by CORT ( 8 ) . The worms weré readily identified by their Íarge size and distinctly lobed ovary and testes. They showed some resemblance to H. IOllgiplex1IS but couId be separated from it by the more pronounced lobations of the ovary and testes, as well as by the contour of the longitudinal folds of the uterus. The life history of H. brelliptexlIS is given by SeHELL ( 32 ) , who states that dragonflies (Aeschno mltlfic% l') pass the infections on to frogs. I-Iaematoloechus parviplexus (Irwin, 1 9 3 9 ). (Fig. 1 2 ) A single specimen of this species was collected from a lung o f a bullfrog. The specimen was not readiiy identified and was initially thought to be H. buttemis, however, the lobed nature of the ovary showed the fluke to be different, and as to morphology, measurements, and disposition of organs it agrees c10sely with the original description and diagram as given by IRWIN ( 1 5) . Apparcntly, there are no other reports of this species i n bllllfrogs. A detailed description of the l ife cyele of H. parFiplextls is given by KRULL ( 1 8 ) . CESTODA o phiota enia LaRue, 1 9 1 1 Ophiotaenia magna Hannum, 1925. ( Figs. 1 3-1 5 ) The genus Ophiotae¡úa infects fishes, amphibians and reptiles. YAMA (42 ) lists only two species as infecting bullfrogs, O. magna and Q. gl'acilis Jones, Cheng an.' Gillespie, 1958 . Six Nevada bullfrogs harbored adlllt cestodes in their small intestines, with a. range of infection per host of 1 to 3 worms. Morphological stlldy of these tapeworms showed that they fitted the des cription of O. magna as presented by HANNUM ( 1 1 ) . THOMAS ( 3 7 ) i n his djscussiol� of O . persPima LaRue, 1 9 1 1 stated that the first intermediate host for the species is Cyciops 1!ltlgaris, although other copepods, such as Cydops lIiridis, C. pr(/sintls and Mesocyclops obsoJetlls will take the infection. I n these latter hosts, however, growth, according to Thomls, is much slower. Thomas also statcs that tadpoles, frogs and mudmin nows ( Umbra !imi) may also serve as t�e second intermediate 11Ost, passing the infections on to snakes (Thamnophis sertalis and Natrix sipedon ) . He states that the plerocercoids in ta dp oles continue to grow with the metamorphosis of GUTI. ..

(9) BABERD & GOLLlNG:. the animals into. HELMINTH PARASITES. frogs. segments may form,. and. may break. 01'. 'NEVADA BULLl'ROGS. out into. 215. the coelom, and immature. In the case of O. sapheila Osler,. 1931,. observed Copepada, Cladocera, a n d aquatic beetles, a s well. THOMAS. as snails,. ( 3 6) i n the. intestirial debris of frogs amI suggested that these amphibia can become d irectly. i nfected hy the accidental eating oE i nfected C)'clops. Although no copepods \Vere examined from the Ash Mtadows arca from which bullfrogs were collected, they were observed to be present.. The l i fe-cycle of. parallels that. O. magna. of O. saPhew¡ in that bull frogs may become d i rectly i nfected by the consumption of copepods.. ACKNOWLEDGEMENTS The writers extend their s incere thanks to the fol!owing persons whose assistance made this study possible : Department,. who. inspired. this. Mr. Dale Lockard, Nevada Fish and Game. study by. bringing to. the. writers'. attention. infections in bullfrogs : Drs. Charles Hansen, National Park Service, and James Deacon, University of Nevada, Las Vegas,. for sllpplying reference materials. and reading the manuscript.. RESUMEN En. un estudio de los parásitos. de las ranas,. llevado a cabo en Ash. Meadows, Estado de Nevada, EE.UU., colectamos doce especies comprendidos. en. siete. géneros,. como. slgue :. (Nematoda ). wellriebi, Spirollou/'tl catesbeiaJIae y A b brevicrta sp. ;. de helmintos. - EltStrong)'! ides. (Trematoda). - Langerollia. prOt1ifeltaria, Glypthefmhzs q¡úeta, G. sllbtl'Opica, G. proximt.ts, G. sera, Haema. lotoecbtlJ bttttemiJ, H . bre l'ip/exttS y H. parviplexlts; ( Cestod a ) Opbiotae17ia magnel. Se hace un comentario breve de cada uno de estos parás itos. ElIstroll -. gylideJ 1/Jenrichi es el helminto gue se encontró con más frecuencia en ranas. en el área de estudio, y enquistado en los músculos, vísceras y huevos causa alteraciones patogénicas graves.. LITERATURE CITED l.. BABERO, B. B. 1951.. RtlUJChiella tine-ri n.g.,. }. Prlr,lsit., 3 7 : 2.. trematode. ( PJagiorcbiinae). from. a. frog.. Notes on t h e trematode genus Gly!J/belmins Stafford, 1 9 0 5 . Pl'oc. Helll/illtb.. Soc.. WaJ"h., 1 8 : 1 0 3 - 1 06 .. BE ATLEY, ]. C.. 197 1 .. Vrlsculm'. !Jlalils 01 Ash. Rad. BioJ.. 4.. a. BABERO, B. B .. 195 1 .. 3.. n.sp.,. 5 60 - 5 6 2 .. BYRD, E 1 95 0 .. ( 0 4 . 1 , Gen.. Merldows, Nn·ada. 1 2 ) , 59 pp.. Univ.. CaJif.. Lab. Nud.. Med.. E. AlIoglyPIIIS cremhawi,. a. new. genus. und. .species. of. J igenetic. trematode. ( PJagiorch iinae) from the chameJeon. I'ranJ. Amer. l\1icrosc. Soc., 69 : 2 80 - 2 8 7 ..

