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Mass Mortality of Fishes in Lake

Titicaca (Peru–Bolivia) Associated
with the Protozoan Parasite
Ichthyophthirius multifiliis
a b
Wayne A. Wurstbaugh & Rene Alfaro Tapia
a
Department of Fisheries and Wildlife/Ecology Center , Utah
State University , Logan, Utah, 84322, USA
b
Instituto del Mar del Peru, Lahoratorio Regional de Puno ,
Apartado 292, Puno, Peru
Published online: 09 Jan 2011.

To cite this article: Wayne A. Wurstbaugh & Rene Alfaro Tapia (1988) Mass Mortality of
Fishes in Lake Titicaca (Peru–Bolivia) Associated with the Protozoan Parasite Ichthyophthirius
multifiliis , Transactions of the American Fisheries Society, 117:2, 213-217, DOI:
10.1577/1548-8659(1988)117<0213:MMOFIL>2.3.CO;2

To link to this article: http://dx.doi.org/10.1577/1548-8659(1988)117<0213:MMOFIL>2.3.CO;2

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 fransactitrns of the American Fisheries Society 1 1 7 : 2 1 3 - 2 1 7 . 1988
c Copynghi by ihc Amencan Fisheries Society 1988

Mass Mortality of Fishes in Lake Titicaca (Peru-Bolivia)

Associated with the Protozoan Parasite
Ichthyophthirius multifiliis

WAYNE A. WURTSHAUGH limnological investigation, we noted large num-

Department of Fisheries and
Wildlife/Ecology Center
Utah State University
Lagan. Utah S4322. USA
RENE ALFARO TAPIA
Institute* del Mar del Peru
Downloaded by [Harvard Library] at 03:40 27 April 2015
bers of dead fish floating on the surface of Lake
Titicaca, Peru-Bolivia. Here we describe this mass
mortality of native fishes that was apparently
caused by 7. multifiliis.
Lake Titicaca is located at an elevation of 3,812
m in an enclosed basin of the Peruvian and Bo-
livian Andes. Despite its tropical location, water

Lahoratorio Regional de Puno temperatures seldom exceed 17°C. The lake cov-
Apart ado 292. Pit no, Peru ers 8,100 km 2 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 fishes were slightly affected. Ichthyophthir- 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 deciembre de 1981, una epidcmia cau- populate only a tributary stream. Lake trout Sal-
sada por el parasite Ichthyophthirius 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 dc altura. Adultos de O. agassii. especie de im- 1979). A final exotic species, the pejerrey Basil-
portancia comercial. y abundante en la zona literal, 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 literal no fueron afectados notoriamcntc. Evi-
dcncia limitada sugicre que /. multifiliis fue introducido Cousteau and Diole (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
fishes. One organism spread widely by fish is the mention what parasites were observed. Villwock
ciliated protozoan Ichthyophthirius multifiliis, (1972) also suggested that the introduction of an
commonly referred to as Ich (Hoffman 1970). This unspecified "sporozoen" parasite to Titicaca had
parasite penetrates the skin and gill epithelium of killed endemic fishes, but he provided no sup-
fish and causes mortalities when rates of infesta- porting data.
tion are high (Amlacher 1970). Hoffman and
Schubert (1984) consider it to be the most dan- Methods
gerous freshwater parasite of cultured fishes, but To estimate the extent of the mortality, we sam-
epizootics of /. multifiliis in wild fishes are only pled dead and dying fish in Puno Bay (Figure 1)
rarely reported (Elser 1955; Allison and Kelly on 28 December 1981. Seven transect sites were
1963). In December 1981, during the course of a chosen haphazardly (without regard to fish den-
211
 214
70° W
16° S
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10 20 30 km
70° W
FIGURE I.—Map of Lake Tilicaca showing the areas where fish parasitized by Ichthyophthirius multifiliis were
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
of 100-200 m, we counted and sampled dead and
moribund fish within 5 m of each side of the boat.
Six of the transect paths were perpendicular to the
edge of the reed community (Scirpus tatora) that
borders much of the lake. The seventh transect
was parallel to the reeds so that the fish that had
washed up against the vegetation could be sam-
pled. The fish collected were identified by refer-
ence to Tchernavin (1944) and Parent! (1984). The
parasites on the fish were excised, and were iden-
tified by reference to Richenbach-Klinke (1973).
Fish standard lengths were measured and con-
verted to wet weights with length-weight regres-
sions developed by H. Trevino (Instituto del Mar,
unpublished data).
NOTES
69° W
16° S
69° W
Most of the fish observed were blown against
the emergent vegetation. Consequently, to esti-
mate the lake-wide mortality, we calculated the
number of dead fish counted per meter of shore-
line sampled, and extrapolated this to the shore-
line of the entire lake basin. Because we sampled
only a small area of the lake, our estimate may be
quite biased. Nevertheless, because the epizootic
was observed in two distant portions of the lake
(see below), we made the lake-wide estimate to
demonstrate the potential magnitude of the fish
kill.
Results and Discussion
The fish mortality was first noticed in Puno Bay
on 22 December 1981, and it continued at least
 NOTES 215

TABLE 1 .—Total numbers of dead fishes collected on seven transects in Puno Bay (Lake Titicaca) on 28 December
1981, and the estimated lake-wide mortality during the epizootic of Ichthyophthirius multifiliis. The juveniles of
all species of Orestias are pooled into one group.
Fish collected from Puno Bay Estimated lake-wide mortality
Mean numbcr/m of Mean Numbers Mass
Species Total % of total shoreline (SE) weight (g) (millions) (tonnes)
Orestias agassii 3.574 93.0 14.44(4.00) 11.7 16.5 193
O. mulleri 24 0.6 0.34(0.12) 12.7 0.4 4
O. luteus 113 2.9 0.30 (0.32) 12.0 0.3 4
O. albus 23 0.6 0.20(0.15) 8.9 0.2 2
O. olivaceus 80 2.1 0.16(0.01) 3.2 0.2 1
Orestias spp. juveniles 10 0.3 0.01 (0.11) 2.0 0.01 <0.1
O. ispi (adult) 1 0.0 0.01 (0.01) 3.2 0.01 <0.1
Basilichthys honariensis 15 0.5 0.09 (0.07) 11.6 0.1 1

