Helminth Fauna of Suckers (Catostomidae) of the GilaRiver System, Arizona. l. Nematobothrium texo-

mensis Mclntosh and Self, 1955 (Trematoda)

and Glaridacris con{usus Hunter, 1929(Cestoda) from Buffalofish

OMAR M. AMIN

Reprinted {rom

THE AMERICAN MIDLAND NATURALIST

Vol. 82, No. 1, July, 1969, pp. 188-196

Univenity of Notre Dame Press

Notre Dame. Indiana

A

Helminth Fauna of Suckers (Catostomidae) of the GilaRiver System, Arizona. l. Nematobothrium texo-mensis Mclntosh and Self, 1955 (Trematoda)

and Glaridacris confusus Hunter, 1929(Cestoda) from Buffalofish'

OMAR M. AMIN2Department ol Zoology, Arizona State Uniuersity, Tempe 85281

Ansrnecr: Three species of buffalofish from Apache and RooseveltLakes on the Salt nivei lGila River System), Arizona, were examinedfor helminth parasites. They are Bigmouth buffalofish Ictiobus cyprinel-lzs, Smallmouth buffalofish I. bubalus, and Black buffalofish I. niger,All host species were infected with Nematobothrium texomensis Mc-Intosh andself, 1955 (Trematoda: Didymozoidae) and Gtaridacris con-fzsas Hunter, 1929 (Cestoda: Caryophyllaeidae) (new locality records).In the present paper ecological and morphological data concerningthese oarasites and their relationshio with their fish-hosts are reported.Notes

-on the feeding behavior and capture of hosts, and procesiing of

parasitic worms are also included.

INrnooucrroNThis study was designed to investigate the helminth parasites of

the suckers (Catostomidae) of the Gila River System, Arizona (Amin,1968). Three introduced species of buffalofish of the genus lctiobusand two native species of the genus Calostomuss were utilized. Onlyone species of caryophyllaeid cestode, Isoglaridacris hexacotyle(Linton, 1897), has been previously reported from the genus Catosto-mus in Arizona (Linton, 1897; Hunter, 1930; Mackiewicz, 1968).No helminths had been reported frorn Arizona buffalofish; apparentlythese have not been examined for parasites since their introduotioninto Roosevelt Lake, Arizona, in 1918. The helminth parasites of thebuffalofish {rom Roosevelt and Apache Lakes on the Salt River arereported herein, those o{ the native suckers from the Upper andLower Salt, Verde, and San Pedro Rivers, tributaries of the GilaRiver system, will appear in subsequent publications.

Mernnrer-s eNo MBrrrorsFish were captured by netting or by boat shocking using the current

from a 230-v, 2650-3000-w generator. After capture and transfer to

1 Abstracted from a dissertation submitted in partial fulfillment of therequirements of the Doctor of Philosophy degree in Zoology at Arizona StateUniversity.

2 Present address: Virology Section, National Communicable Disease Center,Atlanta, Georgia 30333.

3 The genus Pantosteus is considered a subgenus of the genus Catostomus,as has been established by Smith (1965) on morphological and osteologicalgrounds, which had been suggested earlier by Miller and Evans (1965) on thebasis of brain morphology.

188

1969 AurN: Hnr-lrrNrss rnolr BurreLoFIsH 189

the laboratory in coolers, the fish were sorted. Quick freezing wasfound to be destructive to their viscera. They were kept in ice anddissected to examine all body tissues and organs as soon as possitrleafter capture.

Upon recovery worrns were placed at once in warm 70/o ethylalcohol and then processed and stained with Semichon's carmine asdescribed by Cable (1955), with some modifications. After usingascending concentrations of alcohol for dehydration, the worrns werefurther dehydrated in lo0/o alcohol for 2-3 hours before mounting;two or three changes of alcohol were made.

