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History (USNM 51078).

Another P. platurus was collected in the area of Bahia Magdalena on 17
January 1977 by John Kipping. The snake was dead when found on Isia Mag-
dalena, 3 miles south of Boca de Soledad ( lat 25°1 5'N ) , but appeared to be fresh
with no obvious signs of decay (j. Kipping, pers. Commun.). This specimen is
deposited at the California Academy of Saiences (CAS 143253).

DISCUSSION
Distribution

The pelagic adaptations of P. platurus (such as the ability to feed at the sea
surface) permit individuals to survive ocean current transport over great dis-
tances ( Pickwell 1 972 ) , but the thermal tolerances of the species appear to limit



174 CALIFORNIA FISH AND CAME

breeding populations to between the 18-20°C isotherms (Dunson and Ehlert
1971; Graham et al. 1971; Hecht et al. 1974).

Along the Pacific coast of North America, the northernmost locality at which
a breeding population of P. platurus has been found is Bahia Banderas, Jalisco,
Mexico (lat 20°38'N; Pickwell pers. observ.). Occasionally the species may be
abundant farther north. Zweifel (1960) reported 13 individuals collected on 7
February 1920, about 24 km offshore between San Bias, Nayarit, and Mazatlan,
Sinaloa, Mexico.

In the Gulf of California, individuals of P. platurus were reported before the
turn of the century from Isia Espiritu Santo (Baja Calif. Sur; lat 24°30'N) by
Mocquard (1899) and as far north as Guaymas (Sonora; lat 27°54'N) by Cope
(1887). Shaw (1961 ) reported the species from Bahia de los Angeles (Baja Calif.
Norte; 29°N), and individuals at least periodically range to near the head of the
Gulf at San Felipe (Baja Calif. Norte; 3rN; LACM 104332) where one of us
(Fitch) has seen live P. platurus on the beach on two separate occasions.

While these records do not seem indicative of a resident reproducing popula-
tion of Pelamis in the Gulf of California, they do suggest that it may be a regular
visitor there. Northward-moving surface currents prevail near the mouth of the
Gulf from June through November and in some years may be greatly accentuat-
ed during the August-September period of strong chubasco winds. In summer
and fall the surface temperatures (approximately 30°C) throughout the Gulf
approximate those of the eastern tropical Pacific and in winter remain above
18-20°C to a latitude of about 25°N (Hubbs and Roden 1964, Robinson 1973).

Most of the outer coast of Baja California, on the other hand, is generally
dominated by the cool southward-moving California Current system and by
areas of cold-water upwelling. As the California Current moves southward it
veers progressively westward and below about 25°N the outer coast of Baja
California receives warm northward-moving equatorial water for at least part of
the year. Thus, while tropical marine faunas dominate the Gulf of California, they
usually extend to only Bahia Magdalena on the outer coast ( Hubbs 1 960; Walker
1960; Thomson et al. 1979).

North of 25°N latitude, the northward-moving current generally submerges to
a depth greater than 200m. In certain years, however, it surfaces on the inshore
side of the California Current during late fall and winter, particularly if north
winds are weak. At times this warm counter-current, called the Davidson Cur-
rent, may extend at the surface from Cabo San Lucas to Point Conception or
beyond (Reid, Roden, and Wyllie 1958). It seems reasonable that individuals of
P. platurus wou\d be recruited occasionally into this northward-moving current
system.

The movement into southern California waters of tropical marine species
during the 1957-59 warm period was well documented by Radovich (1961).
Similar northward incursions occurred in 1972-73 and 1976-77, the years when
the sea snakes were found. A longnose puffer, Sphoeroides lobatus, was taken
off California for the first time in December 1 972 ( Fitch 1 973 ) . At least five other
southern species of fishes not normally found in California waters were taken
in 1972-73 and six others in 1977 (Fitch and Schultz 1978, Fitch unpublished
data). Unusually large numbers of the pelagic red crab, Pleuroncodes planipes,
were observed off southern California in early February 1973 (Mais 1973) and
great numbers washed ashore onto the beaches. Pelagic red crabs also were



SEA SNAKE OCCURRENCES 175

seen in southern California waters in large numbers in the 1957-59 warm period
(Radovich 1961) but quantities seen in 1973 appeared greater (Mais 1973).
Normally P/euroncodes occurs in waters south of central Baja California. These
occurrences further suggest an association between the northward incursion of
warm southern water and the yellow-bellied sea snake records reported here.

