r: nsaCiions oJ the America n Fisheries Society 11 7:2 13-217. 1988 c'~OPYright by the American Fisheries Society 1988

Mass Mortality of Fishes in Lake Titicaca (Peru-Bolivia) Associated with the Protozoan Parasite I chthyophthirius multifiliis

WA YNE A. WURTSBAUGH limnological investigation, we noted large num­ Department of Fisheries and bers of dead fish floating on the surface of Lake Wildlife/Ecology Center Titicaca, Peru-Bolivia. Here we describe this mass Utah State University mortality of native fishes that was apparently Logan, Utah 84322, USA caused by I. multifiliis. Lake Titicaca is located at an elevation of3,812 RENE ALFARO TAPIA m in an enclosed basin of the Peruvian and Bo­ Instituto del Mar del Peru livian Andes. Despite its tropical location, water Laboratorio Regional de Puno temperatures seldom exceed 17°C. The lake cov­ Apartado 292, Puno, Peru ers 8, I 00 km2 and has a 1,140 km shoreline (Rich­ erson et al. 1986). The fishes and other resources Abstract. - In December 1981 , an epizootic of the pro­ of Lake Titicaca are an important part of the econ­ tozoan parasite Ichthyophthirius multifiliis killed an es­ omy for the one million people living in the basin. timated 18 million killifish Orestias spp. in Lake Titi­ There are 30 native and several introduced fish caca, a high-altitude tropical system. Of the dead fish collected, 93% were adult O. agassii, a commercially species in the Titicaca watershed. The natives are important species that is abundant in the littoral zone. dominated by 28 species of small killifish of the Juvenile Orestias spp., pelagic species, and some other genus Orestias, of which 23 are endemic to the littoral zone fis hes were slightly affected. lchthyophthir­ drainage (Parenti 1984). Rainbow trout Salmo ius multifiliis was probably introduced with exotic fishes gairdneri were introduced into Lake Titicaca in brought to Lake Titicaca in the 1940s and 1950s. 1941 and are now common (Everett 1973). Brown trout S. trutta were stocked in 1939, but presently Resumen. - En deciem bre de 1981 , una epidemia cau­ populate only a tributary stream. Lake trout Sal­ sada por el parasito lchthyophthirius multifiliis mato un estimado de 18 millones de "killifish" del genero velinus namaycush were also introduced between Orestias en el Lago Titicaca (Peru-Bolivia), un sistema 1939 and 1941 , but now are rare or absent (Laba tropical de altura. Adultos de O. agassii, especie de im­ 1979). A final exotic species, the pejerrey Basil­ POrtancia comercial, y abundante en la zona litoral, re­ ichthys bonariensis, a large atherinid from Argen­ presentaron el 93% de los peces muertos colectados. Ju­ tina, was stocked in the basin and became abun­ veniles de Orestias spp., especies pelagicas, y otros peces dant in the lake by 1955 (Alfaro et al. 1982). de la zona litoral no fueron afectados notoriamente. Evi­ dencia limitada sugiere que I. multifiliis fue introducido Cousteau and DioU: (1973) reported seeing large en la cuenca junto con peces exoticos en los anos 1940- numbers of dead Orestias spp. during an expedi­ 1950. tion to Lake Titicaca in 1968, and they noted that fish suffered from "parasites and from furuncu­ Many parasites are inadvertently transported to losis, which was perhaps transmitted by the trout new environments by the introduction of exotic with which the lake was stocked." They did not fi~~es. One organism spread widely by fish is the mention what parasites were observed. Villwock Ciliated protozoan Ichthyophthirius multifiJiis, (1972) also suggested that the introduction of an COmmonly referred to as Ich (Hoffinan 1970). This unspecified "sporozoen" parasite to Titicaca had ~Site penetrates the skin and gill epithelium of killed endemic fishes, but he provided no sup­ Sh ti and causes mortalities when rates of infesta­ porting data. s:: are high (Amlacher 1970). Hoffman and ubert (I984) consider it to be the most dan- Methods egerous . fr es h water parasite. of cultured fishes, but To estimate the extent of the mortality, we sam­ r:;ZOotics of I. multifiliis in wild fishes are only pled dead and dying fish in Puno Bay (Figure 1) 19;~Y reported (Elser 1955; Allison and Kelly on 28 December 1981. Seven transect sites were ). In December 1981, during the course ofa chosen haphazardly (without regard to fish den- 214 NOTES

