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Short Communication Prymnesium parvum, an Ichthyotoxic Alga in ...

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The Israeli Journal of Aquaculture – Bamidgeh 60(1), 2008, 5-8. 5<br />

<strong>Short</strong> <strong>Communication</strong><br />

<strong>Prymnesium</strong> <strong>parvum</strong>, <strong>an</strong> <strong>Ichthyotoxic</strong> <strong>Alga</strong> <strong>in</strong> <strong>an</strong><br />

Ornamental Fish Farm <strong>in</strong> Southern Israel<br />

Nurit Gordon <strong>an</strong>d Angelo Colorni*<br />

Israel Oce<strong>an</strong>ographic <strong>an</strong>d Limnological Research, National Center for Mariculture,<br />

P.O. Box 1212, Eilat 88000, Israel<br />

(11.9.07, Accepted 12.10.07)<br />

Key words: d<strong>in</strong>oflagellate bloom, <strong>Prymnesium</strong> <strong>parvum</strong>, molly, koi, ammonium sulfate<br />

Abstract<br />

The haptophyte alga <strong>Prymnesium</strong> <strong>parvum</strong> (Prymnesiophyceae) caused “creep<strong>in</strong>g” mortality <strong>in</strong><br />

ornamental fish, molly (Poecilia sp.) <strong>an</strong>d koi (Jap<strong>an</strong>ese carp, Cypr<strong>in</strong>us carpio), farmed <strong>in</strong> the<br />

Arava Valley <strong>in</strong> southern Israel. The toxicosis occurred when the water system was ch<strong>an</strong>ged<br />

from flow-through to closed circulation. A moderately high temperature, three-fold <strong>in</strong>crease of<br />

sal<strong>in</strong>ity, <strong>an</strong>d probable rise <strong>in</strong> eutrophication created conditions suitable to P. <strong>parvum</strong> blooms. The<br />

system was treated with 10 ppm ammonium sulfate <strong>an</strong>d fish mortality ceased.<br />

<strong>Prymnesium</strong> <strong>parvum</strong> is a relatively small haptophyte<br />

phytoflagellate that produces tox<strong>in</strong>s of<br />

lethal effect on gill-breath<strong>in</strong>g <strong>an</strong>imals <strong>an</strong>d<br />

extensive fish mortality <strong>in</strong> brackishwater fishponds.<br />

It was first associated with ichthyotoxicity<br />

<strong>in</strong> the Netherl<strong>an</strong>ds (Liebert <strong>an</strong>d Deerns,<br />

1924) <strong>an</strong>d some years later <strong>in</strong> Denmark<br />

(Otterstrom <strong>an</strong>d Steem<strong>an</strong>n-Nielsen, 1939). In<br />

Israel, the flagellate was first described <strong>in</strong> carp<br />

ponds <strong>in</strong> the Beit She’<strong>an</strong> (Beis<strong>an</strong>) Valley <strong>in</strong> the<br />

northern part of the country <strong>in</strong> the fall of 1945<br />

(Reich <strong>an</strong>d Aschner, 1947). Fish mortality was<br />

always preceded by a typical ch<strong>an</strong>ge of water<br />

color from tr<strong>an</strong>sparent light green <strong>in</strong> healthy<br />

ponds to a dirty yellow-brown. The condition<br />

gradually spread south <strong>an</strong>d <strong>in</strong> the follow<strong>in</strong>g<br />

w<strong>in</strong>ter reached the ponds of Beit Ha’arava, a<br />

settlement north of the Dead Sea. Although<br />

situated some 100 km apart, the two locations<br />

shared the same water supply. Soon after this<br />

first case report, the toxicosis became enzootic,<br />

affect<strong>in</strong>g <strong>an</strong> estimated 3,000 acres, 60% of<br />

the total Israeli pond area (Sarig, 1971).<br />

The toxicity of P. <strong>parvum</strong> was extensively<br />

studied <strong>in</strong> Israel (Yariv <strong>an</strong>d Hestr<strong>in</strong>, 1961;<br />

Bergm<strong>an</strong>n et al., 1963; Parnas, 1963; Reich<br />

et al., 1965; Dafni <strong>an</strong>d Shilo, 1966; Shilo,<br />

1967). The alga produces prymnes<strong>in</strong>, a com-<br />

* Correspond<strong>in</strong>g author. Tel.: +972-8-6361427, fax: +972-8-6375761, e-mail:<br />

