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J. Parasitol., 93(2), 2007, pp.

418–421
䉷 American Society of Parasitologists 2007

Infection of Myxobolus galaxii (Myxozoa) in Galaxias maculatus


(Osmeriformes: Galaxiidae) From Northwestern Patagonian Andean Lakes (Argentina)
Verónica Flores and Gustavo Viozzi, CONICET-UNC Laboratorio de Parasitologı́a, Centro Regional Universitario Bariloche,
Quintral 1250 (8400), San Carlos de Bariloche, Argentina. e-mail: vflores@crub.uncoma.edu.ar

ABSTRACT: The infection of Myxobolus galaxii Szidat, 1953, from the TABLE II. Seasonal sample size and mean length (⫾SD) of Galaxias
musculature and abdominal organs of northwestern Patagonian Galaxias maculatus from Lake Gutiérrez.
maculatus is described. Plasmodia are histozoic and intercellular. Spores
are pyriform in valvar view and biconvex in sutural view, with 4–9
Season n Mean length (mm) SD
edge notches in the sutural line, varying in shape within the same plas-
modium. Myxobolus galaxii was detected in fish from 7 of 17 Andean 1995
Patagonian lakes, with prevalences ranging between 2 and 17%. A re-
peating pattern of summer increment in prevalence was observed, which Summer 52 47.4 3.9
could be explained by the ontogenetic migratory movements of the fish Autumn 141 49.2 5.8
in Lake Gutiérrez. Also, accumulation of plasmodia through the life Winter 96 40.0 3.1
span of fish was detected. Spring 61 44.5 5.1
1996
Galaxias maculatus (puyen) is a circum-Antarctic fish species dis-
tributed in Chile, Argentina, Malvinas Islands, Australia, and New Zea- Summer 135 45.4 4.3
land (Berra et al., 1996). Four species of Myxobolus (Bütschli, 1882) Autumn 166 46.4 4.9
parasitizing G. maculatus (Jenyns) have been recorded: Myxobolus gal- Winter 105 42.5 4.9
axii Szidat, 1953, is from the musculature and other abdominal organs Spring 134 42.5 5.4
and Myxobolus magellanicus Szidat, 1953, is reported from the gills of
fish collected in Tierra del Fuego (southern Patagonia, Argentina); Myx- 1997
obolus iucundus Hine, 1976, was found to parasitize muscles of fish in Summer 154 44.2 5.0
New Zealand; and Myxobolus bartoni Kalavati, Brickle, et MacKenzie,
2000, was reported in the trunk musculature of specimens from the
Malvinas Islands (Szidat, 1953; Hine, 1976; Kalavati et al., 2000).
During a survey of parasites of G. maculatus from northwestern Pata- maculatus. In Lake Gutiérrez. The fish mature at 1 yr of age and spawn
gonian lakes, plasmodia containing spores like those of M. galaxii de- in the littoral zones of the lakes from early spring to early summer
scribed by Szidat (1953) were found in the musculature and abdominal (Barriga et al., 2002). Lake Gutiérrez has a surface area of 16.4 km2,
organs of fishes. The original description of M. galaxii did not report and a maximum depth of 111.2 m. After capture, the fish were trans-
the distribution in tissues, the type of sporogenesis, the number and the ported to the laboratory and kept alive at 6 C until killed and necropsied
position of polar filaments, or the histological and ecological features between 24 and 48 hr after capture. Samples of 12–73 fish from 17
of infection. The aim of this study was to characterize the infection of Andean Patagonian lakes were collected in the summer–autumn (Table
M. galaxii from muscles and other organs of G. maculatus from north- I). Specimens from Lake Gutiérrez were collected monthly from Feb-
western Andean Patagonian lakes. ruary 1995 to February 1997. Sex and total length of fish were recorded.
Fish were captured with baited traps in 17 oligotrophic lakes located Musculature and abdominal organs were removed. Plasmodia were dis-
in northwestern Argentinean Patagonia between 40⬚10⬘S and 41⬚30⬘S sected to obtain fresh spores or fixed in 10% buffered formalin. Mus-
(Table I). All of these lakes have only landlocked populations of G. culature was fixed in 10% buffered formalin, dehydrated in graded eth-
anol series, cleared in xylene, and embedded in paraffin. Histological
sections (7 ␮m thick) were stained with hematoxilin and eosin. Mor-
TABLE I. Coordinates of lakes, sample size, and prevalence of infection phometric measurements were based on 141 fresh and 80 fixed spores
of Myxobolus galaxii from Galaxias maculatus. obtained randomly from plasmodia of different fish. Measurements are