Rrsur-rs AND DrscussroNBufalofish examined.-Buffalofish eggs (unknown species) were

planted in Roosevelt Lake in 1918 by the U. S. Bureau of Fisheries(Lowe, 1964) . Although they were reported in all four lakes on themain stream of the Salt River, Rooswelt, Apache, Canyon and SahuaroLakes, only the first two lakes appear to be significantly populated bythem. The three species of buffalofish,I. cyprinellus, I. bubalur, andI. niger, inhabit Apache Lake (collected at Burnt Corral) , whereasRoosevelt Lake appears populated only by I. cyprinellu,s (collected atTonto, Grape Vine, and 3 Bar) . Collection data are partially includedin Table 1.

Buffalofish "do not confine their feeding to any particular depthbut frequent those levels where the desired or required food is to befound" (Canfield, 1922). I. cyprinellus (with a large terminal mouth)is predominantly a zoo-plankton feeder (Moen, 1954; Minckley, 1967) ;zoo-plankton is usuallv above 95a/o of the food volume with a pre-dominance of Entomostraca (McComish, 1967). I. bubalus andI. niger (with small subterminal mouths) have similar food habitsbut feed somewhat more on benthic invertebrates (Koster, 1957:Minckley, 1967) ; zoo-plankton supply about one-third of their foodvolume (McComish, 1967). Diet does not appear to be affected bybuffalofish size (age), collection method, or area of capture (McCom-ish, 1967). Mouth position and diet are related to at least part of thepaiasitic'fauna. Accordingly, I. cyprinellu.r is placed into one group,and I. bubalzs and I. niger into another for analysis of parasitic fauna.

Nematobothrium texomensis Mclntosh and Self, 1955

This parasite was first reported from the ovary of I. bubalus f.romLake Texoma, Willis, Oklahoma, by Mclntosh and Self (1955) ; ithas also been reported from 1. bubalus and 1. cyprinellus in LakeTexoma by Self and Campbell (1956), and from the same species andI. niger in Lake Texoma and the Red River by Self et al. (1963). InArtzona, N. texomensrLr is herein reported frorn the three species ofbuffalofish from Apache Lake and from I. cyprinellus, in RooseveltLake (Table 1). These are new locality records.

All the worms recovered in this study appear to be remnants ofdegenerate infections from a previous year. They occurred most fre-

190 Trre ArrrftlceN Mrorexp Narunlr,rsr s2(r )

quently in the gotradal blood vessels and lgs frequently in intestinalmesenteric blood vessels ahd other tissues. They were opaque white orgreyish brown worms of varlorrs shapes, generally disterided with eggs,and attaining a maximum length of 3 cm and width of 1.0 cm. Theeggs were described by Self et aI. (1963); who classed them'as eitherunfertilized and nonViable, measuring 13 to 20 p in diameter, orfertilized, viable, and operculated, in'easuring 26 to 30 p in'diameter.Eggs examined by me were all misshapen; their measurements corre-sponded to those of the nonviable category delcribed above.

Self et al. (1963) recovered only fully adult w-orms, mainly fromthe lumina and lamellae of gravid ovaries and infrequently from ma-ture testes. There are Some difference3 betvfe'en their results and thoseof the pr'esent study. Fintly, the c'urrent iesults show an almo^ gt equalfrequ.ency of infection in males (+1.54%) and in females (38.7L%)(Table 1). Secondly, p mush higher incidence of lbcalizatiqn outsidethe.gonads is report'ed.here than ebserved by $elf et aL (1963). Of the39 infected fish; 32 (82.1%) suffered gonad infections, 19 (58.7%)

Trsr-e l.-Infection with Nematobothtium texomensis of 96 buffalofishfrorn .Rooievelt and Apache Lakes; Arizona, in relation to ho'st size and sex

RooseveltLake

Lcyprinellu!

