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First record of a Heterosigma(Raphidophyceae) bloom withassociated mortality of cage‐rearedsalmon in Big Glory Bay, New ZealandF. Hoe Chang a , Colin Anderson b & Nelson C. Boustead ca New Zealand Oceanographic Institute, DSIR Marine andFreshwater, Department of Scientific and Industrial Research ,Private Bag, Kilbirnie, Wellington, New Zealandb Central Animal Health Laboratory, Wallaceville AnimalResearch Centre , Ministry of Agriculture and Fisheries(Quality) , P. O. Box 40063, Upper Hutt, New Zealandc Freshwater Fisheries Centre , Ministry of Agriculture andFisheries , P. O. Box 8324, Riccarton, Christchurch, New ZealandPublished online: 30 Mar 2010.

To cite this article: F. Hoe Chang , Colin Anderson & Nelson C. Boustead (1990) First record ofa Heterosigma (Raphidophyceae) bloom with associated mortality of cage‐reared salmon in BigGlory Bay, New Zealand, New Zealand Journal of Marine and Freshwater Research, 24:4, 461-469,DOI: 10.1080/00288330.1990.9516437

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New Zealand Journal of Marine and Freshwater Research, 1990, Vol. 24: 461-4690028-8330/2404-0461 $2.50/0 © Crown copyright 1990

461

First record of a Heterosigma (Raphidophyceae) bloom with associatedmortality of cage-reared salmon in Big Glory Bay, New Zealand

F. HOE CHANG

New Zealand Oceanographic InstituteDSIR Marine and FreshwaterDepartment of Scientific and Industrial ResearchPrivate Bag, Kilbirnie, Wellington, New Zealand

COLIN ANDERSON

Central Animal Health LaboratoryWallaceville Animal Research CentreMinistry of Agriculture and Fisheries (Quality)P. O. Box 40063, Upper Hutt, New Zealand

NELSON C. BOUSTEAD

Freshwater Fisheries CentreMinistry of Agriculture and FisheriesP. O. Box 8324, RiccartonChristchurch, New Zealand

Abstract In early January 1989, a dense phyto-plankton bloom occurring in Big Glory Bay, StewartIsland, New Zealand, was associated with chinooksalmon kills. The total loss was estimated to be NZ$17million. Water samples collected between 5 and 6January showed Heterosigma cf. akashiwo as thedominant species. This bloom is the first record ofHeterosigma in New Zealand, and is the first NewZealand record linking this species to salmon kills.During the period of salmon mortality, Heterosigmaattained densities of nearly 2 × 106 cells 1-1, and wasfound in greatest concentration on the north-westside of Big Glory Bay where lowest Secchi diskdepths were recorded. Histopathological investi-gations of salmon which were affected by the bloomrevealed gill and intestine pathology characterised bydegenerative changes of the branchial epithelium and

M89055Received 7 November 1989; accepted 19 October 1990

vasculature. The pathology observed was similar tothat reported for Gyrodiniwn aweolum in Atlanticsalmon. Impairment of respiratory and osmoregulatoryfunction of gills was implicated as the cause of deathin fish exposed to Heterosigma bloom.

Keywords phytoplankton bloom; Heterosigma cf.akashiwo; first record; salmon mortalities;histopathological examinations; Big Glory Bay;Stewart Island

INTRODUCTION

The first floating cages or "sea pens" for rearingsalmon were established in New Zealand in 1981inside Big Glory Bay, Stewart Island (Fig. 1).Subsequently this bay has become the main area forrearing chinook salmon in New Zealand waters,although an increasing number of salmon are alsobeing reared in the Marlborough Sounds and AkaroaHarbour.

Big Glory Bay, an embayment of Paterson Inlet,is c. 4.8 km long and 2.8 km wide with a surface areaof c. 12 km2. Most of the bay is shallower than 20 m,and the sea bed is of mud and muddy sand. In January1989 there were seven salmon farms inside the Bay,and their anticipated annual production was 15001.