Prevalence
Lake Coordinates Sample size (%)

Lácar 40⬚10⬘S–71⬚30⬘W 31 16
Villarino 40⬚28⬘S–71⬚35⬘W 20 —
Filo Hua Hum 40⬚32⬘S–71⬚20⬘W 20 —
Espejo 40⬚41⬘S–71⬚42⬘W 24 —
Traful 40⬚41⬘S–71⬚35⬘W 24 —
Correntoso 40⬚44⬘S–71⬚39⬘W 35 —
Piré 40⬚44⬘S–71⬚39⬘W 35 14
Nahuel Huapı́ 40⬚48⬘S–71⬚39⬘W 24 8
Moreno 41⬚04⬘S–71⬚33⬘W 64 2
Escondido 41⬚04⬘S–71⬚35⬘W 41 —
Gutiérrez 41⬚11⬘S–71⬚25⬘W 52 17
Mallı́n Ingeniero 41⬚15⬘S–71⬚40⬘W 24 4
Mascardi 41⬚17⬘S–71⬚34⬘W 73 15
Fonck 41⬚19⬘S–71⬚45⬘W 12 —
Hess 41⬚22⬘S–71⬚43⬘W 17 —
Guillelmo 41⬚23⬘S–71⬚27⬘W 37 —
Steffen 41⬚30⬘S–71⬚40⬘W 27 — FIGURE 1. Seasonal fluctuation of water temperature and prevalence
of Myxobolus galaxii in Galaxias maculatus from Lake Gutiérrez.

418
RESEARCH NOTE 419

FIGURE 2. Prevalence of Myxobolus galaxii in relation to length of


Galaxias maculatus from Lake Gutiérrez.

given in micrometers, with mean and standard deviation followed by


range in parenthesis.
The data for monthly samples from Lake Gutiérrez were grouped
into seasons according to water temperature. Sample size and mean
length of fish are summarized in Table II. Prevalence of infection was
calculated according to Bush et al. (1997). The correlation between
prevalence and water temperature and length of fish was analyzed with
a Spearman rank correlation test (Conover, 1980). A test of indepen-
dence (Conover, 1980) was carried out to establish the relationship be-
tween prevalence and the host’s sex. A 1-way analysis of variance test

FIGURE 4. Histological section of Myxobolus galaxii plasmodium in


musculature of Galaxias maculatus. Scale bar ⫽ 100 ␮m (A, B).

