Observations on Pyrodinium bahamense Plate, a toxic dinoflagellate, in Papua New Guinea

Observations on Pyrodinium bahamense Plate, a toxic dinoflagellate, in Papua New Guinea

J. L. Maclean Department of Agriculture, Stock and Fisheries, Fisheries Research Station, Kanudi, Papua New Guinea

Abstract

Pyrodinium bahamense, a dinoflagellate causing paralytic shellfish poisoning, is widely distributed through Papua New Guinea waters. Some similarities and differences in bc- havior of the species in Papua New Guinea and other oceans are noted.

Pyrodinium bahamense, an armored, bioluminescent dinoflagellate, was until recently unknown in waters of Papua New Guinea. Wall and Dale ( 1969) gave its previous distribution as restricted to tropical and subtropical latitudes of the Carib- bean Sea, castcrn Pacific Ocean, Red Sea, Persian Gulf, and North Atlantic Ocean. It is well known for persistent bioluminescent displays and blooms in the Bahamas, Ja- maica, and Puerto Rico (Seliger et al. 1970). Its distribution in Puerto Rico is in shallow bays and to a lesser extent neritically inshore. “Red water” species such as Pyro- ctinium are characteristic of mangrove areas ( Margalef 1957, 1961). Off Florida it has been found in bottom samples offshore (40- 80-m depth ) as well as in surface inshore samples (Steidinger and Williams 1970). It has not been found in Australian waters (Wood 1954, 1963a,h). Markina ( 1972) did not record its presence in waters to the north of Australia, including the Gulf of Carpentaria, Arafura Sea, and Torres Strait.

Pyrodinium bahamense has now been found responsible for fatal paralytic shellfish poisonings in waters of Papua New Guinea (Worth et al, 1975). Most of the red tides observed oft! the coast of the mainland and outer islands arc attributable to this species ( Maclean 1973). Extensive red tides in Port Moresby Harbor and along the nearby coast during 1973 pro- vidcd an opportunity for observing the blooms. Supplementary data were gained

1 Present address : Fisheries Division, Dcpart- ment of Primary Industry, Canberra, A.C.T. 2600 Australia.

from phytoplankton hauls at a regular station in the harbor, as well as from investi- gations of earlier blooms. Further studies were made during the 1974 season. Here I summarize these observations.

I acknowledge the assistance of those who provided time or facilities during this investigation including personnel of the De- partment of Agriculture, Stock and Fisher- ies, the Papua New Guinea Dcfence Force, Officers of the Papua New Guinea Hydro- graphic and Meteorological sections, the Australian Information Service, and the Australian Development Assistance Agency. I also acknowledge the help of K. Wabis, B. Dauka, J. Peters, J. Kailey, S. Rainer, A. Adams, F. J. R. Taylor, and D. Tranter.

Methods

Regular aerial observations between Port Moresby and Hood Point were carried out at altitudes of between 300 and 400 m in various light aircraft. Visibility of blooms was improved scveralfold by using polarizing sunglasses. Samples in this area, other than in Port Moresby Harbor, were taken by lowering a Nansen bottle from a heli- copter hovering directly over a bloom. In the harbor, samples were generally collected in plastic 1.5-liter bottles.

Salinities were measured by AgNOs titra- tion, checked against standard seawater, except in 1974 when a salinity-temperature conductivity meter ( G.M. ) was used. Phy- toplankton hauls in various parts of Papua New Guinca were made with a 0.5-m, 48 p, polyester plankton net. Regular sampling in Port Moresby Harbor was done with a similar 15-cm diameter net; at the

LIMNOLOGY AND OCEANOGRAl?IIY 234 MARCH 1977, V. 22 ( 2)

P. bahamensc in Papua New Guinea 235

Table 1. Proportion of Pzjrodinizcm bahamense in plankton hauls at various stations with 48-p plankton net.