(10) REVISTA D E BIOLOGIA TROPICAL. 216 5.. B YRD, E . E ., & \YI. P. MApLES 1963 . The Glypthelminths (Trematoda: Digenea ) , with a description of one species and the erection of a new genus. Z. Parasitkde., 2 2 : 5 2 1 - 5 3 6 .. 6.. CANAVAN, \YI. P. N . 1 929.. Nematode paras ites Pd1'asitology,. 7.. CHENG, T. C . 1 959.. Studies. on. 21:. the. of ver t eb rates. m. t b e zoological garden ancl vicinity.. 63·102.. trematocle family Brachycoeliidae, II . Rev i si o n o f the ( St a ffor cl , 1 900 ) Stafford, 1 905, and Margeal1a Cort, description oE Rey¡¡oldst"ema n. gen. ( Glypthelminae, n.. genera Glypthelmins 1919;. ancl. the. subfam. ) . Amer. Midl. Nat., 6 : 68-88. 8.. CORT, \YI. W.. 1915. 9.. North American frog l ung flukes. TI'(/J/s. A m e r. MicroJc. S oc ., 34: 2 0 3 · 240.. DEACON, J., .& S. BUNNELL 1970. A process of destruction, man and pupfish.. 10.. FREITAS, J. F. 1 9 4 1 . Sobre alguns trematocleos parasitos de r as.. 1 1.. HANNUM, C . A. 1925.. J. Ca/if. Tomonoll', 5 : 1 4- 2 1 .. Ret'. Brasil. B ial . , 1 : 3 1 · 40.. A new species of ce3tode, Ophiotaenia mag'h1 n. sp. fro l1l the Erog.. TI'(/II.f.. Amer. Microse. Soc., 44 : 148- 1 5 2 .. 12.. HARWOOD, P. D . 1 9 3 2 . The helmintbs parasltlc. vicinity. 13.. Proc.. m Amphibia and Reptilia o f Houston, Texas, amI U. S. Nat. MIIS., 8 1 : 1 - 7 1 .. INGLES, L. G. 1 9 3 2 . Four new species of H"eJllatoloechus ( Tr em atod a ) from Ralla. aílr01". df(/ytolli. from California and CephalogonilllllS bl'evici1'1'us, a ne\\' species of t r emat ode. from the intestine of R:ma. aUrofa. from California .. VIIi/'_ Cali!.. 3 7 : 189-20 1 . 14.. INGLES, L. G . 1936.. 15.. \YIo rm parasites o f California Amphibia. Trans. Amer. Mie/oH. Soc., 5 5 : 7 3-92 .. IRWIN, M. S . 1929.. A n e w l ung f1uke from R,m?l clamitClIlJ Latreille. T,.cIII J . A 111 ..1 ' . MiC1·OSC. Soc., 48:. 16.. Pub/. Zoo!.,. 74-79.. JÁGERSKlOLD, L. A. 1909.. Zur Kenntnis der Nematoden-Gattungen Eust" ongylides uncl Hystrichis .. A cta R. Soco. Sci.. UpsCil., Ser. IV, 2 : 1-48.. Figs. 1 - 3. Eflsholtgylides wellrichi Fig. 1 . Anterior end ( lateral view, male) Fig. 2. Pos terior end ( lateral view, male) Fig. 3. Posterior end ( latera.! view, fem a l e ) Fi gs . 4 - 7. SpirOIlOlil't¡ Fig. 4 . Anterior Fig . 5 . Posterior Fig. 6. Poster i or Fig. 7. Po ste ri or. ctlteJbimlCle end ( lateral view, male) end (ventral view, m ale) end ( lateral view, male) end ( lateral view, fem a le ). Not·.�.