was employed to evaluate differences in the size of the fish among


seasons and a multiple comparison Sheffé test was used to detect the
differences in the length of fish between seasons (Sokal and Rohlf,
1981). All P ⬍ 0.05 were considered significant.
In total, 1,044 G. maculatus from Lake Gutiérrez were analyzed (Ta-
ble II). Significant differences in fish length were detected between sea-
sons (F ⫽ 81.328; P ⫽ 0.0001); a Scheffé test showed that the speci-
mens in the winter samples were significantly smaller than the fish of
the other seasons. Maximum values of prevalence were detected in the
summers of 1995 and 1996 (17 and 13%, respectively) and minimum
values in spring 1995 and 1996 (3 and 5%, respectively) (Fig. 1). No
significant correlation was found between the water temperature and
prevalence (rS ⫽ 0.515; P ⫽ 0.156). The prevalence of M. galaxii in-
creased with total length of G. maculatus (Fig. 2), and there was a
significant positive correlation between these 2 variables (rS ⫽ 0.786;
P ⫽ 0.021). The sex of 587 fish specimens was determined; 372 were
female and 215 were male. Prevalence was not significantly different
(␹2 ⫽ 0.56; P ⬎ 0.05) between males (16%) and females (14%).
The plasmodia located in musculature (14.4%) were visible through
the integument as elongated spots and were distributed throughout stri-
ated muscle of the flank and caudal peduncle (Fig. 3A). In abdominal
organs, plasmodia were located in the gut (58.9%), spleen (11.1%),
kidney (8.9%), gonads (4.4%), and liver (2.2%). They were white and
usually subspherical in shape (Fig 3B). In spleen, liver, and kidney, the
plasmodia were found in the parenchyma. In the gonads, they were
embedded in the tissues, and in the digestive tract, they were found in
the tissues or protruding from the surfaces into the abdominal cavity
FIGURE 3. Plasmodia of Myxobolus galaxii in Galaxias maculatus. surrounded by mesenteries (Fig. 3C). The plasmodia, 585.1 ⫾ 120.2
(A) Plasmodia in musculature of caudal peduncle, visible through the (426–850) ␮m long and 151.9 ⫾ 43.8 (85–227) ␮m wide (n ⫽ 13),
integument. (B) Plasmodia dissected from musculature. (C) Plasmodi- have a thin wall (Fig. 4A). They are histozoic, intercellular, and poly-
um on gut surface surrounded by mesentery. Scale bar ⫽ 1,000 ␮m. sporous. Sporogenesis is synchronous (Fig. 4B). No gross or tissue le-
420 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 2, APRIL 2007

sions were observed by light microscopy. The only host reaction de-
tected was the formation of a connective tissue–like capsule around the
plasmodia (Fig. 4B).
Mature spores were smooth, pyriform to ovate in frontal view, and
biconvex in sutural view. They have a straight sutural line, with 4–9
small edge notches (Fig. 5A). A mucous envelope and triangular inter-
capsular processes were absent. An iodophilous vacuole was not ob-
served. Measurements of fresh and fixed spores are given in Table III.
The polar filaments exhibited 9–12 coils perpendicular to the longitu-
dinal axis of the polar capsules. The polar capsule dimensions and the
relation of the polar capsule to spore length are shown in Table III.
Variation in morphology of spores can be found even in the same plas-
modium. A few spores with an elongated caudal zone of valves in
plasmodia from musculature were observed (Fig. 5A–B).
Seasonal fluctuation in the prevalence of myxosporeans appears to
be common in those species having cysts on exposed host surfaces
(Cone, 1994), like M. magellanicus, which are released from the fish
when spores are mature (Flores and Viozzi, 2001). Histozoic species
found deep in host tissues, like M. galaxii, have a dispersal strategy
requiring host death (Marcogliese and Cone, 2001). These diverse strat-
egies lead to differences in the annual infection cycle of M. magellan-
icus and M. galaxii in the same G. maculatus population. The infection
pattern of M. galaxii in Lake Gutiérrez showed that the young G. ma-
culatus had the lowest values of prevalence and increased with fish
length. Because plasmodia are accumulated through the life span of fish
and spores are not released until death, the probability of becoming
infected seems to increase with the size of the fish because of the length
of time they are exposed to infection. During the study period, there
was a repeating pattern of a summer increase of prevalence and a de-
cline from summer to spring, which could be explained by the signifi-
cantly smaller size of the specimens captured in winter (Table II). This
infection pattern could be related to the life history of G. maculatus in
Lake Gutiérrez (i.e., the spawning period ranges from spring to summer
so that larvae are found in autumn and juveniles are mostly found in
winter) (Barriga et al., 2002). In contrast, M. magellanicus show the
highest values of prevalence in the smallest fish, with a peak prevalence
in winter (Flores and Viozzi, 2001).
In Patagonia, Myxidium biliare Viozzi et Flores, 2003 (a coelozoic
species with prevalences between 4.2 and 70%), and M. magellanicus
(a surface species with prevalences between 3.2 and 50%) are widely
distributed in lakes situated between 39⬚25⬘S and 41⬚30⬘S (Flores and
Viozzi, 2001; Viozzi and Flores, 2003). In contrast, the histozoic M.
galaxii was found only in 7 lakes with prevalences ranging between 2
and 17%. This prevalence and distribution pattern is similar to that
suggested by Cone et al. (2004), in which coelozoic species shedding
spores from the live host would have higher local prevalence and a
wider geographical range than histozoic species in which transmission
occurs only after host death. All G. maculatus populations parasitized
by M. galaxii also harbored M. magellanicus (Flores and Viozzi, 2001).
Although other native and introduced fishes have been examined for
myxozoan infections in Patagonia (data not shown), M. galaxii is lim-
FIGURE 5. Photomicrographs of formalin-fixed spores of Myxobolus ited only to G. maculatus. Szidat (1953) reported the presence of white
galaxii from muscles of Galaxias maculatus showing morphological plasmodia mainly located in musculature, kidney, and ‘‘other organs’’
variability. Scale bar ⫽ 15 ␮m (A, B). in G. maculatus. In this study, a multiorgan infection, mainly in the
abdominal cavity (85.6%), was observed. The organ most frequently
affected was the gut (58.9%) and the least frequently affected was the