Data from La Jolla (Scripps Pier; lat 32°52'N ) indicate that ocean temperatures
off southern California were above average during the years and months in
which the two specimens of P. platurus were recently taken along the outer coast
of Baja California. The mean annual surface temperature at La Jolla for 1917-
1978 is 16.85°C ( ±0.07), with a range of annual means of 1 5.53-1 8.50°C. For
1 976, 1 977 and 1 978 the means were 1 7.76, 1 7.25 and 1 7.42°C, respectively, each
higher than any year since the 1957-59 warm period (Radovich 1961). The
recent Bahia Magdalena specimen was taken in January 1977, for which the
mean La Jolla temperature was 1 6.22°C, 2.1 8°C above the 62 year January mean.
The Bahia Blanca specimen was taken in November 1977, with a La Jolla mean
of 17.38°C, 1.1 2°C above average. Although these temperature data are from
hundreds of kilometres north of the two Baja California localities, they suggest
that stronger than usual Davidson Current conditions prevailed along the outer
coast at the time.

The San Clemente specimen (23 November 1972) also was taken in a slightly
warmer than average year. At La Jolla (70 km south of San Clemente) the
November 1972 average temperature was 0.1 2°C above the 62-year average
while the preceding 2 months were 0.1 9°C and 0.4rc above their respective
means.

It is possible that one or more of these sea snakes could have been transported
northward accidentally or intentionally by man (e.g., aboard fishing vessels).
However, the timing of the three occurrences and their congruence with avail-
able information on temperature and the incursion of tropical species of fishes
and invertebrates into southern California waters suggest natural oceanic disper-
sal.

Predation

Other sea snakes (family Hydrophiidae) are commonly fed upon by large
fishes, particuarly sharks, and by sea eagles, but predation on P. p/aturus appears
to be extremely rare ( Heatwole 1 975, Kropach 1 975 ) . Examination of the stom-
ach contents of 457 fishes representing 25 species of potential predators from
the Gulf of Panama, where Pelamis is seasonally abundant, yielded no remains
of the sea snake; and birds frequenting slicks with Pelamis were not observed
to attack or pick up the snakes (Kropach 1975). Two attacks on Pelamis by
sailfish or small marlins were described by Paulson (1967) but ingestion of the
snakes was not observed, Wetmore (1965) reported seeing a frigate bird, Frigata
magnificens, pick up a Pelamis, carry it for a short distance, and then drop it.

An adult male leopard seal, Hydrunga leptonyx, collected in poor condition
on a beach in New South Wales, Australia, was reported to have regurgitated
a partly digested Pelamis (Heatwole and Finnie 1980). While the seal was almost
certainly a naive or opportunistic predator on the sea snake, this represents the
first verified account of predation on Pelamis in the wild and the first known
instance of predation on any sea snake by a mammal.

In the laboratory, Rubinioff and Kropach (1970) demonstrated that Pelamis



176 CALIFORNIA FISH AND GAME

(alive, dead, skinned or in pieces) was strictly avoided by 10 species of eastern
Pacific predatory fishes (even when the fishes were starved). Fishes of nine
closely related Atlantic species attacked and occasionally ingested the snakes;
three fishes died from resultant snake bites. Van Bruggen (1961 ) reported that
an octopus in an aquarium attacked and ingested a 30-cm Pelamis.

The regurgitation of the specimen of P. platurus (LACM 127002) by a puffer
Sphoeroides cf. annulatus from Bahia Blanca represents the second reported
occurrence to date of predation on this snake in nature. It is possible that the
snake was scavenged, but the food habits of puffers and the freshness of the
Pelamis at the time it was brought in suggest that the snake probably was alive
when attacked and eaten. The exceptionally strong crushing plates in the mouths
of puffers allow them to feed on a variety of armored organisms that are unavail-
able to most other fishes (e.g., certain crustaceans, mollusks, sea urchins, brittle
stars, polychaete worms, etc.; Hiatt and Strasburg 1960; Hobson, 1974; Shipp
1974). With this crushing mechanism and feeding strategy, it seems reasonable
that large puffers might occasionally attack, crush, and swallow sea snakes.
Nevertheless, predation on P. platurus by Sphoeroides is probably a rare occur-
rence in spite of the widespread distribution of both species in the tropical
eastern Pacific. This is due to the largely epipelagic habits of Pelamis as opposed
to the primarily epibenthic habits of puffers.