69°W

16° 5 16°S

oi _ 10 20 _ 30 km

WW ~W FIGURE I.-Map of Lake Titicaca showing the areas where fish parasitized by Ichthyophthirius multifiliis" collected in Puno Bay (A, B) or were observed near the town of Desaguadero (C). sity) in two sections of the bay. On each transect Most of the fish observed were blown a~ of 100-200 m, we counted and sampled dead and the emergent vegetation. Consequently, to estfJ moribund fish within 5 m of each side of the boat. mate the lake-wide mortality, we calculated the Six of the transect paths were perpendicular to the number of dead fish counted per meter of shoro­ edge of the reed community (Scirpus tat ora) that line sampled, and extrapolated this to the borders much of the lake. The seventh transect line of the entire lake basin. Because we sarnPl- 1 was parallel to the reeds so that the fish that had only a small area of the lake, our estimate may washed up against the vegetation could be sam­ quite biased. Nevertheless, because the CO,'l£"'''­ pled. The fish collected were identified by refer­ was observed in two distant portions of the enceto Tchernavin (1944)and Parenti (1984). The (see below), we made the lake-wide estimate parasites on the fish were excised, and were iden­ demonstrate the potential magnitude of the tified by reference to Richenbach-Klinke (1973). kill. Fish standard lengths were measured and con­ verted to wet weights with length-weight regres­ Results and Discussion sions developed by H. Trevino (lnstituto del Mar, The fish mortality was first noticed in Puna unpublished data). on 22 December 1981 , and it continued at NOTES 215

TABLE I.-Total numbers of dead fishes collected on seven transects in Puno Bay (Lake Titicaca) on 28 December 1981 , and the estimated lake-wid.e mortality during the epizootic of lchthyophthirius multifiliis. The juveniles of all species of Oresllas are pooled Into one group.

Fish collected from Puno Bay Estimated lake-wide mortality Mean number/ m of Mean Numbers Mass Species Total % of total shoreline (SE) weight (g) (millions) (tonnes)