TABLE III. Measures of Myxobolus galaxii spores from musculature and internal organs of Galaxias maculatus.

Spore Polar capsule


Spore Spore length/polar
source Condition n Length Width Thickness Length Width capsule length ratio

Musculature Fixed 60 14.1 ⫾ 1.0 (12–17) 9.7 ⫾ 0.7 (8–11) 8.0 ⫾ 0.8 (7–9) 6.9 ⫾ 0.7 (5–8) 3.4 ⫾ 0.5 (3–4) 2.1 ⫾ 0.2 (1.6–2.5)
Fresh 30 13.8 ⫾ 0.7 (13–15) 9.5 ⫾ 0.7 (8–11) — 6.3 ⫾ 0.6 (5–7) 3.0 ⫾ 0.2 (2.5–3) 2.2 ⫾ 0.3 (1.9–2.8)
Gonads Fixed 20 13.8 ⫾ 0.8 (12–15) 9.9 ⫾ 0.5 (9–11) 9 6.8 ⫾ 0.7 (6–8) 3 2.0 ⫾ 0.2 (1.6–2.5)
Fresh 11 14.9 ⫾ 0.8 (13–16) 9.5 ⫾ 0.5 (9–10) 8 7 3 2.1 ⫾ 0.1 (1.8–2.3)
Stomach Fresh 80 14.7 ⫾ 0.8 (13–17) 8.6 ⫾ 1.0 (6–10) 7.9 ⫾ 0.5 (7–9) 8.1 ⫾ 0.7 (7–9) 3.1 ⫾ 0.3 (3–4) 1.8 ⫾ 0.2 (1.4–2.3)
Intestine Fresh 20 13.6 ⫾ 0.7 (13–16) 9.4 ⫾ 0.7 (8–10) 8 7.6 ⫾ 0.5 (7–8) 3.2 ⫾ 0.3 (3–4) 1.8 ⫾ 0.1 (1.6–2.0)
Szidat (1953) Fixed — (13.7–15) (8.8–10) — — — —
RESEARCH NOTE 421