.Apache Lake

Total

Size*andsex

I.cyprinellus

I.'bubalus

I.niger

bmallExaminedInfectedPercentage

MediumEiaminedInfectedPercelttage

LargeExaminedInfectedPerc'entbge

MaleiExaminedInfectedPercentage

FemalesE:taminedInfectedPercentage

Torer-ExaminedInfectedPercentage

253

12.00

600

21

50.00

28a

t+.28

500

.lJ

412.12

l49

64.28

,411

70.83

42

50.00

26l973.08

169

56.25

422866.66

92

22.22

42

50.00

000

I3

.) J. J.l

I25.00

l.l

,30.70

a

IJJ.JJ

52

40.00

21

50.00

481+29.r7

JI

2054.05

1l5

45.+5

652741.54

3119

38.71

963940.62

000

6a

.f.)..).1

B

J

37.50

I Sizes small, medium, and large represent three host size classes of 15-20.20-25, and 25-30 inches, respectively, in total length.

r969 AlrrN: Hrr"urr.ltns rnou Bqnner-on'rsH 191

rpgsenteric blood vessel infectbns, +d 5 (\7.8/6) liver and air bladderserosa nfectigns, Thesg resuks sugge$t that although the cycle of thewgrrq r} the 6sh-host is probably terminated in the gonads, the'wornsmust undergo more extensive migration in this host, particularly in theintestinal mesenteric area, than has been assumed. Thirdly, the presentstudy shows that in 31 ;i the 3.2 hosts suffering. fiom gonadaf ittf".-tions, both males and females, the infections *ere limited to .qonadalblood vessels. In only one host were worms present in the lumini of theovary.. Specimens encountered in the intestinal mesenteries were alsocontaine{ within hlood vessek The incidence in blood vessels is muc}rtog hrgh to be attrihuted to random migration. Fgrtheq Self' (personalcoqrmunication) mentiorrs that in some Oases, he suspected that wormswere present in the posrcardinal veins. This suggests that these trema-todes utilize the crrculatory system during part of the life cycle in thefish.host.

No srgnificant relationships were found between sites of infectionand the season or the hreeding conditions of the firh-hosts. No suchrelationships were expected since all worms appeare{ to be localizedrelics of prior infections. whith could be r"co.r"*"d at any time.

The iailure to find vi4bJe adults in the present study is somewhatpuzzlilg and. this problem requires further stud'y.

N. ibxornensis wal previously recorded onl;y once f.rom the threespecies of buffalofish (Sel$ qt a!,,1963), but no data concerning para-site abundance were given. Cornparison of the incidence of i4feqtion ofthe three species of buffalof,q\ in {,pache Lake shows I:. cyprinellus tobe more frequently infected (66'.66%) than I. bubalus $A.7Vfo) or1", niger (37.50/a). No co.nclusfons could be drawn as to the effect ofhost size on parasites because of the small number of host itrdividualsrepresenting bach size clars. There i3, however, an apparent tendenc).for larger fish to be more frequently infected than smaller ones(Table 1).' 'The parasite was observed to. block blood vessels in which it islggalized and sould qause se4ious host tissue C,quqq4ge, p3rtlc\rlarly inthe gonads. Such conditions were more noticeable in I. cyprinellusfrorn Apache Lake.

Glaridacris con,fusus Hunter, 1929

Since the comprehensive description by Hunter ( 1930) , G. coef usushas been reported from various hosts from the Mississippi Riverdrainage and the New York area. Due to erroneous identificatigns, tl,renumber of hosts from which this parasite has been reported is fewerthan previously assumed (Mackicwicz, 1960) . G. confusu.i has beenreported from eight vertebrate hosts (Mackiewicz, 1961). Among thebuffalofish, it was reported in 1. bubalus,less often in I. cypinellus, andrarely in I. niger by Self anS Campbel (1956) frorn Lake Texoq,ra.The three species o'f buffalofish in Arizona la"kes were all infectgfl (newlogality records) ; Table 2 shows the order of inci{ence of infeciion.