Although very dense phytoplankton blooms havebeen recorded in New Zealand coastal waters (Table1), with fish kills being occasionally reported (Chang1983; Chang & Ryan 1985; Boustead et al. 1987),there have been no reports of salmon mortality insideBig Glory Bay that implicated phytoplankton.

In January 1989, however, a dense phytoplanktonbloom inside Big Glory Bay was linked to an estimatedloss of 6001 of farmed chinook salmon (Boustead etal. 1989). Salmon mortalities first occurred on 3January 1989, and continued until after 11 January.This study was conducted on 5 and 6 January and isaimed at firstly, identifying aetiology of the salmonkill and secondly, describing the histopathologicalchanges observed in salmon tissues sampled duringthe fish kill in Big Glory Bay.

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462 New Zealand Journal of Marine and Freshwater Research, 1990, Vol. 24

Fig. 1 Big Glory Bay, at StewartIsland. Al-3 and C are sites atwhich Secchi disk visibility wasmeasured. Also shown is horizontaldistribution otHeterosigma (X 106

cells I"1) on 5-6 January 1989.

MATERIALS AND METHODS

Water clarity was estimated at several farm siteswithin Big Glory Bay, Stewart Island (Fig. 1), usingSecchi disk four times during the day on 5/6 January1989. Water samples were collected at three farms(Al, Bl, B2) and one site at the main channel (C) atthe surface, and additional subsurface samples wereobtained from a fourth farm (B2), at 1,2.5, 5, and10 m depth (Fig. 1). Live samples, sent immediatelyby air to Wellington, were examined on thefollowing day at the Oceanographic Institute.Subsamples were fixed at Big Glory Bay by addingLugol's iodine solution (1 %).

Using a Nikon inverted microscope, all phyto-plankton were identified to species level. Positive

identification of Heterosigma cf. akashiwo was aidedby work of Hara & Chihara (1987). Cell numbers ofthe dominant species were counted after a 24 h settlingperiod (Utermohl 1958). Betweeen five and tenreplicates were counted per sample, and at least 200cells were counted per replicate.

A variety of organs, e.g., gill, intestine, heart,liver, kidney, spleen, pancreas, mesenteric fat, gonad,and skin, from each of 16 moribund and 2 healthy2- and 3-year-old salmon (showing no signs ofdistress) were removed and fixed in neutral bufferedformal-saline for histopathological study. Thesetissues were processed and mounted in paraffin wax.Thin sections (5 |am) stained with haematoxylin andeosin, periodic acid shiff and aniline blue, wereexamined under a Reichert Divar light microscope.

Table 1 Historical outbreaks and localities of phytoplankton blooms in New Zealand coastal waters.

Year

1976,1978198119821983198519861987198719871988

Locality

Karamea BightTasman BayWestlandBream BayMarlborough SoundsMarlborough SoundsAkaroa HarbourWellington HarbourBreaksea Sound, Gilbert IslandNorthland

Dominant taxa

Prorocenlrum micansPhaeocyslis pouchetiiP. micansCerataulina pelagicaCochlodinium sp.Gyrodinium aureolumG. aureolumMyrionecta rubraGonyaulax polygrammaAmphidinium sp.

Source

Cassie(1981)Chang (1983)Chang (1988)Chang & Ryan (1985)Chang (unpubl. data)Chang (unpubl. data)Chang (1987a), Boustead et al. (1987)Chang (unpubl. data)Chang & Grange (unpubl. data)Chang (unpubl. data)

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Chang et al.—Heterosigma bloom in New Zealand waters 463

RESULTS

Water clarityOn 5 January the transparency of the water variedfrom 1.5 m on the north-west side of the bay where afish kill was occurring, to 6 m on the south-east sideof the bay where fish were not distressed or dying(Table 2). On 6 January poor transparency wasrecorded across the entire bay.