<strong>an</strong>gelo@oce<strong>an</strong>.org.il, colorni@attglobal.net


6<br />

Gordon <strong>an</strong>d Colorni<br />

plex of highly toxic compounds whose synthesis<br />

is greatest dur<strong>in</strong>g the late stages of logarithmic<br />

growth <strong>an</strong>d stationary phases (Shilo,<br />

1967). The primary site of action of prymnes<strong>in</strong><br />

appears to be the gill membr<strong>an</strong>e, whose permeability<br />

becomes severely compromised<br />

(Yariv <strong>an</strong>d Hestr<strong>in</strong>, 1961; Ulitzur <strong>an</strong>d Shilo,<br />

1966). Fish may die with<strong>in</strong> hours without present<strong>in</strong>g<br />

<strong>an</strong>y particular <strong>an</strong>atomo-pathological<br />

lesions. <strong>Prymnesium</strong> <strong>parvum</strong> tox<strong>in</strong>s c<strong>an</strong> kill<br />

other aquatic org<strong>an</strong>isms as well, <strong>in</strong>clud<strong>in</strong>g<br />

protozo<strong>an</strong>s, cnidari<strong>an</strong>s, turbellari<strong>an</strong>s, rotifers,<br />

oligochaetes, polychaetes, irud<strong>in</strong>e<strong>an</strong>s, cladocer<strong>an</strong>s,<br />

amphipods, isopods, gastropods, <strong>an</strong>d<br />

amphibi<strong>an</strong>s <strong>in</strong> the gill-breath<strong>in</strong>g stage<br />

(Valk<strong>an</strong>ov, 1964; Paster, 1973).<br />

Although euryhal<strong>in</strong>e <strong>an</strong>d able to survive <strong>in</strong><br />

fresh water (250 mg chloride per l water;<br />

Kimor, 1948), P. <strong>parvum</strong> requires a sal<strong>in</strong>ity of<br />

0.1-3% to grow (Shilo <strong>an</strong>d Shilo, 1962; Larsen<br />

<strong>an</strong>d Bry<strong>an</strong>t, 1998). The optimum sal<strong>in</strong>ity for<br />

growth as well as the environmental factors<br />

that <strong>in</strong>fluence tox<strong>in</strong> production are uncerta<strong>in</strong><br />

(Larsen <strong>an</strong>d Bry<strong>an</strong>t, 1998), however, stagnat<strong>in</strong>g<br />

brackish water, raised nutrient concentrations,<br />

<strong>an</strong>d a mild climate provide <strong>an</strong> ideal ecological<br />

niche for P. <strong>parvum</strong> <strong>an</strong>d favor blooms<br />

(Coll<strong>in</strong>s, 1978; Holdway et al., 1978; Baker et<br />

al., 2007).<br />

In the past, confirmation of P. <strong>parvum</strong> was<br />

made by challeng<strong>in</strong>g small fish that are particularly<br />

sensitive to the tox<strong>in</strong> (such as Gambusia<br />

aff<strong>in</strong>is) with <strong>an</strong> activator (3,3 diam<strong>in</strong>odipropylam<strong>in</strong>e/DADPA)<br />

that lowers the m<strong>in</strong>imal toxic<br />

concentration. Presence of at least 1 ITU<br />

(ichthyo-toxic unit) was confirmed by the death<br />

of all test fish with<strong>in</strong> two hours (Ulitzur <strong>an</strong>d<br />

Shilo, 1966). <strong>Prymnesium</strong> <strong>parvum</strong> blooms<br />

were controlled ma<strong>in</strong>ly by us<strong>in</strong>g 10 ppm<br />

ammonium sulfate (Reich <strong>an</strong>d Aschner, 1947),<br />

10-15 ppm liquid ammonia (Sarig et al., 1960),<br />

or 2-3 ppm copper sulfate (Sarig, 1971).<br />

The present report describes a case<br />

brought to our attention <strong>in</strong> J<strong>an</strong>uary 2007.<br />