This was the only species of caryophyl'laeid cestode found in the

r92 Trrn ArrnnrceN Mror-eNo Nerunelrsr 82(t )

three species of Arizona buffalofish, introduced about 50 years ago,whereas Mackiewicz (1964) reported eight species of Caryophyllaeidaein I. bubalus and I. cyprinellus frorn Lake Texoma. This pattern sug-gests that the parasitic fauna of fish is reduced following introductioninto new habitats. According to Dogiel et al. (1961), this is probablybecause "the distribution of the intermediate host does not coincidewith that of the final host: the parasite cannot exist in the areas frourwhich either host is absent."

From whole mounts, I took measurements of the local populationof mature worms frorn Apache and Roosevelt Lakes. The total lengthranged between 0.90 and 4.69 mm (mean 2.150, N : 105). Thelength of the pre-vitelline region (the distance between the anteriorend of the scolex and the anterior tip of the first vitelline sland ortestis, whichever is anterior-most) ranged between 0.25 and d.94 rn-(mean 0.560, N : B3). The length of the post-vitelline region (thedistance between the first vitelline gland, or testis, and the hind endof the body) ranged between 0.65 and 3.75 mm (mean 1.590, N :83). Scolex width ranged between 0.22 and 0.94 mm (mean 0.598,N : 70) . Width at uterine coils ranged between 0.16 and 0.69 mm(mean 0.474, N : 81). Width at male gonopore ranged between 0.20and 0.77 mm (mean 0.461, N : Bl). Width below scolex (neck)ranged between 0.18 and 0.65 mm (mean 0.446, N : 70). While thebody outline was more or less stable, the scolex assumed a variety ofshapes (Fig. 1A) the most cornmon of which is illustrated in Figure lD.Figure lB shows a profile view of the scolex. Scolex length rangedbetween 0.20 and 0.77 mm (mean 0.473, N : 70). Cirrus sac widthransed between 0.04 and 0.14 mm (mean 0.100. N : 53). The out-line"of the immature !\'orms (Fig. lC) differed conspicuously fromthat of the mature worms. In the immatures. the scolex was the widest

Tanr-B 2.-Infection of 96 buffalofish examined from Roosevelt and ApacheLakes, Arizona, with Glaridacris confusus

RooseveltLakeI.

cyprinellus

Apache LakeI. I.

cyprinellus bubalusI.

nigerTotal

No.examinedNo.infectedPer centinfectionParasitesrecoveredRange perhostMean perhost

JJ

A

1q 1'

o

0-5

0.24

42

3

7.t4

+

0-2

0.09

38.46

52

0-22

4.00

75.00

90

0-34

1 1.25

1 8.75

t54

0-34

1.60

96

1B

8

6

13

5

1969 Alrrx: Hn'r-lrrNrrrs rnorvr BunreloFrsg

CDFig. l.-Glaridacris conlusur from the three species of buffalofish in Apache

and Roosevelt Lakes, Arizona. A. Variation in shape of scolex. B. Profile of ascolex. C, Immature worms. D, A whole mature worm. Abbreviations: CS:cirrus sac; EP: excretory pore; ESV: external seminal vesiclel FGP: femalegonopore; GpOT: glandular portion of ootype; MGP: male gonoporel O:ovary; POV: post-ovarian vitellaria; T: testis; IJ: uterus; Va: vagina; Vi:vitelline gland; VD: vas deferens.

193

place, the unpronounced neck and the uterine coils region rankedsecond and third in width, respectively.

All worms were weakly attached to the mucosal folds of the smallintestine, and were readily washed away.

In Apache Lake .I. cyprinellus was less frequently infected (7 .l+%)than 1. bubalus (38.+6%) and .L niger (75.0A/o) (Table 3). Thesepercentages correspond with the mean parasite burden per host(Table 2). All three species seem to have the potential to serve as thefinal host for G. confisus. Quantitative differ-ences in frequency andrate of infections appear to be related to differences in the feedingbehavior and the diet of the three host species as catesorized into twogroups earlier, I. cyprincllus in one group and l. bubilus and I. niger

r*\t/\rj

N

s'R4ryB

19,[ Trrn AunnrcAN MTDLAND N.,4-rune.Lrst 82(r )

sex of 96 buffalofish frqm bn4 A Ari

R,goseyeltLakeI.

in thg other group. I. niger might appear to be signifipantly mgre fr91quently infected than 1. bubalus; $owever,. the I. bqbalzs e;amingd(9, small and 4 +edium) wEre cor\sidqrably smaller than the I. niger(3 medium and 5 large) . Thpsp lpger fiphes. wqrld consume l4r-gervolmmes of food organrims (includ,'ng the infected iptermediate h,osts) .