Abundance and distribution of phytoplanktonMicroscopic examination of samples collected on5 January revealed a motile, golden brown micro-flagellate, reminescent ofHeterosigma akashiwo Hadaex. Hara et Chihara (Hara & Chihara 1987). Thesecells (18-20 \xm in length) are slightly flatteneddorsoventrally with two subequal heterodynamicflagella, which arise from a furrow approximatelyone-third to half way around the cell (Fig. 2).

A total of 26 species of phytoplankton wereidentified (Table 3), and in all samples, Heterosigmacf. akashiwo (0.5-1.9 X 106 cells I"1) was consistentlyshown to be dominant, with Nitzschia pseudoseriata(0.5-1.1 X 105 cells I"1), and Skeletonema costatwn(0.5-1.9 X 105 cells I"1) to be sub-dominant. Otherdinoflagellates species, such as Ceratiwnfurca (0.2-0.5 X 104 cells I"1), Dinophysis acuta (0.02-0.1 X104 cells I"1), and Polykrikos schwartzii (0.02-0.2 X104 cells I"1), were also found to be common in allsamples.

During the study, Heterosigma was not uniformlydistributed throughout the bay. Of the four sitessampled, the highest concentration of Heterosigmacf. akashiwo was found along the north-western shoreof the bay. The highest value at the surface was atSite B3, where >0.5 X 106 cells I"1 was recorded(Fig. 1). In a vertical profile situated at Site B2 on thenorth-west side of the bay, the highest cellconcentration of nearly 2 X106 cells I"1 were recorded5 m below the surface in samples collected in the lateafternoon (Fig. 3).

Pathological examinationHistopathological examination of tissues from affectedsalmon showed significant gill pathology and mildintestinal tissue changes, but no consistent pathologyin a range of other organs.

Gills of a 2-year-old healthy fish sampled in aprevious year (Fig. 4A) differed from the gills ofsalmon collected from the Big Glory Bay during thebloom. The latter showed mild oedema and epithelialcell hypertrophy (Fig. 4B) in fish which were grosslyhealthy and vigorous, to a severe acute exudative and

degenerative change (Fig. 4C) in fish which wereswimming sluggishly in a disoriented manner at thewater surface. These changes were superimposed ona mild chronic hyperplastic branchitis. Although smallamounts of proteinaceous cellular debris, mucus, andamorphous non-host material were present betweenthe primary lamellae (Fig. 4C), no algal cells wereobserved. The secondary lamellae formed a wavypattern with pathological changes being most evidentdistally (Fig. 4C and 4D). Sections of secondarylamellar epithelium were separated from their pillarcell base by transudate. Epithelial cells werehyperplastic and in some areas there was adhesionbetween the epithelial cells of adjacent lamellae

Table 2 Secchi disk visibility in Big Glory Bay.

Farm sites inBig Glory Bay

South-east sideAlA2A3

North-west sideBlB2B3B4

Sunny4pm5 Jan 89

6.04.53.9

1.51.5-2.0

_-

Cloudy10 am6 Jan 89

2.53.53.0

2.52.52.42.0

Clearing1.30 pm6 Jan 89

_

-

3.02.0_2.0

Clearing4pm6 Jan 89

1.7_2.0

2.0__-

Table 3 List of phytoplankton taxa identified in samplescollected from Big Glory Bay, Stewart Island, on 5 and 6January 1989.

Class Raphidophyceae Class DinophjceacHeterosigma cf. akashiwo Dinophysis acuta

Polykrikos schwartziiCeratiwnfurcaGonyaulax polygrammaScrippsiella sp.Proloperidinium sp.Prorocentrum balticumAmphidinium sp.

Class Prasinophyccae

Pyramimonas sp.

Class Prymnesiophyceae

Chrysochromulina sp.

Class Cryptophyceae

Cryptomonas spp.

Class Chrysophyceae

Gymnodinium spp.Gyrodinium sp.