Oreslias agassii 3,574 93.0 14.44 (4.00) 11.7 16.5 193 O. /lllIlIeri 24 0.6 0.34 (0.12) 12.7 0.4 4 O./lIlells 113 2.9 0.30 (0.32) 12.0 0.3 4 O. a/blls 23 0.6 0.20 (0. 15) 8.9 0.2 2 O. o/il'acells 80 2. 1 0.16 (0.01) 3.2 0.2 I Orpslias spp. juveniles 10 0.3 0.01 (0. 11) 2.0 0.01 < 0.1 O. ispi (adult) I 0.0 0.01 (0.01) 3.2 0.01 <0. 1 Basilichlhys bonariensis 15 0.5 0.09 (0.07) 11.6 0.1 I until our survey of 28 December. We also ob­ a small pelagic species that is probably the most served dead fish on 24 December 1981 near the abundant fish in the lake (Alfaro et al. 1982). Be­ town of Desaguadero, 130 Ian to the south ofPuno cause the life cycle of I. multifiliis includes a ben­ Bay. Consequently, the epizootic lasted at least 6 thic cyst from which the mobile infective stages d and extended over much of the lake. All of the develop, it is not surprising that pelagic fishes such fish were heavily infected with I. mutifiliis: one as O. ispi were rare in our collections. 14-cm O. agassii was covered with more than We have observed low mortalities of fishes in 1,800 protozoans. A secondary infection of an the lake during the wann season (November-Jan­ unidentified fungus was also present on some uary) in other years, but the cause of the major fish , but there were no other obvious pathological epizootic in 1981 is unclear. Often, unusually high symptoms. or low temperatures cause stress that can precip­ The epizootic killed large numbers of fish. On itate diseases in fish (Snieszko 1974). Offshore sur­ the 260 m of shoreline surveyed, we observed face temperatures in the middle of Puno Bay at 3,840 dead fish , primarily Orestias spp. (Table 1). the time of the outbreak were 15-17°C, and the The lake-wide estimate of fish mortality was 18 diurnal temperatures in the shallow littoral vege­ million individuals and 206 tonnes. However, tation probably exceeded this. These temperatures these figures could have underestimated the total could have contributed to the epizootic, because impact, because moribund fish may have sunk to I. multifiliis reproduces rapidly between 12-27°C the bottom of the lake, making them unavailable (Bauer et al. 1973). Nevertheless, it is unlikely that to our sampling technique. temperature alone triggered the disease, because We observed seven species of fish infected with temperatures in the bay during the outbreak were the parasite, but 93% of the fish collected were comparable to those observed in the summers of adult O. agassii (Table 1). This species is among 1980-1981 and 1982-1983 (Vincent et al. 1986), the most abundant of the littoral zone fishes when only limited mortalities were noted. (Loubens et al. 1984; Trevino et al. 1984), and it Another potential stressor that could have pre­ constitutes 70% of the fish yield in Lake Titicaca cipitated the disease was the spawning activity of (Alfaro et a1. 1982). The estimated mortality of O. agassii. As mentioned previously, very few ju­ this species, 193 tonnes, represents 6% of its an­ venile fish were found, and most of the adult O. nual yield to the fishery (Alfaro et al. 1982). We agassii that we collected were either gravid or found few O. agassii in juvenile size-classes. Other spent. Because fish frequently shunt energy to the codominant littoral zone fishes such as O. luteus ovaries and stop feeding during spawning (Woot­ and O. olivaceus apparently were not greatly af­ ton 1985), and because malnourished hosts are fected by the epizootic, as they represented only less able to mount effective immunological re­ 1.7 and 0.8% of the dead fish collected. Similarly, sponses to infections (Anderson 1982), this may We found few peierrey which are abundant in both have facilitated the I. multifiliis outbreak in O. th r " e tHoral and pelagic zones (Loubens et al. 1984; agassii. ~aux et al. 1988). No dead rainbow trout were The origin of I. multifiliis in Lake Titicaca is fio~nd , but they are rare in relation to the other unknown, but it is likely that it arrived with the 1~8es , particularly in Puno Bay (Treviiio et al. exotic fishes, because both salmonids (Am1acher 4). Only 0.1% of the affected fish were O. ispi, 1970) and atherinids (Fistolera 1946) are carriers 216 NOTES of the parasite. Fish introductions are believed to Anderson, R. M. 1982. Host-parasite population bi­ have spread this protozoan nearly worldwide from ology. Pages 303-31 2 in D. F. Mettrick and S. S. its origins in Asia (Hoffman 1970). Desser, editors. Parasites-their world and ours. J!I. The introduction of exotic fishes into Lake Ti­ sevier Biomedical Press, Amsterdam. Bauer, O. N., V. A. Musselius, and Yu. A. Strelkov ticaca has been accompanied by several changes 1973. Diseases of pond fishes. Translated rr-oa; in the native fish fauna. Orestias cuvieri, which Russian: Israel Program for Scientific Translationa, was the largest (up to 220 mm long) and one of Jerusalem. (Also available from the National Tecla­ the most important food fish in the lake before nicai Information Service, Springfield, Virginia.) the introductions (Tchernavin 1944), is now pre­ Cousteau, J. I. , and P. Diolt~ . 1973. Three adventura. sumed extinct (Alfaro et al. 1982). The relative GaJapagos-Titicaca-The Blue Holes. Doubleday. New York. abundances of other species have also changed Elser, H. J. 1955. An epizootic of IchthyophthirilMil radically (Alfaro et al. 1982; Vaux et al. 1988). among fishes in a large reservoir. Progressive F... The reasons for these changes are not clear, but Culturist 17: 132-133. predation by and competition with the rainbow Everett, G. V. 1973. The rainbow trout Salrno gaird. trout and pejerrey have been suggested (Laba neri (Rich.) fishery of Lake Titicaca. Journal ofF" 1979), as has the development of gill-net fisheries Biology 5:429-440. Fistolera, A. L. 1946. Observaciones sobre /cht",. which followed the introductions (Levieil 1987). ophthirius rnultifilliis Fouquet. Anales del Museo The possible introduction of I. multifiliis with the Argentino de Ciencias Naturales 62:58-90. (BueDCII introduced fishes may have also contributed to the Aires.) changes in the native fish community. Hoffman, G. L. 1970. In tercontinental and transcoa­ Information on Lake Titicaca before the intro­ tinental dissemination and trans-faunation of fiIIa ductions is so limited that it is doubtful we will parasites with emphasis on whirling disease (Myxo­ ever know the relative impact of exotic fishes, dis­ soma cerebralis). American Fisheries Society Spe­ cial Publication 5:69-81. ease, and increased fishing on the native fauna. Hoffman, G. L., and G. Schubert. 1984. Some para. Rainbow trout and pejerrey introductions into sites of exotic fishes. Pages 233-261 in W. R. C0ur­ Lake Titicaca have allowed important commer­ tenay and J. R. Stauffer, Jr., editors. Distributioa. cial fisheries to develop, and this has benefitted biology, and management of exotic fishes. Joha some segments of the society. However, the ad­ Hopkins University Press, Baltimore, Mary\and. dition of exotic fishes always carries unforseen risks Laba, R. 1979. Fish, peasants, and state bureaucrac:ia. The development of Lake Titicaca. Comparatiw (Moyle et al. 1986). In this case, the result may Political Studies 12:335-361. have been the introduction of I. multifiliis and the Levieil, D. 1987. Territorial use rights in fisbIII subsequent loss of millions of commercial fish. (TURFS) and the management of small-scale filii. eries: the case of Lake Titicaca (Peru). Doctoral diI­ Acknowledgments sertation. University of British Columbia, VanCOU­ We thank D. Levy, D. Neverman, L. Parenti, ver, Canada. Loubens, G., F. Osorio, and J. Sarmiento. 1984. and D. Levieil for reviewing the manuscript and ~ servations sur les poissons de la partie bolivienat H . Treviiio Bernal and 1. Torres for assisting with du lac Titicaca. Revue d'Hydrobiologie TropiClle the field survey. E. Flores and E. Moreno edited 17:153-161. the Spanish resumen. The research was partially Moyle, P. B., H. W. Li, and B. A. Barton 1986. 1111 funded by a National Science Foundation grant Frankenstein effect: impact of introduced fishes OIl (DEB 7921933) to P. Richardson and by funds native fishes of North America. Pages 41~26 III from the Instituto del Mar del Peru. R. H. Stroud, editor. Fish culture in fisheries mill­ agement American Fisheries Society, Bethesda. Maryland. References Parenti, L. 1984. A taxonomic revision of the ~ Alfaro, R., E. Bustamante, J. Torres, H. Trevino, and killifish genus Orestias (Cyprinodontiformes. c,. W. Wurtsbaugh. 1982. La pesqueria en el Lago prinodontidae). Bulletin of the American M~ Titicaca (Peru): presente y futuro. Food and Agri­ of Natural History 178: 107-214 . culture Organization of the United Nations, Fish­ Reichenbach-Klinke, H. H . 1973. Fish pathology: ~ eries Department, Field Document FI:DP/PERl761 guide to the recognition and treatment of di~ 022, Rome. and injuries of fishes, with emphasis on en~ Allison, R., and H. D. Kelly. 1963. An epizootic of mental and pollution problems. T.F.H. PubliCI" l chthyophthirius rnultifiliis in a river fish popula­ tions, Jersey City, New Jersey. tion. Progressive Fish-Culturist 25 : 149-150. Richerson, P. J., P. Neale, W. Wurtsbaugh, R. AI: Amlacher, E. 1970. Textbook of fish diseases. T.F.H. and W. Vincent. 1986. Patterns of temporal_.-: ...... Publications, Jersey City, New Jersey. at ion in primary production and other limnolot-l NOTES 217