Sta Site Date Sal&nity ( /oo)

Tgw Pyrodinium "/o ( c>

5

z

10 China Straits 1 OJu173 33.9 0.8 11 South East edge Milne Bay lOJu173 32.3 4.7 12 Alotau, Milne Bay lOJul73 26.8 16.7

z 15 16

17 Garili (near Talasea) lOMay 33.8 31.2 18 Pangalu (near Talasea) lOMay 33.6 31.9 19 Kimbe lOMay 33.6 31.6

20 21

;g 24 25 26 27

28 29 30

;; 35 36

Moresby - Yule Island

Yule Island 18Apr73 Yule Island 11May73 Gubbins Point 18Apr73 Gubbins Point Redscar Point

llMay73 17Apr73

Redscar Point lOMay Haidana Island lOMay Port Moresby Harbor 13Apr73 Port Moresby Harbor 8May73

Moresby - Cloudy Bay

Port Moresby Harbor 20Mar73 33.1 Kapa Kapa 22Mar73 33.0 Hood Point 22Mar73 3205 Hood Lagoon 23Mar73 31.8 Between Keppel Point and Urapi Point 24Mar73 31.4 Cloudy Bay 26Mar73 14. lt

Milne Bay area

Trobriand Islands

Losuia Boli Point Kiriwina Lagoon Muwo Island

25May73 25May73 25May73 25May73

30.2 35.2 g.2

n

West New Britain (Willaumez Peninsula)

Madang District

Binnen Harbor Madang Harbor Nagada Harbor Kranket Island (tidal lagoon) Sek Harbor Bos-trem Bay Mugil Point Karkar Island

Rabaul

Rabaul Harbor 16Aug73 Matupit Island (near Rabaul) Karavia Bay (near Rabaul)

lGAug73 17Aug73

Wewak

West Harbor Wewak Harbor

OPfshore Port Moresby

g"~8'O"S, 147'88'0"E 1o021'o"s, 147 88'O"E 10,26'3O"S, 14g 32'O"E 10 33'O"S, 148 0'O"E

21Aug73 21Aug73 21Aug73 21Aug73 21Aug73 21 Aug73 26Aug73 24Aug73

19Jul73 19Ju173

2Apr74 2Apr74 2Apr74 2Apr74

33.0 33.4

2; 3314 30.9 32.7 34.0

34.4 33.0

32.5

;;2 33:8

0.2 negative

0.3 nega-tive

0.7

2::; 2.5 0.1

27.0 negative 27.0 negative 27.5 negative 27.9 negative

2:; negative

29.5 23.6 29.5 29.6 29.9 30.9 29.5 29.7

Aa!: 1:4 1.7 0.1

rlegative negative negative

negative negative negative

29.5 29.5

29.2 29.2 28.9 28.9

0.2 negative

1 .4 0.6 0.9 1.2

236 Maclean

145”d MAWS

a’l50”E

3x. Q /3

?ig. 1. Index map of Papua New Guinea region.

fixed station near Napa Napa, hauls were made between 0900 and 1000 hours over a distance of 400 m between a buoy and a prominent landmark. Towing speed was about 1 m s-l. Hauls other than near- surface tows were made using a simple rope choke device near the mouth of the net.

Various phytoplankters were counted for proportionality and concentration analysis was by hemocytometer or Millipore filtra- tion Generally, about 400 organisms were counted, except when PyrocEinium was very dense, when up to 1,600 were counted.

During March and April of the IQ74 Port Moresby red tide season, water temperature and salinity were measured at l-m

depth intervals for stations within and outside red tide areas. Atmospheric conditions were recorded. Depth of the Pyro- dinium band was noted by divers. Visible red tides were detected by harbor transects in a fast (25 km h-l) boat. Polarizing sunglasses were worn while making observations from about 6 m above sea level.

Results

Papua New Guinea distribution of P. bahamense-The species was present in plankton samples from stations on the south coast of the mainland from Yule Island to Cloudy Bay; Milne Bay; on the north mainland coast at Morobe, Madang, and We- wak; and on the Willaumez Peninsula of

P. bahamense in Papua New Guinea 237

, FAIRFAX HAR6OUR

Areas of red tide sightings (hatched) in Port Moresby region. Dotted lines-coral reef. Fig. 2.

New Britain. It was present in samples taken 34-60 km offshore south and southeast of Port Moresby, but absent in hauls from the Trobriand Islands and Daru. De- tails are shown in Table 1 and locations in Fig. 1.