Class Bacillariophyceae

Nitzschia pseudoseriataSkeletonema coslatumLeplocylindrus danicusChaetoceros sp.Distephanus speculum

Paraphysomonas imperforala Nitzschia longissimaNavicula sp.

Class Euglenophyceae

Euglena sp.

Eucampia zodiacusThalassiosira sp.Thalassiothrix

nitzschioides

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A

New Zealand Journal of Marine and Freshwater Research, 1990, Vol. 24

Heterosigma (x 103 cells V)

10 urni

5 -

6,XL

1 0 -

Fig. 3 Depth profile of Heterosigma at Site B2 in BigGlory Bay, 5-6 January 1989.

Fig. 2 A, Light micrograph of a live Heterosigma cellshowing only one of the two flagella (F). B, Lightmicrograph of a similar cell fixed with Lugol's iodinesolution. Note the large central nucleus (N) surrounded bychloroplasts (C).

Fig. 4 A, Section of gill from a healthy 2-year-old chinook salmon sampled in a previous year.(continued on p. 465).

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r ^

Fig. 4 (Continued) B, Section of gill from a 2-year-old salmon taken from a cage of salmon whichwere not showing signs of distress during the kills.Oedema is lifting the epithelium from the pillar cellbase (small arrows), and some epithelial cells arehypertrophic (larger arrow).C, Gill from a moribund salmon netted from a cageduring the kill. The secondary lamellae have a wavyprofile with the outer half of the lamellae showingthe greater pathological change. The large arrowindicates proteinaceous cellular and otheramorphous material between the primary lamellae.Transudate (medium-size arrows) has lifted thesecondary lamellar epithelium in a number of places.Pyknotic and karyorrhectic debris (small arrow) inthe vascular spaces is most evident at the secondarylamellae tip.D, Section of affected gill showing a wavy profilewith a dilated and congested vascular space at thetip. Free erythrocytes (e) and sloughed cells, someof which have the appearance of chloride cells(small arrows), are present in the interlamellar space.Epithelial cells show hyperplasia with prominentnuclei (larger arrows) and at the secondary lamellartips they are forming bridge with, in each case theinvolment of a mucus cell (M). Other epithelialcells show pyknosis and degeneration (small arrowat bottom left comer). An oedematous space (O) ispresent beneath the epithelium in some areas.

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466 New Zealand Journal of Marine and Freshwater Research, 1990, Vol. 24

Fig. 5 The intestine of a moribundchinook salmon sampled during thekill. The epithelial cells havepyknotic and karyorrhectic nuclei(medium-size arrows). There areincreased numbers of inflammatorycells in the lamina propria andepithelium (small arrows). Necroticepithelial cells have sloughed(between two large arrows) into thelumen over a large area of the villishown (X 400).

(Fig. 4D). In other areas epithelial cells exhibitedhydropic degeneration and, together with the othercomponent cells of the epithelium, had sloughed tojoin erythrocytes in the interlameliar space.Inflammatory cells were numerous in primary andsecondary lamellar tissues and pyknotic nuclear debriswas often present in the congested vascular space ofthe secondary lamellae.

The pyloric caecae and intestine exhibited mildinflammatory and degenerative changes consistingof focal necrosis and sloughing of epithelial cells(Fig. 5). Inflammatory cells had infiltrated the laminapropria and epithelium. Inflammation and vascularcongestion were more pronounced in the intestinethan the pyloric caecae. The lumenal content of theintestine also contained more necrolic degeneratingepithelial and inflammatory cells, together with smallnumbers of bacteria and moderate amounts of mucus.

DISCUSSION

Several factors may have caused the sudden highmortality of cage-reared ch inook salmon in Big GloryBay in early January 1989. These include temperaturestress, low dissolved oxygen, phytoplankton toxicityor poisoning from another source, and microbial orparasitic organisms.