(11) BABERO & GOLLlNG :. HELMINTH PARASITES OF NEVADA BULLFROG.>. 217.

(12) REVistA DE BIOLOGIA TROPICAL. 218. 17.. ]ONES, A. W., T. C. CHENG, 1958.. R. F. GILLESPIE sp., a proteocephalid cestode from a frog. J. T�nn.. 11<. Ophiofaenia grttcilts n. Acd4. Sá., ;3: 84-88.. 18.. KRULL, W. H. 1931.. Life history studies. on. two frog lung flukes, PnellmorJoeces mediop/exlIs and. PneumobiteJ P4rt,ip/exus . 19.. Amphibians and reptiles In Nevada. Pro.. Amer. Acad. ArlS, 9 3 :. A program for action saving the pupfish. J. Calif . Tomorrow, 5: 22 2 5 .. A collection o f trematodes from Florida Amphibia. Soc.,. Studies on G/YPlheltnins quieta Stafford. J. Porasit., 1 6 : 2 37-243.. MILLER, R. R. 1948.. The cyprinodont fishes of the Death Valley System of eastern California and 50uthwe<stern Nevada. Mus. Zoo/_ ( Mise. Pub/. ) , UnÍ/'. Mich., 68 : 7- 1 5 5 .. lci.. MILLER, R . R.. 27.. NASIR, P.. 1950.. 1 966.. Speciation in fishes of the genera Cyprinodon and Empetrirhlhys, inhabiting the Death Valley Region. Evo/ulion, 4: 1 5 5- 1 63.. Two species of digenetie trematodes from He/minlh. Soco Wttsh., 3 3 :. 28.. TranJ . Amer. MicroJC.. 5 7 : 26-37.. MILLER, E. L. 1 930.. 25.. 197-257.. MANTER, H. W . 1938.. 24.. ( Stafford,. urrON, M.. 1970. 23.. Experimental studies on the life cycJe of G/YPlhe/mins qlliela 1900 ) , a trematode of frogs. Amer. Mid/. Na/., 3 5 : 460-4 8 3 .. UNSOALE, ). M. 1938.. 22.. The life cycle of a trernatode of frogs. Sáenu, 86: 423. LEIGH, W. H . 1 946.. 21.. 5 0 : 2 1 5-276.. LEIGH, W. H. 1937.. 20.. TranJ. Amer. Microse. So",. Venezuelan. amphibians.. ho... 1 66 - 1 70.. PALMER, T. S. 1 893.. Norlh American Fauna (No. 7 ) : The Dealh Valley Expedílion, a bi%. gica/. survey of parls of California, NeJ.'d4a, Arizona, and Uta.h . U.S.O.A., Gov't.. Print. Off., Wash., 394 pp. 29.. RANKlN, J S.. review of the trematode genus G/YPlhe/mins Stafford, 1905, with an account of the life eycJe of G. quieta ( Stafford, 1900) Stafford, 1905.. 1944.-11.. Trans. Amer. MicroS(. So .. , 63:. Fig_ El. Fig. 9. Fig. 10. Fig. 1 1 . Fig. 1 2 .. Langeronia provitellaria G/YPlhe/mins quiela Haema/o'¡oechus bUllensis H. breviplexus H. parvip/exus. Figs. 1 3 - 1 5 Fig. 1 ; . Fig. 14. Fig. 1 5 .. 30-43.. Ophiotaenia maJ(na. Scolex Mature proglottid Gravid proglottid.