liver (2.2%). The spore length and width ranges of M. galaxii given by CONOVER, W. J. 1980. Practical nonparametric statistics, 2nd ed. John
Szidat (1953) are within the range of our fixed and fresh spores, but Wiley & Sons, New York, New York, 493 p.
variation in shape was not mentioned. In our material, the spores varied FLORES, V., AND G. VIOZZI. 2001. Redescription, seasonality and distri-
in length and width between those from the musculature and those from bution of Myxobolus magellanicus (Myxosporea) in Galaxias ma-
other organs. Such variations in spore sizes in multiorgan infections culatus (Osmeriformes: Galaxiidae) from Patagonian Andean lakes
were also observed in Myxidium zealandicum Hine 1975 from the fresh- (Argentina). Acta Parasitologica 43: 159–163.
water eel Anguilla australis (Hine, 1978). Mitchell (1989) demonstrated HINE, P. M. 1976. Myxobolus iucundus n. sp. (Sporozoa, Myxosporidea)
great intraspecific morphometric variation among spores of Myxobolus parasitic in Galaxias maculatus (Jenyns, 1842) in New Zealand.
muelleri Bütschli, 1881, within individual plasmodia and among spores Journal of Royal Society of New Zealand 2: 157–161.
from different tissues of an individual squawfish Ptychocheilus orego-
———. 1978. Variations in the spores of Myxidium zealandicum Hine,
nensis.
1975 (Protozoa: Myxosporidea). New Zealand Journal of Marine
Financial support for this study was provided by UNC-B-115; and
CONICET PIP 02752); V.F. had a fellowship funded by CONICET and Freshwater Research 12: 189–195.
(Consejo Nacional de Investigaciones Cientı́ficas y Técnicas, Argenti- KALAVATI, C., P. BRICKLE, AND K. MACKENZIE. 2000. Two new species
na). We thank Richard Sage for English revision of the manuscript. of myxozoan parasites (Myxosporea, Multivalvulida, Bivalvulida)
from fishes of the Falkland Islands. Acta Parasitologica 45: 285–
288.
LITERATURE CITED
MARCOGLIESE, D. J., AND D. K. CONE. 2001. Myxozoan communities
BARRIGA, J. P., M. A. BATTINI, P. J. MACCHI, D. MILANO, AND V. E. parasitizing Notropis hudsonius (Cyprinidae) at selected localities
CUSSAC. 2002. Spatial and temporal distribution of landlocked Gal- on the St. Lawrence River, Quebec: Possible effects of urban efflu-
axias maculatus and Galaxias platei (Pisces, Galaxiidae) in a lake ents. Journal of Parasitology 87: 951–956.
in the South American Andes. New Zealand Journal of Marine and MITCHELL, L. G. 1989. Myxobolid parasites (Myxozoa: Myxobolidae)
Freshwater Research 36: 349–363. infecting fishes of western Montana with notes on histopathology,
BERRA, T. M., I. E. CROWLEY, W. IVANTSOFF, AND P. A. FUERST. 1996. seasonality, and intraspecific variation. Canadian Journal of Zool-
Galaxias maculatus: An explanation of its biogeography. Marine ogy 67: 1915–1992.
and Freshwater Research 47: 845–849.
SOKAL, R., AND F. ROHLF. 1981. Biometry, 2nd ed. W. H. Freeman and
BUSH, A. O., K. LAFFERTY, J. LOTZ, AND A. SHOSTAK. 1997. Parasitology
Co., San Fransisco, California, 859 p.
meets ecology on its own terms: Margolis et al. revisited. Journal
of Parasitology 83: 575–583. SZIDAT, L. 1953. Einige neue Arten der Familie Myxobolidae Thélohan
CONE, D. K. 1994. Annual cycle of Henneguya doori (Myxosporea) (Protozoa, Klase Sporozoa) aus Süßwasserfischen Argentiniens.
parasitizing yellow perch (Perca flavescens). Journal of Parasitol- Gewässer und Abwässer 5: 7–16.
ogy 80: 900–904. VIOZZI, G. P., AND V. R. FLORES. 2003. Myxidium biliare sp. n. (Myx-
———, D. J. MARCOGLIESE, AND R. RUSSEL. 2004. The myxozoan fauna ozoa) from gall bladder of Galaxias maculatus (Osmeriformes:
of spottail shiner in the Great Lakes basin: Membership, richness, Galaxiidae) in Patagonia (Argentina). Folia Parasitologica 50: 190–
and geographical distribution. Journal of Parasitology 90: 921–932. 194.