On 3 January 1989, the sea surface temperature inBig Glory Bay was 16.2°C. This was warmer thanthe range 13.8-14.2°C recorded in summer in thenearby Glory Cove (Batham 1969). However, aschinook salmon are sucessfully farmed in watertemperatures which for short periods reach 20°C inthe Marlborough Sounds of New Zealand (Andersonunpubl. data), and the incipient lethal temperature foryoung chinook salmon acclimated to 10°C is 25°C(Anon. 1976), temperature stress on its own was notbelieved to be responsible for this kill.

Throughout the bay, the level of dissolved oxygenappeared to remain reasonably high. Oxygen levelsin the cages where fish were dying was normal andsatisfactory when taken by farm staff using a YSIoxy-gen meter. These levels were higher than 5 ppmwhich is the generally accepted minimum oxygenlevel for maintaining heathy salmon populations(Anon. 1976).

Infectious fish disease was eliminated as a causeof the kill because of the absence of microbial andparasitic organisms in the tissues sampled fromaffected fish during the kill, and because the historywas not typical of an infectious disease episode. Thepresence of toxins other than those associated withthe bloom was viewed as most unlikely, consideringthe absence of industry and farming, and the infrequentvisits to the Paterson Inlet by yachts and pleasure

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launches. The association of salmon mortalities withthe presence of grossly observeable tea-brown algalbloom which contained an algal species previouslyreported to be associated with fish kills, was strongevidence for the bloom being responsible for thesalmon kill.

Heterosigma is a raphidophycean, and is closelyrelated to Chatonella (Hara & Chihara 1987), a toxicgenus which is well known to cause fish kill in theInland Sea of Japan (Okaichi 1983; Toyashima et al.1989). The link between the fish kill and theHeterosigma bloom in Big Glory Bay is consistentwith observations made by Gaines & Taylor (1986),Fraga (1988), Murphy (1988), and Stockner (1989)(Table 4). The Heterosigma cell concentrationrecorded in the vicinity of salmon farms at Big GloryBay were well below the recorded maximum concen-tration at which fish kills have occurred (Table 4).Given the limited number of samples collectedbetween 5 and 6 January 1989, it is likely that patcheswhich contained greater concentrations of Hetero-sigma than those recorded might not have beensampled. This is demonstrated in a sample collectedon 11 January 1989, five days after the first kill, froma patch in close vicinity of a farm, where as many as70 X 106 cells I"1 of Heterosigma were recorded(Chang unpubl. data).

Histopathological examination of grossly healthyfish in this study showed mild hyperplasia of thesecondary lamellar epithelium which is notuncommon in New Zealand sea-reared Chinooksalmon (Anderson unpubl. data). However, the gilland intestine changes observed are an uncommonfinding in New Zealand farmed salmon.

It has been suggested that mucus produced bysome marine algae which have been associated withfish kills in Norway, Chrysochromulina polylepis(Anon. 1988), and in Canada, Heterosigma akashiwo(Anon. 1989), causes mortality by mechanical

Table 4 Fish mortalities which have been associatedwith Heterosigma akashiwo blooms worlwide.

Year

1975,1981

1985,1986

1987198819891989

Country

Japan

Canada

SpainChileCanadaNew Zealand

Type offish

Yellowtail

Salmon

BassSalmonSalmonSalmon

Cell cone.(XIO6!"1)

_

-

18180

0.8-6300.5-2

Source

Gaines &Taylor (1986)

Gaines &Taylor (1986)

Fraga (1988)Murphy (1989)Stockner(1989)This study

obstruction to gill perfusion. In our case mucus wasnot present in greater amounts than would be expectedon gills undergoing the degree of pathological changesdescribed. Thus toxins produced in association withthe Heterosigma bloom appear to have caused thesegill and intestine lesions. Pure mechanical obstructionto gills would have caused asphyxiation without thecellular changes observed and ingested algal mucuswould not produce the intestinal lesions described bymechanical action.