ACKNOWLEDGMENTS

For information on museum records we thank J. Collins, M. Dodero, R.
Drewes, H. Greene, F. McCullough, R. McDiarmid, M. Nickerson, J. Simmons,
H. Voris and R. Zweifel.

We thank I. Goyette, J. Kipping, and A. Reich for information and details on
individual specimens and K. Mais, M. Stinson, and F. Wilkes for information on
northern occurrence of certain species and temperature data.

For helpful information and references or critical review of the manuscript we
thank W. Culotta, W. Friedl, J. Graham, H. Heatwole, L. Hubbs, C. Swift, H.
Voris, and J. Wright.

LITERATURE CITED

Cope, E. D. 1887. Catalogue of batrachians and reptiles of Central America and Mexico. Bull. U.S. Natl. Mus.,
32:1-98.

Dunson, W. A. and G. W. Ehlert. 1971. Effects of temperature, salinity and surface water flow on distribution
of the sea snake Pelamis. Limnol. Oceanog., 16{6):845-853.

Fitch, |. E. 1973. The longnose puffer, Sphoeroides lobatus (Steindachner) added to the marine fauna of Califor-
nia. Bull. So. Calif. Acad. Sci., 72:163.

Fitch, J. E. and S. A. Schultz. 1978. Some rare and unusual occurrences of fishes off California and Baja California.
Calif. Fish Came, 64 (2): 74-92.

Graham, ). B., I. Rubinoff and M. K. Hecht. 1971. Temperature physiology of the sea snake Pelamis platurus: An
index of its colonization potential in the Atlantic Ocean. Proc. Natl. Acad. Sci., 68(6): 1360-1363.

Heatwole, H. 1975. Predation on sea snakes, pages 223-249. In W. A. Dunson ed. The Biology of Sea Snakes.
University Park Press, Baltimore.

Heatwole, H., and E. P. Finnie. 1980. Seal predation on a sea snake. Herpetofauna, 11:24.
Hecht, M. K., C. Kropach, and B. M. Hecht. 1974. Distribution of the yellow-bellied sea snake, Pelamis platurus,
and its significance in relation to the fossil record. Herpetologica, 30(4): 387-396.

Hiatt, R. W., and D. W. Strasburg. 1960. Ecological relationships of the fish fauna on coral reefs of the Marshall
Islands. Ecol. Monogr,, 30:65-127.

Hobson, E. S. 1974. Feeding relationships of teleostean fishes on coral reefs in Kona, Hawaii. Fishery Bull.,
72(4):915-1031.

Hubbs, C. L. 1960. The marine vertebrates of the outer coast Syst. Zool., 9: (3-4) 134-147.



SEA SNAKE OCCURRENCES 177

Hubbs, C. L., and C. I. Roden. 1964. Oceanography and marine life along the Pacific coast of middle America,
pages 43-186. In R. C. West ed. Handbook of Middle American Indians, Vol. 1, Natural environment and early
cultures. Univ. of Texas Press, Austin.

Kropach, C. 1975. The yellow-bellied sea snake, Pelamis, in the eastern Pacific, pages 185-213. //» W. A. Dunson
ed. The Biology of sea snakes. University Park Press, Baltimore.

Mais, K. 1973. Cruise report 73-A-1 . Fisheries resources sea survey. Calif. Resources Agency, Dept. Fish & Game,
Marine Resources Region, Long Beach. 2 pp. Mimeographed report

Mocquard, M. F. 1899. Contribution a la faune herpetologique de la Basse-California. Nouv. Arch. Mus. Hist. Nat,
Paris. (Ser. 4) 1:297-344.

Paulson, D. R. 1%7. Searching for sea serpents. Sea Frontiers, 13:244-250.

Pickwell, G. V. 1972. The venomous sea snakes. Fauna, 4:17-32.