variables in Lake Titicaca, a high altitude tropical Fischfauna durch Einbiirgerungs-versuche und Ak­ lake. Hydrobiologia 138:205-220. k1imatisation von Fremdfischen am Beispiel des Ti­ Snieszko S. F. 1974. The effect of environmental stress ticaca-Sees (Peru/ Bolivien) und des Lanao-Sees on outbreaks of infectious disease of fishes. Journal (Mindanao/ Philippinen). Internationale Vereini­ of Fish Biology 6: 197-208. gung fuer Theoretische und Angewandte Limnolo­ Tchemavin, V. V. 1944. A revision of the subfamily gie Verhandlungen 18:1227-1234. Orestiinae. Proceedings of the Zoological Society of Vincent, W. F., W. A. Wurtsbaugh, P. J. Neale, and P. London 114: 140-233. J. Richerson. 1986. Polymixis and algal produc­ Trevino, H., J. Torres, D. A. Levy, and T. G. Northcote. tion in a tropical lake: latitudinal effects on the sea­ 1984. Experimental fishing in littoral areas of the sonality of photosynthesis. Freshwater Biology 16: "agua negra" and "agua limpia" ofPuno Bay, Lake 781-802. Titicaca, Peru. Boletin Instituto del Mar del Peru. Wootton, R. J. 1985. Energetics of reproduction. Pages Volume 8, number 6, Lima. 231-256 in P. Tytler and P. Calow, editors. Fish Vaux, P., and seven coauthors. 1988. Ecology of the energetics. Johns Hopkins University Press, Balti­ pelagic fis hes of Lake Titicaca (Peru-Bolivia). Bio­ more, Maryland. tropica 20:220-229. Received February 1, 1988 Villwock, W. 1972. Gefahren fiir die endemische Accepted May 3, 1988