Distribution of reel tides--Red tides caused by Pyrodinium in these waters have occurred on the south coast from Port Moresby east to Milne Bay (Fig. 2 shows the area between Port Moresby and Hood Point where shellfish poisonings took place

in 1972), on the north coast between Mo- robe and Lae (Fig. 3), and on the west coast of New Britain ( Fig. 4)) especially around the Willaumez Peninsula (Maclean 1973). Paralytic shellfish poisoning, a product of certain dinoflagellate blooms, has also occurred in the Trobriand Islands and at Manus Island ( Maclean lQ73). The responsible dinoflagellates are unknown at this time. Only one other species of dinoflagellate has been known to form a red tide in Papua New Guinea waters, Gony-

238 Maclean

Fig. 3. Areas of red tide sightings (hatched) in Morobe district. Dotted lines-reef boundaries; broken line-200-m depth contour.

aulax polygramma, which bloomed in Bos- trem Bay near Madang in 1968 (B. Sweeney personal communication). In this locality, P. bahamense was absent at the time from open coastal waters but was found in land- locked salt water pools on Kranket Island in Madang Harbor.

Coastal zones of Papua New Guinea sub- ject to Pyrodinium red tides have little in common. Rainfalls range from 90 to 500 cm per year. Geophysical nature varies from limestone to volcanic, while topography ranges from low islands to extinct volca- noes. The only common features of these zones arc the presence of mangroves, fring- ing coral reefs, and some sheltering from prevailing winds during blooms. Physical features of Port Moresby Harbor, where most observations were made, are shown in Fig. 5.

Composition of blooms-Samples of red

Fig. 4. Areas of red tide sightings (hatched) on Willaumcz Peninsula (New Britain). Dotted lines-reef boundaries; broken line-200-m depth contour.

tides analyzed had 84% to >99% Pyrodin- ium by numbers of individuals. Details are shown in Table 2. The other organisms (in 48-p net samples ) were mainly di- atoms, except on one occasion when large numbers of Crustacea were present. Trich- odesmium sp. was a significant phyto- plankter in one sample.

Table 3 gives Pyroclinium densities at various sites in previous blooms. Data for the 1973 blooms in the Moresby-Hood Point area are shown in Table 4. The high- cst concentration observed was 5 x 10” liter-l in Port Moresby Harbor, 27 March 1973. Concentrations over about 200,000 cells liter-l indicate red tides visible from the air. However, most of the samples were near-surface, while the heaviest Pyrodinium concentrations were often deeper-up to 4 m in surface-visible blooms.

Seasonality-Rough estimates of red tide seasons in Papua New Guinea waters have been given by Maclean (1973). Blooms in the Port Moresby area seem directly related to rainfall, which is highly seasonal; most rainfall is between Dccem- ber and June. Figure 6 shows the duration of reported red tides in the vicinity of Port Moresby, compared with monthly rainfall.

240 Mackan

Table 3. Concentrations of Pyrodinium bahamense in red tide blooms in Central district, May 1972, and Morobc Lagoon, December 1972. (Data from Maclean 1975. )

Sample Pyrodinium/ L Salinity Temp Comments (%,) C°C)

1 17May72 Bootless Bay, 10 km 37,000 * 26.2 in clear water near red tide

2 east Port Moresby

17May72 Bootless Bay !l9G,OOO * 26.2 in medium red tide 3 17May72 Bootless Bay * 26.2 in medium red tide 4 17May72 Off j/alai Village,

G19,OOO 2,000 * 27.7 clear water. Fatal shellfish

2

SO km east Port Moresby 2Dec72 Morobe Lagoon

poisonings there 29Apr72

2Dec72 Morobe Lagoon 3,500,000 25.1 30.5 in dense red tide

270,000 24.7 29.8 in dense red tide

*Not recorded.

adjacent to Morobc Harbor, show peaks in October-November ( 1970)) December ( 1968, 1969), and January ( 1967).