Also, the age of the larger fish-hosrs n directly associaled with thecurnulative pa.rasitic infeqtions i{ the life span of the parasite is lqng.

G. conlusus was wea.kly attache{ to the intestinal wall and signq ofobservable tissue pathology were lacking.

Ffuures in Table 3 suggest a tendency for larger fish to be morefrequently infscted'than smaller ones. Such a tendgncy might be dueto the increased' volumq qf food org4nisms, i+clu.d,pS thg igtgqmediaJehoats engulfed by the larger fish, and also to the cumulative effect ofparasitic infections in the older and larger fish. The incidence of infec-iion in the medium;size groups is lorg,-ppopably because 30 of the 37infected fish of' this We lyeqe 1,. cyprinslluS ghich is the least frequentlyinfected species.

Acknowledgments.-I am grateful to my advisory committee at the Depart-ment of Zoology, Arizoni State Uniyersity, particularly Dr. E. J. Landers for

Tesr,E 3.-Infectign with Glaridac.ris confusu,s in relation to, ho.st. size and

Sizeandsex

Apache. LakeI. I.

bubalusI.

nigerTotal

cyprinellus cyPrinellusSmall

ExaminedInfectedPercentage

MediumExaminedInfectedPercentage

LargeExaminedInfected.Percentage

MalesExaminedInfectedPercentage

FemalesExaqnined"InfectedPercentage

Torer-ExaminedIniectedPercentage

254

16.00

600

I

00

2B'^I

t+.28

500

JJ

12.t2

141

7 il4

242.8;33

400

262

7.69

161

6.2!

423

7.14

9J

JJ.JJ

A

2

5,0.00

l35

38,46

5A

80.00

a

I50.00

E.5

83,33

B

675.00

4B1020.83

3t

10.81

l14

36.36

651015.38

q1

B

25.e1

961818.75

000

2

66.66

95

55.55

400

000

1969 ArurN: Htr.lrrNrrrS rno*r BurpeLoI'IsH 195

technical help arrtl :rtlvice and Dr. Id. L. Minctley for making fish collectionsavailable for this .study, through a Bureau of Commercial Fisheries Progrqry.I. am also grateful to Professor H. W. Manter,- Department of Zoology andPhysiology, University of Nebraska, for irid in identification of N. texomensisand Profeisor J. S. Mackiewicz, Departmbnt of Bioldgical Sciences, State Uni-versity of New York at Albany, for his ionstent advice as well. as his aid inthe identification of G. ''ionfusus. Further, I rnould like to gratefully acknowl-edge the financlal assistance of the Depaitment of Zoololy through the awardofl Faculty Associateship; the financial assistance io cover field transportationcosts provided by Dean Karl Dannenfeld't of the College of Liberal Arts; andthe assisiance providdd by the G'faduate College in the award of Out-of-State

Juition Scholarships between 1965 and 1967, a Foreign Graduate StudentScholarship for the academic year 1965-1966, and the award of a SummerFellowship for Graduate Teaching Assistants for the summer of 1967.

REFERENaEsArurN, O. M. 1968. Helminth fauna of suckers (Catostomidae) of the Gila

River System, Arizona. Ph.D. thesis, Arizona State University, Tempe.202 p.

Cenr-r, R. M. 1965. An illusuated laboratory manual of parasitolo3y. BurgessPubl. Co., Minneapolis. 165 p.