J. Parasitol., 93(2), 2007, pp. 421–422


䉷 American Society of Parasitologists 2007

Paleoparasitological Analysis of a Raptor Pellet From Southern Patagonia


M. H. Fugassa, N. H. Sardella, and G. M. Denegri, Laboratorio de Zoonosis Parasitarias, Deptamento de Biologı́a, Universidad Nacional de
Mar del Plata—CONICET, Argentina. e-mail: mfugassa@mdp.edu.ar

ABSTRACT: Organic remains attributable to one regurgitated pellet were Cruz Province, Argentina, belonging to a deposit dated 6,540 ⫾ 110 yr
examined. The pellet, belonging to a bird of prey and collected from a B.P. (before present) (Aschero, 1996). CCP5 is a hill in the Nothofagus
cave of Southern Patagonia, was dated at 6,540 ⫾ 110 yr. With standard sp. forest Patagonian steppe ecotone, associated with human occupation
paleoparasitological procedures, eggs of Capillaria sp. and a mite, De- of hunter-gatherer groups (Aschero, 1982; Aschero et al., 1992). The
modex sp., were found. The parasites found in the pellet belong to a sample examined consisted of a light concretion, externally covered by
rodent ingested by the bird. The present report constitutes the first pa- hair, suggestive of a pellet regurgitated by a bird of prey (Marti, 1987).
leoparasitological study of a regurgitated pellet. The pellet was described, measured, and weighed according to the
method of Jouy-Avantin (2003). Two samples of approximately 0.5 g
Paleoparasitology includes the study of parasites isolated at archae- each, one from the surface and the other from the interior, of the con-
ological and paleontological sites. Coprolites are the main sources of cretion were rehydrated with a 0.5% trisodium phosphate aqueous so-
parasite findings, together with sediments of latrines, middens, and lution (Callen and Cameron, 1960) and concentrated by spontaneous
mummified tissues (Bouchet et al., 1999, 2003). The magnitude of the sedimentation according to Lutz (1919). The macroscopic remains were
contributions that paleoparasitology offers to archaeology depends on separated and dried to room temperature for diet analysis.
the number of samples examined, the availability of different methods, Weight and volume of the sample were 7.78 g and approximately 38
i.e., the application of immunological techniques (Gonçalves et al., cm3, respectively (Fig. 1). Externally, it consisted of rodent hairs and
2003), DNA amplification of ancient material (Araújo et al., 1998), and quills. The partial dissection showed numerous bones of a small rodent.
the source of evidence. The sediment obtained was limited. Microscopic examination of the
The improvement of methods applied to free sediments of burials, sample revealed eggs of Capillaria sp. with ornamented walls possess-
shell middens, and deposits of refuse have extended the scope of pa- ing radial perforations (Fig. 2a), 37.5–42.5 ␮m (36.25 ⫾ 6.29; n ⫽ 4)
leoparasitology in Patagonia (Fugassa and Guichón, 2005; Fugassa et ⫻ 63.75–68.75 ␮m (65.93 ⫾ 2.13; n ⫽ 4) in diameter. A mite, identified
al., 2006). The aim of the present study was to examine new archaeo- as Demodex sp. (112.5 ⫻ 32.5 ␮m in diameter), was also identified
logical material for paleoparasitological purposes. (Fig. 2b).
The sample was collected from the archaeological site, Cerro Casa Microscopic examination of the concretion revealed that the hair frag-
de Piedra 5 (CCP5), located in the Perito Moreno National Park, Santa ments of the rodent were more predominant (Chehebar and Martı́n,
422 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 2, APRIL 2007

hepatica, mostly parasites of rodents (Thienpont et al., 1979). The pres-


ence of Demodex sp. is the first documentation from an ancient sample.
The present report is the first paleoparasitological study of a regur-
gitated pellet. The pellet provides evidence of nondigestible scales,
feathers, hair, and bones, most likely of rodent origin (Marti, 1987).
Although pellets do not reflect the parasitic fauna of an individual host,
they may provide a parasitological record of prey.
We thank Marı́a Teresa Civalero (INAPL-CONICET) and Carlos As-
chero (UNT-CONICET) for providing the samples. Ricardo A. Guichón,
Susana L. Burry, and Pablo A. Martinez contributed to the laboratory
work. Editorial comments were valuable in an early version of the man-
uscript. This work is supported by PICT 03-13889, PICTO 04-849, and
CAPES/SECyT.

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