In view of the public health risk posed by red tide, fortnightly observation flights were made along the coast from Port Moresby to Hood Point from June to De- cember 1972, and thereafter weekly flights until early July 1973. Thus it was possible to determine more accurately the seasonality of the 1973 blooms. The flight path followed the coastline and returned along the outer barrier reef. The first sighting was in Port Morcsby Harbor on 15 Febru- ary 1973; the last was there also, on 26 June. During this period, red tides were common in the harbor and along the coast. (Fig. 8). A general description of the

blooms has been given earlier (Maclean 1973). At the beginning of the red tide season, blooms were prominent early in the mornings. Observation flights were carried out between 0730-0930 until April 1973, when it was noticed that occasionally blooms were becoming more widespread later in the day, reaching a maximum around midday. Later flights were run between 1130-1300.

Figure 8 shows the weekly position of the Pyroclinium blooms during the season. The maps arc based mainly on aerial sightings, supplemented, in the vicinity of Port Moresby only, by some observations from vantage points. There was no pattern in the sequence of bloom appearances that might suggest a general movement or

Table 4. Conccntrationi of Pyrodinitcm bahamense in water samples from Central district, March- June 1973.

Sample Pyrodinium/e Sal$;ty T,";p Comments "0.

1 6Mar Moresby Harbor 2 20Mar Kapa Kapa 7:;':;: 3 20Mar 3 km NW Kapa Kapa $62 : 400 4 20Mar 7 km NW Kapa Kapa 5 20Mar Gaile "?~0000 (1 20Mar 6 km NW Caile 2,170:OOO '7 2OMar Barakou zj76,OOO 8 20Mar Bootless Bay 549,000 9 27Mar Moresby Harbor 5,010,000 10 27Mar Moresby Harbor 1,282,960 11 15May Moresby Harbor

16May 234,000

12 Moresby Harbor 2 16May

u2,goo

16May Moresby Harbor 110,200 Moresby Harbor

16May 83,600

15 Moresby Harbor 16 22May Moresby Harbor T;$:: 2 22May Moresby Harbor G5'900

22May Moresby Harbor 66:600 290 22Jun Moresby Harbor 26,540

22Jun Moresby Harbor 72,450 21 22Jun Moresby Harbor 267,030

32.5

28.5

30.4 in medium red tide 30.7* in visible, diffuse red tide

in medium red tide on edge of dense red tide in clear water in dense red tide in visible, diffuse red tide in medium red tide

30.5 in dense red tide 30.5 in dense red tide 28.6 in medium red tide 28.5 surface water, with diffuse red tide at I-jm 28.5 surface water, with diffuse red tide at I-3m 28.5 surface water, with diffuse red tide at I-3m 28.5 surface water, with diffuse red tide at I-3m 27.9 surface water, with diffuse red tide at I-Jm 27.9 surface water, with diffuse red tide at I-3m 27.9 surface water, 27.8 in diffuse 27.8 in diffuse I

with diffuse red tide at I-3m visible) red tide visible) red tide

27.8 in medium red tide

* Temperature in Port Moresby Harbor at 0900.

I?. bahamense in Papua New Guinea 241

Fig. 6. Monthly rainfall at Port showing red tide scale in cm.

seasons ( black bars ) . Rainfall

-

i

1973

Moresby,

spread of red tide along the coast during the season. Neither was there any doubt that blooms originated close to the coastline: they were never seen near or outside the barrier reef in the area under regular aerial observation. Water conditions became favorable for bloom formation over a large area of coasthne virtually simul- taneously. Red tide appeared near Amazon Bay, southeast of Port Moresby (Fig. l), on 20 February 1973, 5 days after the first sighting in Port Moresby Harbor (Maclean 1973).

Regular near-surface (upper 0.5 m) phytoplankton hauls were made at a station in Port Moresby (Fig. 9). Sampling began at the end of May 1972, and data are available to August 1973, so that both prc- and post- bloom plankton populations were obtained. Sampling was fortnightly until May 1973, then weekly until the end of the program. Counts were made to determine the percentage by number of Pyrodinium and to estimate numbers per liter of seawater (Ta- ble 5). Pyrodinium formed an insignificant percentage of the plankton population, as sampled by 48-p net, until mid-January 1973. Thereafter, the proportion of Pyro- dinium remained >2% of the sample, except for a period in May when there was a lull in red tide sightings in the harbor, until about 3 weeks after the last visibIe red tides. Then, Pyrodinium became once again an insignificant constituent of the plankton.