Pickwell, G. V., and W. A. Culotta. 1980. Pelamis, P. platurvs. Cat Amer. Amphib. Rept: 255.1-255.4.

Radovich, J. 1%1. Relationships of some marine organisms of the northeast Pacific to water temperatures
particularly during 1957 through 1959. SUte of Calif. Dept. Fish and Game, Fish Bull., 112:1-62.

Reid, J. L. Jr., G. I. Roden, and J. G. Wyllie. 1958. Studies of the California Current system. Calif. Coop. Oceanic

Fisher. Investig., Prog. Rep., 1 July 1956 to 1 Jan. 1958: 27-56.
Robinson, M.K.I 973. Atlas of monthly sea surface and subsurface temperatures in the Gulf of California, Mexico.

San Diego Soc. Nat Hist Mem., 5:1-97.
Rubinoff, I., and C. Kropach. 1970. Differential reactions of Atlantic and Pacific predators to sea snakes. Nature,

228 (5278): 1288-1290.
Schmidt K. P. 1922. The amphibians and reptiles of Lower California and the neighboring islands. Bull. Amer.

Mus. Nat Hist, 46(11):607-707.
Shaw, C. E. 1%1. Snakes of the sea. Zoonooz (San Diego), 34(7) :3-5.
Shipp, R. L. 1974. The pufferfishes (Tetradontidae) of the Atlantic Ocean. Publ. Gulf Coast Res. Lab. Mus.,

4:1-163.
Smith. H. M. 1943. Summary of the collections of snakes and crocodilians made in Mexico under the Walter

Rathbone Bacon traveling scholarship. Proc. U.S. Natl. Mus., 93(3169):393-504.
Strauch, A. 1873. Die Schlangen des Russischen Reichs in systematischer und zoogeographischer Beziehung.

Mem. Acad. Imp. Sci. St-Peterbourg, Ser. 7, 21 (4):1-287.

Thomson, D. A., L. T. Findley, and A. N. Kerstitch. 1979. Reef fishes of the Sea of Cortez. John Wiley, New York:

302 p.
Townsend, C. H. 1916. Voyage of the 'Albatross' to the Gulf of California in 191 1. Bull. Anner. Mus. Nat Hist,

35(24) :399-476.
Van Bruggen, A. C. 1%1. Pelamis platurus, an unusual item of food of Octopus spec. Basteria, 25:73-74.
Walker, B. W. 1960. The distribution and affinities of the marine fish fauna of the Gulf of California. Syst Zool.,

9(3-4):123-133.
Wetmore, A. 1%5. The birds of the Republic of Panama, Part 1: Tinamidae (Tinamous) to Rynchopidae

(Skimmers). Smithsonian Misc. Coll., 150:1-483.
Zweifel, R. G. 1960. Results of the Puritan-American Museum of Natural History expedition to western Mexico.

9. Herpetology of the Tres Marias Islands. Bull. Amer. Mus. Nat Hist, 119(2):77-128(-(- 4 plates).



178 CALIFORNIA FISH AND CAME

THELOHANIA COSITEJEASII PARASITISM OF THE CRAY-
FISH, PACIFASTACUS LENIUSCULUS, IN CALIFORNIA ^

DARLENE MCCRIFF

California Department of Fish and Canne

Inland Fisheries Branch

1701 Nimbus Road

Rancho Cordova, California 95670

and

JOHN MODIN

California Department of Fish and Game

Fish Disease Laboratory

2111 Nimbus Road

Rancho Cordova, California 95670

This is the first record of the occurrence of microsporidian parasite, Thelohania
contejeani, from western North America, and the first report of infection in Pacifas-
tacus leniusculus. Clinical symptoms observed in the crayfish are described, and the
parasite is described microscopically from slides of the pansporoblasts and spores.
The possible impacts of this new sighting of Thelohania contejeani ue discussed and
recommendations for further research are given.