(13) BABERO. & GOLUl-; G :. HEI.M/NTH PARAS/TES OF NEVADA BULLFROGS. 219.

(14) REVISTA DE BIOLOGIA TROPICAL. 2 20 30.. RUlZ, J. M. 1 949. Considerac;óes sóbre o genero Choledocyslus Pereira et Cuocola, matooa,. 31.. Plagiorchiidae) Rev. Brasil. Biol.,. SACKS, M. 1 95 2 . Lmguonia. pro vilellaria. ( Lecithodendriidae ) ,. from Rana pipien! sphenocephala.. �2.. 9:. a. new. species. The life h istory of Haelllaloloechus brel /iplexus Stafford,. Haplometridae McMulJen,. ( Tre·. of. trematooe. Trans . Amer. Mhrosr. Soc., 7 1 : 267·269.. S:::HELL, S. C. 1965.. 1 94 1. 1 67· 1 74 . .. 1937 ) ,. with. emphasi5. on. 1 902. the. ( Trematoda :. development. the sporocysts. ]. ParaJiI., 61 : 587·593.. H.. STAf'FORD, ].. �4.. STAFFORD, J.. 1900.. 1905. 35.. Sorne undescribed trematodes.. 13:. 399·4 14.. Trematooes from Canadian vertebrates. Zool. Anz., 2 8 : 681 ·694.. L.. STE]NEGER, 1893.. Zool. lb. 5ysl.,. oí. Nor/h Amerit"an Fauna (No. 7 ) : The Death Valley Expedi/ion, a biological rurvey of parlS of California, Nevada, Arizona and U/ah (parl 11 ) . U .S.O . A . ,. Gov'!. Print. Off., Wash., 394 PP. 36.. THOMAS, L. J . 1931.. 37.. Notes o n the life history o f Ophiolaenia saphena from Rana clamitans Latr.. l. Pararil. , 1 7 :. 187·195.. THOMAS, L, J . 1941.. The life eycle o f Ophiolaenia perspit"ua LaRue, a eestJde o f snakes.. RelJ.. MeJ. Trop. Parasit., 7 : 74·78. 38.. TRAVASSOS, L, J. F. FREITAS, 1969.. 39.. Insl.. Oswaldo Cruz, 67 :. 1 · 866.. Studies on sorne nematodes of North American frogs. f. ParaJiI., 1 5 : 227·240.. WAL TON, A. C. 1947.. 41.. A. KOHN. Mem.. WALTON, A. C. 1929.. 40.. .le. Trem.ltodeos do Brasil.. Parasites of Ranidae ( Amphibia ) . III.. ( 70 ) , f. Parasil.,. ( Suppl. ) , 3 3 :. 1 18 .. YAMAGUn, S. 1 95 8 .. Systema Helminlhum .. The JigenetÍt" IremaloJes 01 ver/ebrales. I & JI. Inter.. Se. Pub., Inc., N. Y., 1 57 5 pp. 42.. yAMAGUn, S. 1959.. SySlema Helmin/hum.. 1. The t"eS/odes. 0. N. Y., 860 pp.. 43.. Y AMAGUTI, 1961.. 44.. S.. Syr/ema Helminlhum. The nema/odes Pub., Inc., N. Y., 1 2 59 pp.. YAMAGUTI, S. 1 97 1 .. 5ynopsis. 0. 1. Co., Tokoyo.. Digenelh. Trema/oJes. 1. 0. verlebrales.. 1. 0. I.. Inter. Se . Pub.,. verlebrr.les.. Verlebrales.. I &. I. &. 11.. Ine.,. Inter.. 11. Keig3ku. Se.. Pub.,.

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