The proportionality of Pyrodinium in the harbor plankton samples during the 1973 red tide season is shown in detail in Fig.

Fig. 7. Available discharge data by month for Waria River, Morobe district. Discharge scale in m3 X 10’.

10 together with weekly rainfall data at two stations near the harbor and the sequence of red tide appearances there. The estimates of numbers of Pyrudinium per liter in the samples followed the same pattern. In the months preceding and after the red tide season, there were always fewer than one individual per liter; from the end of December 1972 to mid-July 1973, there were always significantly more than one per liter. The counts given are based on estimated volume of water sampled. They are uncorrected for net efficiency but provide relative concentrations of the dinoflagellate throughout the year.

Vertical distribution and movements- Blooms of P. bahamense in Port Moresby Harbor always formed a discrete horizontal orange band in the water column, generally l-3 m thick. The upper edge of subsurface blooms was quite distinct, while the lower edge was often a gradation of intensity through a vertical distance of 0.3- 0.5 m. On different days, the blooms appeared at various depths. Some observations of the depth at which the band appeared were made by diving during the 1973 and 1974 red tide seasons (TabIes 6 and 7). Depth to the upper surface of the band ranged from O-6 m, with one cxcep- tion-13 April 1973-when the bloom ap- pcared at 9 m.

Apart from day-to-day variations in band

242 Ma&an

-1

I_----.- I

I ------ ---- .--

-I

18-2413173 /

I 1

.::..

.’

25-3113173

6-1215173

~--------- 1

13-1915173

~.-:\

Fig. 8. Areas of red tide (blackened), 1973 season, Port Moresby to Hood Point (from aerial survey). Red tides were observed only in the weeks depicted, except for 11-17 February, 25 Feb- ruary-3 March, and 24-30 June when there were patches in Port Moresby Harbor; during 25 Feb- ruary-3 March there was also a small patch off Kapa Kapa.

depth, visible blooms were sometimes absent for a period. For example, during the 1973 season they were absent for 3 weeks in June along the whole coastline under aerial surveillance. In Port Moresby Har- bor, they were sometimes absent even when prevailing weather might have suggested ideal bloom conditions-windless, hot,

sunny days (various citations in Quayle 1969). On the other hand, they have been observed to persist in both sunny and cloudy days in southeasterly and northwesterly winds of up to 15 knots and in rain. Further, as noted earlier, blooms became more widespread later in the morning as the season progressed. Red tides have been

P. bahamensc in Papua New Guinea 243

Fig. 9. Port Moresby Harbor showing 5-m ( dotted line) and 10-m (broken line) depth contours, regular plankton station near Napa Napa ( 1 >, and 24-h plankton station (2). A-F are stations occupied in a transect showing undulations of red tide band shown in Fig. 13.

visible from the air as early as 0700 hours; on other occasions they have not appeared until I.100 hours.

During the 1974 red tide season in Port Mores by, observations on these phenomena were made to determine the underlying mechanisms. Blooms were first noticed as a faint brown turbidity in the normally green water. The color became orange and more distinct as the blooms rose toward the surface, in most cases between 08.30 and 1130 hours (Table 7). The area occupied by visible blooms was generally the central inner half of the main harbor, between the 5- and 10-m depth contours (Fig. 9)) cov- cring usually about 518% of the total harbor surface area (Table 7). On 21 and 23 April 1974, red tide covered about 22% of the harbor surface, extending back into Fairfax Harbor as well as into deeper waters of the main harbor. There was no ap- parent correlation with tides or sunlight. Blooms were present on both sunny and overcast days and were remarkably constant in their position. Winds, which ranged from 0 to about 15 km h-r on red tide days, were mostly from the southcast

Table 5. Proportion of Pyrodinium bahamense (as percentage by numbers of total plankton) and estimated number per liter in 48-p plankton net hauls, Port Moresby Harbor, 1972-1973.