Cont<strong>in</strong>uous, “creep<strong>in</strong>g” mortality <strong>in</strong> <strong>an</strong> ornamental<br />

fish farm <strong>in</strong> the desert area of the<br />

Arava Valley started <strong>in</strong> 2003 when the water<br />

system, fed by local aquifers, was ch<strong>an</strong>ged<br />

from flow-through to closed circulation. The<br />

fish were raised <strong>in</strong> a variety of ponds (concrete,<br />

plastic-l<strong>in</strong>ed, <strong>an</strong>d earthen). The farm<br />

water temperature was ma<strong>in</strong>ta<strong>in</strong>ed at<br />

25±1.5°C <strong>an</strong>d sal<strong>in</strong>ity at the water <strong>in</strong>let fluctuated<br />

with<strong>in</strong> a r<strong>an</strong>ge of 300-500 mg chloride<br />

per l water. After the ch<strong>an</strong>ge, effluent water<br />

flowed through a sedimentation pond <strong>an</strong>d<br />

recirculated back to the fishponds. Fresh<br />

water was added to compensate for evaporation.<br />

Chloride <strong>in</strong> the ponds rose to 700-1100<br />

mg/l (1.3-2‰) dur<strong>in</strong>g the algal toxication.<br />

Neither gross pathology nor parasitological<br />

or histopathological <strong>an</strong>alysis of a sample<br />

of about 20 molly <strong>an</strong>d koi revealed the presence<br />

of pathogens or <strong>an</strong>y particular abnormalities,<br />

as <strong>in</strong> similar cases (Reich <strong>an</strong>d<br />

Aschner, 1947; Sarig, 1971). Microscopic<br />

exam<strong>in</strong>ation of the water, however, revealed a<br />

relative abund<strong>an</strong>ce (over 1 x 105 cells/ml) of<br />

P. <strong>parvum</strong> (length 13.5±1.5 µm, width 9±1<br />

µm; Fig. 1). A bloom of the green microalga<br />

Kirchneriella lunaris was also observed, as<br />

was the presence of the diatoms Chaetoceros<br />

<strong>an</strong>d Skeletonema <strong>an</strong>d the microflagellates<br />

Cryptomonas <strong>an</strong>d Chlamydomonas.<br />

No mortality occurred <strong>in</strong> ten fish that were<br />

tr<strong>an</strong>sferred to <strong>an</strong> aquarium conta<strong>in</strong><strong>in</strong>g fresh<br />

uncontam<strong>in</strong>ated water <strong>an</strong>d kept under observation<br />

for over a month, <strong>in</strong>dicat<strong>in</strong>g that the fish<br />

were <strong>in</strong> <strong>an</strong> <strong>in</strong>itial <strong>an</strong>d still reversible stage of<br />

<strong>in</strong>toxication, a feature already noted by other<br />

authors (Ulitzur <strong>an</strong>d Shilo, 1966). The system<br />

was treated with 10 ppm ammonium sulfate<br />

accord<strong>in</strong>g to the recommendations of Reich<br />

<strong>an</strong>d Aschner (1947) <strong>an</strong>d the fish mortality<br />

stopped.<br />

The propagation of the P. <strong>parvum</strong> was<br />

quite clearly triggered by the up to three-fold<br />

<strong>in</strong>crease <strong>in</strong> sal<strong>in</strong>ity <strong>an</strong>d favored by the moderately<br />

warm water of the fishpond, probably<br />

together with the rise <strong>in</strong> eutrophication caused<br />

by recirculat<strong>in</strong>g the water. The renewed<br />

occurrence of P. <strong>parvum</strong> <strong>in</strong> this region is worrisome<br />

<strong>an</strong>d may require new m<strong>an</strong>agement<br />

strategies to control its spread.<br />

Acknowledgements<br />

This work was carried out <strong>in</strong> the Pathobiology<br />

Department, whose activities are generously<br />

supported by D<strong>an</strong> <strong>an</strong>d Florence Green, North<br />

Americ<strong>an</strong> Friends of IOLR.


<strong>Prymnesium</strong> <strong>parvum</strong> <strong>in</strong> <strong>an</strong> ornamental fish farm <strong>in</strong> Israel<br />

7<br />

Fig. 1. <strong>Prymnesium</strong> <strong>parvum</strong> Carter from the Arava Valley <strong>in</strong> southern Israel.<br />

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