INTRODUCTION

Thelohania contejeani Henneguy is a microsporidian parasite of decapod
crustaceans. First described in Europe in 1892, it is known to parasitize Astacus
astacus\u Finland (Sumari and Westman 1969), Lithuania (Mazylis 1978), and
the U.S.S.R. (Voronin 1971 ); Austropotamobius pallipes in Great Britain (Cos-
sins and Bowler 1974, Brown and Bowler 1977); France (Vey and Vago 1973),
Germany (Schaperclaus 1954), and Ireland (O'Keeffe and Reynolds, In press);
Astacus leptodactylus \u Lithuania (Mazylis 1978) and Poland (Krucinska and
Simon 1968); and Cambarus affinis \v\ Poland (Krucinska and Simon 1968). In
addition, Thelohania sp. parasitism has been reported in Paranephrops zealand-
/■ct/5 and P. planifronsUom New Zealand (Quilter 1976, Jones 1980) and Cherax
destructor irony Victoria and New South Wales, Australia (Carstairs 1978).

Records of microsporidiosis in North American crayfish are sparse. In the
United States, Sprague (1950) described a new species of Thelohania, T cam-
bari, in Cambarus bartoni, from streams along the Georgia/ North Carolina bor-
der; in Louisiana, Sogandares-Bernal (1962) found Cambarellus puer '\niecied
with Plistophora sp. and C. shufeldti \niected with Thelohania sp.; and Norton
H. Hobbs Jr. (Senior Zoologist, Dept. of Invert. Zoo., Natl. Mus. Nat. Hist.,
Washington D.C., pers. commun.) found individuals of Orconectes virginiensis
and Cambarus acuminatus from southeastern Virginia with opaque white ab-
dominal muscles that he assumed were parasitized by Thelohania sp. In Canada,
Orconectes virilis from Ontario are reported to be infected with Thelohania sp.
(France, In press).

This paper documents, for the first time, T. contejeani \r\ Pacifastacus lenius-
culus leniusculus from the Stanislaus River in California.

MATERIALS AND METHODS
Crayfish were collected in the Stanislaus River at Parrots Ferry (Figure 1 ) on



Accepted for publication August 1982.



PARASITISM OF CRAYFISH



179



24 July 1979 as part of a study on the statewide distribution of crayfish in
California. At the time the specimens were collected, this section of the Stanis-
laus River was about 15 m wide, clear, and fast flowing with many riffles and
pools. The bottom composition was about 50% sand and 50% rubble. The
surface temperature was 18°C.

/




^



(



LOCATION MAP



T V F><



fOPjA



'Porrotts Ferry



• STOCKTON

.To the Delta
CommerciOl fishing grounds



• SONORA
old Melones Res

.Tulloch Reservoir



STA



NlS^



aus



/?/</



£ff



<Xi



• MODESTO



>'?.



<>






10

Kilometers
SCALE



FIGURE 1. Map of the Stanislaus River showing collection locality for infected crayfish.



Four crayfish were collected by hand while snorkeling among the rocks in
about 1-2 m of water. They were sealed in a plastic bag and stored in an ice
chest with ice and water until taken back to the laboratory and frozen. On 31
July 1979 the specimens were taken to the Department of Fish and Game's Fish
Disease Laboratory for analysis. Wet mount preparations (coverslip scrapings of
thawed abdominal muscle) examined under lOx, 40x, and 90x objectives on a
Leitz Dialux phase contrast microscope revealed an apparent microsporidian
infection. The specimens were then preserved in 50% isopropanol, and on 2



180



CALIFORNIA FISH AND CAME



October 1980 similar preparations of the preserved abdominal muscle were
made to obtain biometric data on spore and pansporoblast shape and size. All
data were obtained at 900x using preserved material, a calibrated ocular mi-
crometer, and phase contrast equipment.

RESULTS

The four crayfish were identified as P. I. leniusculus, following the nomencla-
ture proposed by Hobbs (1972, 1974). When collected, three of the four crayfish
had semisoft carapaces, indicating a fairly recent molt. They also appeared
stressed and were weak and sluggish. Their abdominal muscles, visible through
the sternum, were an opaque, milky white (Figure 2).




FIGURE 2. Thelohania contejeani \niecled crayfish on the left showing the characteristic white,
opaque abdominal muscles. Noninfected crayfish on the right. Photograph by Junior
author.

Microscopic examination of slides of the abdominal muscle revealed a heavy
infection with spores and pansporoblasts of a microsporidian parasite. Each
pansporoblast contained eight spores. As the number of spores per sporoblast
is a generic characteristic (Cossins and Bowler 1974), the parasite was identified
as Thelohania sp.