A direct action of algal toxins on exposed fishtissues has long been suggested for Prymnesiumparvum (Shilo 1971, 1981; Collins 1978), P.calathiferum (Chang 1985), Gyrodinium aureolum(Jones et al. 1982; Roberts et al. 1983), Ptychodiscusbrevis (syn. Gymnodinium breve) (Lin et al. 1981),and more recently, for Synechococcus sp. (Mitsui etal. 1989) and Chrysochromulina polylepis (Anon.1989). In our case the pathological changes in gillsand intestine were consistent with acute exposure to anecrotising toxin. Severe damage to these organswould produce asphyxiation and osmotic shock. Thechanges observed in the gill lamellae will have reducedblood flow and increased the diffusion distance foroxygen, carbon dioxide, and ammonia. Electrolyteswill have been lost as a result of diffusion andhaemorrhage and chloride cell damage will haveinterferred with sodium transfer (Toyashima et al.1989). Marine teleosts obtain much of their freshwaterrequirements by intestinal absorption from ingestedsea water (Shehadeh & Gordon 1969). Algal toxinsingested with this water will come in direct contactwith the intestinal mucosa and be concentrated as thewater is absorbed.

The pathology reported here has many similaritieswith those recorded for G. aureolum in Atlanticsalmon (Salmo salar) in a farm kill, and laboratorytoxicity trial (Jones et al. 1982; Roberts et al. 1983).These authors reported acute toxic branchial necrosiswith oedemateous separation of the epithelium fromlamellar vessels and epithelial sloughing. Intestinalpathology included mild nuclear pyknosis andsloughing of epithelial cells. The close similarity ofthe pathology observed suggests that toxins producedby these two algal species may have a similar modeof action.

Another toxic alga, Dinophysis acuta, which hasbeen linked to diarrhetic shellfish poisoning (DSP)elsewhere (Chang 1987b), was also found in thisbloom (concentration up to 103 cells I"1). It has beensuggested that DSP occurs whenever concentrationsexceed 103 cells I"1, as reported in a closely relateddinoflagellate species, D. acuminata. Thus D. acuta

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is potentially a problem to shellfish farming which isat its infancy stage in the bay.

No published nutrient data for Big Glory Baywere available before the 1989 Heterosigma bloom.However, throughout Big Glory Bay in early 1988,both the levels of inorganic nitrogen nutrients (NO3~+ NH4

+) and dissolved reactive phosphate (DRP)were very high; the greatest concentrations of bothnutrients recorded were 48 and 14 mg irr3,respectively (Pridmore pers. cornm.). The very highnitrogenous level in the bay is comparable to thesurface NO3~ level (20--70 mg m~3) recorded inFoveaux Strait, on the north-eastern side of StewartIsland (Bradford et al. unpubl. data). The bulk ofnutrients in Big Glory Bay may have originated fromFoveaux Strait through water exchange. Excretoryproducts and nutrients leached from excess fish feedfrom the salmon farms might have contributed tosome of this pool, but the relative significance of thissource is not known.

Several laboratory studies outside New Zealandhave shown that rapid growth of Heterosigma isachieved with high levels of NO3~, NH4

+, and DRP,and also with relatively high level of micro-nutrients,such as manganese, and vitamin B12, in the growthmedia (Fukazama et al. 1980; Takahashi & Fukazama1982; Nishatijima & Hate 1984; Yamochi 1989). Inearly 1989, the region where the bay is located exper-ienced a higher-than-usual temperature and very calmweather. This was part of the unusual weather patternassociated with the La Nina phase of the SouthernOscillation (Laugesen 1989). Coupled with thishigher-than-usual temperature and generally verystable water column in mid summer, it is reasonableto assume that Heterosigma was able to respondfavourably to the high nutrients and outcompeteother species in the bay. Furthermore, the ability ofHeterosigma to migrate downward to reach thenutrient-rich bottom waters at night (Yamochi &Abe 1984) also provides an advantage over otherspecies.

ACKNOWLEDGMENTS

We thank Drs C. H. Hay, R. C. Murdoch, J. M. Bradford,and two anonymous referees for their constructive criticismsof this manuscript.

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