Ce.rsnrrro, H. L. 1922. Care and feeding of buffalofish in ponds. Dep. Com'merce, Bur. Fish., Econ. Circular, No. 56. 3 p.

Docrnr-, V. A., G. K. Pnrnusrrtvsr(r AND Yu. I. Por,vaNsxr. 1961. Parasi-tology of fishes. lst English ed. (1961). Oliver and Boyd, London.384 p.

HuNron, G. W., III. 1930. Studies on the Caryophyllaeidae of North Amer-ica. Illinois Biol. Monogr., No. 11. 186 p.

Kosrnn, W. J. 1957. Guide to the fishes of New Mexico. Univ. of New Mex-ico Press, Albuquerque. 116 p.

LrNroN, E. 1897. Notes on cestode parasites of fishes. Proc. U.S. Nat. Mus.,2O:423-456.

Lown, C. H. 1964. The vertebrates of Arizona. Univ. of Arizona Press,

Tucson. 259 p.McCoursu, T. S. 1967. Food habits of bigmouth and smallmouth buffalofish

in Lewis and Clark Lakes and the Missouri River. Trans' Amer' Fish.Soc.,96:70-74.

MclNrosrr, A. eNo J. T. Solr. 1955. Nematobothrium texornensis n. sp. froma freshwater frsh, Ictiobus bubalus (Rafinesque, 1819). Program andAbstr. 30 Ann. Meet. Amer. Soc. Parasitol., Atlanta, Georgia, Dec.27-30). /. Parasitol., 41, Suppl. 6(2) :36-37.

M.lcrrrwrcz, J. S. 1960. Studies on the Caryophyllaeidae (Cestoidea) ofCatostomus commersoni (Lacepede), with emphasis on those fish nearIthaca, New York (Tompkins County), U.S.A. Ph.D. thesis, CornellUniv., Ithaca, New York. 391 p.

1961. A brief summary of the North American Caryophyllaeidae(Cestoidea) and their vertebrate hosts. Wiadomoici Parazytologiczne,7 t839-M2.

1964. Variations and host-parasite relationships of Caryophyllaeids(Cestoidea) from fish of Lake Texoma, Marshall County, Oklahoma.l. Parasitol.,5o (3, sec. 2):31. (Abstract No. 46.)

1968. Isoglaridacris hexacotyle cornb. n. (Cestoidea: Caryophyllidea)from catostomid fishes in southwestern North America. Proc. HeI-minthol. Soc. W ashington, i5 I 93-196.

196 Trrn AlrnnrceN Mrnr-eNo Naruner.rsr 82(r)

Mrlr,nn, R. J. eNo H. E. EveNs. 1965. External morphology of the brain andlips in Catostomid fishes. Copeia,4:467-487.

MrNcxr-r,v, W. L. 1967. Investigation of commercial fisheries potential inreservoirs. Basic life history studies. A quarterly progress report sub-mitted on 4/10/67 to the U.S. Dept. Interior, Fish and Wildlife Serv.,Bur. of Commercial Fisheries. 26 p.

Mor,w, T. 1954. Food of the bigmouth buffalo, Ictiobus cyprinellus (Valen-ciennes), in Northwest Iowa Lakes. Proc. Iotaa Acad. Sci.,6l:561-569.

Srr-r, J. T. eNo J. W. C.urnnnrr.. 1956. A study of the helminth parasites ofthe buffalofishes of Lake Texoma with a description of Lissorchisgallaris n. sp. (Tremato.da: Lissorchiidae) . Trans. Amer. Microsco.p.Soc.,75:397-401.

L. E. Pnrrns eNo C. E. Devrs.adult of Nematobothrium texomensissitol., 49 t731-736.

Surrn, G. R. 1965. Distribution and evolution of the North American fishesof the subgenus Pantosteus. Ph.D. thesis, Univ. of Michigan, AnnArbor.

SusMrrroo 29 Frrnuanv 1968 Accnprno 12 JuNr 1968

1963. The egg, miracidium, and(Trematoda: Digenea). l. Para-