The pansporoblasts are generally spherical with a mean diameter of 7.5 }x
(range = 6.5 to 8.0 \x) (Figure 3). The oval spores, possessing a vacoule at one
end, have a mean length of 3.4 jll (range = 3.0 to 3.8 \x) and a mean width of
2.2 jx (range = 2.0 to 2.4 /x) (Figure 3). The measurements given in the literature
for T. contejeani pansporoblasts range from 5 to 9 ja; the length of the spore
ranges from 2 to 4 jli, and the width ranges from 1 .5 to 2.3 jli ( Kudo 1 924, Cossins
1973, Cossins and Bowler 1974, Quilter 1976, Bulla and Cheng 1977). Because
of the close clinical and biometrical similarities between this microsporidian and
co/7^e/'e<3^/ infecting other crayfish, we identified this microsporidian as T. con-
tejeani.



PARASITISM OF CRAYFISH



181




FIGURE 3. Photograph (900x) of" phase contrast slide of preserved crayfish abdominal muscle
showing the pansporoblasts and spores of a microsporidian parasite identified as
Thelohania contejeani. Photograph by junior author.

DISCUSSION

Cossins (1973) states that such factors as waterflow, crayfish density, and the
extent of cannibalism may affect the spread of T. contejeani. With the comple-
tion of New Melones Dam, the lotic habitat of the Stanislaus River supporting
the Thelohania infected population has been transformed into a lentic habitat.
The level of the old Melones Reservoir at maximum storage (Figure 1 ) was 224
m above sea level and the capture site is 247 m above sea level. The maximum
storage expected behind the New Melones Dam during 1982 will raise the
reservoir level to 283 m, and the minimum expected storage will drop the
reservoir level to 257 m (U.S. Dept. of the Interior, Bureau of Reclamation,
unpubl. data). Not enough is known about the environmental parameters that
affect Thelohania to predict how this habitat change will effect the level of
infection in the crayfish population or the possible spread of Thelohania to other
crayfish populations.

This is the first record of the occurrence of T. contejeani hom western North
America and the first report of infection in a member of the genus Pacifastacus.
If past trends are repeated, T. contejeani ca^u be expected to spread downstream
to the Delta population of P. leniusculus where it may have an adverse impact
on the commercial fishery. The capture site is separated from the commercial
fishing grounds of the Delta by two dams and about 200 km of river. The disease
is apparently not now present in the Delta. Over 30,000 P. leniusculus from the
commercial catch in the Sacramento-San Joaquin Delta were measured and
sexed at processing plants between 1975 and 1980, with no sign of Thelohania
parasitism.

Locality records of Thelohania sp. indicate clustering. Quilter (1976) found

Paranephrops zealandicus on the South Island of New Zealand infected with T
contejeani in 1974 and concluded that the distribution of the parasite was



182 CALIFORNIA FISH AND CAME

restricted. However, by 1977 P. planifronsirorr\ the North Island of New Zealand
was found to be infected with Thelohania sp. (Jones 1980). T. contejeani was
not known in Finland until 1 965, but between 1 965 and 1 969 it was reported from
four different waterways (Sumari and Westman 1969). This clustering of new
sightings may simply be an artifact of increased crayfish research and exploita-
tion rather than new introductions of the parasite.

The levels of infection reported in the literature range from 0.3 to 30% (Scha-
perclaus 1954, Vey and Vago 1973, Cossins and Bowler 1974, Quilter 1976,
Carstairs 1978, Mazylis 1978, Jones 1980, France, In press, O'Keeffe and Rey-
nolds, In press). However, O'Keeffe and Reynolds (In press), using microscopic
examination, found that 40% of Austropotamobius pallipes infected with Thelo-
hania in Ireland eluded detection by macroscopic examination. Therefore, the
figures given may be underestimates.

All individuals infected with Thelohania apparently die. However, the time
required for the disease to run its course is unknown, but it may be lengthy. In
Lithuania, experimentally infected individuals took 5 to 6 months to exhibit
clinical symptoms, and they could feed, molt, and remain vigorous for up to a
year in captivity before dying (Mazylis 1978). Detailed and controlled experi-
ments are needed to establish the exact environmental and biological factors
that affect the parasite and the susceptibility of crayfish to it.

LITERATURE CITED


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