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 km to the south of Puno cause the life cycle of /. multifiliis includes a ben-
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Bay. Consequently, the epizootic lasted at least 6
d and extended over much of the lake. All of the
fish were heavily infected with /. mutifiliis: one
14-cm O. agassii was covered with more than
1,800 protozoans. A secondary infection of an
unidentified fungus was also present on some
fish, but there were no other obvious pathological
symptoms.
The epizootic killed large numbers of fish. On
the 260 m of shoreline surveyed, we observed
3,840 dead fish, primarily Orestias spp. (Table 1).
The lake-wide estimate of fish mortality was 18
million individuals and 206 tonnes. However,
these figures could have underestimated the total
impact, because moribund fish may have sunk to
the bottom of the lake, making them unavailable
to our sampling technique.
We observed seven species offish infected with
the parasite, but 93% of the fish collected were
adult O. agassii (Table 1). This species is among
the most abundant of the littoral zone fishes
(Loubens et al. 1984; Trevino et al. 1984), and it
constitutes 70% of the fish yield in Lake Titicaca
(Alfaro et al. 1982). The estimated mortality of
this species, 193 tonnes, represents 6% of its an-
nual yield to the fishery (Alfaro et al. 1982). We
found few O. agassii in juvenile size-classes. Other
codominant littoral zone fishes such as O. luteus
and O. olivaceus apparently were not greatly af-
fected by the epizootic, as they represented only
1.7 and 0.8% of the dead fish collected. Similarly,
we found few pejerrey, which are abundant in both
the littoral and pelagic zones (Loubens et al. 1984;
Vaux et al. 1988). No dead rainbow trout were
found, but they are rare in relation to the other
fishes, particularly in Puno Bay (Trevino et al.
1984). Only 0.1% of the affected fish were O. ispi.
thic cyst from which the mobile infective stages
develop, it is not surprising that pelagic fishes such
as O. ispi were rare in our collections.
We have observed low mortalities of fishes in
the lake during the warm season (November-Jan-
uary) in other years, but the cause of the major
epizootic in 1981 is unclear. Often, unusually high
or low temperatures cause stress that can precip-
itate diseases in fish (Snieszko 1974). Offshore sur-
face temperatures in the middle of Puno Bay at
the time of the outbreak were 15-17°C, and the
diurnal temperatures in the shallow littoral vege-
tation probably exceeded this. These temperatures
could have contributed to the epizootic, because
/. multifiliis reproduces rapidly between 12-27°C
(Baueret al. 1973). Nevertheless, it is unlikely that
temperature alone triggered the disease, because
temperatures in the bay during the outbreak were
comparable to those observed in the summers of
1980-1981 and 1982-1983 (Vincent et al. 1986),
when only limited mortalities were noted.
Another potential stressor that could have pre-
cipitated the disease was the spawning activity of
O. agassii. As mentioned previously, very few ju-
venile fish were found, and most of the adult O.
agassii that we collected were either gravid or
spent. Because fish frequently shunt energy to the
ovaries and stop feeding during spawning (Woot-
ton 1985), and because malnourished hosts are
less able to mount effective immunological re-
sponses to infections (Anderson 1982), this may
have facilitated the /. multifiliis outbreak in O.
agassii.
The origin of /. multifiliis in Lake Titicaca is
unknown, but it is likely that it arrived with the
exotic fishes, because both salmonids (Amlacher
1970) and atherinids (Fistolera 1946) are carriers
 216
of the parasite. Fish introductions are believed to
have spread this protozoan nearly worldwide from
its origins in Asia (Hoffman 1970).
The introduction of exotic fishes into Lake Ti-
licaca has been accompanied by several changes
in the native fish fauna. Orestias cuvieri, which
was the largest (up to 220 mm long) and one of
the most important food fish in the lake before
the introductions (Tchernavin 1944), is now pre-
sumed extinct (Alfaro et al. 1982). The relative
abundances of other species have also changed
radically (Alfaro et al. 1982; Vaux et al. 1988).
The reasons for these changes are not clear, but
predation by and competition with the rainbow
trout and pejerrey have been suggested (Laba
1979), as has the development of gill-net fisheries
which followed the introductions (Levieil 1987).
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The possible introduction of /. multifiliis with the
introduced fishes may have also contributed to the
changes in the native fish community.
Information on Lake Titicaca before the intro-
ductions is so limited that it is doubtful we will
ever know the relative impact of exotic fishes, dis-
ease, and increased fishing on the native fauna.
Rainbow trout and pejerrey introductions into
Lake Titicaca have allowed important commer-
cial fisheries to develop, and this has benefitted
some segments of the society. However, the ad-
dition of exotic fishes always carries unforseen risks
(Moyle et al. 1986). In this case, the result may
have been the introduction of/, multifiliis and the
subsequent loss of millions of commercial fish.
Acknowledgments
We thank D. Levy, D. Neverman, L. Parenti,
and D. Levieil for reviewing the manuscript and
H. Trevino Bernal and J. Torres for assisting with
the field survey. E. Flores and E. Moreno edited
the Spanish resumen. The research was partially
funded by a National Science Foundation grant
(DEB 7921933) to P. Richardson and by funds
from the Instituto del Mar del Peru.
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