Date Pyrodinium/liter % Pyrodinium in total plankton

26May72 ?Jun72

14Jun72 Z'lJun72

6Ju172 205~172

3Aug72 22Aug72

5Sep72 1;;:;;;

17oc t72 31 oc t72 l4Nov72 28Nov72 12Dcc72 2'7Dec72 17Jan73 23Jan73

6Feb73 20Feb73

6Mar73 20Mar73

3Apr73 19Apr73

'iMay 8May73

22May73

2;2~;; 12Jun73 14Jun73 19Jun73 26Jun73

3Ju173 1OJu173 17Ju173 245~173 31Ju173

9Aug73 lhAug73 21Aug73

500,000 <I <I <I <I (1 <I (1 <I <I <I (1 <I Cl 41 C?

&

z:o 2,&O 270 2;290 360 170 40 20 500 3,150 90 290 530 1,850 4,560 240 20 380

Cl (1 (1 <I <I

9X 010 0.0 0.0 0.0 0.0

007 0:o

1.2 0.3 h.6 4.1

20.9

2.5

20.5 93.7s 41.8 40.7 61.U 78.1 50.8 53.9

2.7 39.1

0”:; 0.5 1.0 0.4

* Red tide visible.

until a northwesterly change occurred near the end of the sampling period. As the southeasterly set progressed, red tide in the harbor dccrcased in abundance and ap- pcared later in the morning, until it disappeared a few days bcforc the weather change. A band of Pyrodinium was still in evidence, but was unusually narrow and at a depth of 6 m. With the reversal of wind flow, red tide appeared at its earliest, and most abundant. Further rain followed that change but began to fall after the red tide had appcarcd at the surface.

244 Maclean

DEC ; JAN; FEBIMARIAPR; MAY ;JUN

Fig. 10. Proportion of Pyrodinium bahamense in surface plankton at a station in Port Moresby Harbor, December 1972-July 1973. Red tides were present intermittently from February to July, black bars ( top ) . Rainfall data by week ( in cm ) shown for two stations near harbor-Port Moresby (P.M.) and Kanudi (K.).

Details of these phenomena are included in Table 7, with some salinity and temperature data. Detailed examples of typical salinity and temperature profiles from surface

Table 6. Depth of Pyrodinium layer in Port Moresby Harbor between 0900 and 1000 hours on various days during 1973 blooms. Near-surface salinity (0.6 m) also shown.

Date Depth (m): to Thickness Surface upper surface of band

15Feb 16Mar 20Mar l3Apr 19Apr.

IMay 5Jm

12Jun 19Jun 22Jun

: 7.5 35.9

0.6 :.4 33Tl 2 35.3 1.5 33.4

z ;E 2 y

g:g

33k

to 10 m are shown in Fig. 11. Patterns of thermoclines and salinity gradients varied considerably during the observation period. There was no discernible correlation between the shapes of these patterns and the depth of the Pyrodinium band.

The widespread red tide on 23 April was associated with an unusual salinity and temperature gradient ( Fig. 11) in which the normal pattern of decreasing temperature with depth was reversed and the salinity gradient was more marked than usual. At shallower stations ( 10 m), the increasing temperature gradient was maintained throughout the water column, At deeper

Table 7. Observations on red tide blooms, Port Moresby, 1974. ++++-22% of total harbor surface covered; + + +--5-87 o covered; $+-l-5% covered; +-<l% covered. (Band depth in m.)

Date Time Overall Abundance Midband Midband wind red tide band depth

light salinity

High tides

appeared and thickness tempera&u-e range ( C)

';8i::,

27Mar 1130 3.5-6 ++ 23.1-29.3 31.7-31.9 Bright sun light SW 1010 intermittent from 1100 23118

291ular

5Apr

YApr

13AQr 'I7AQr

IRApr

IYApr

21Apr

25Apr

1045

1115

0930

0930 1115

1100

absent

bePore 0830 0030

3 -3

0.5-3

0.5-4

0.5-3 2 -5

0 -3.5

6 -7

0 -3

0 -3

+++

++

k+

+-c+ ++

+

++++

++++’

29.2-30.4 31.8-32.1

30.3-39.6 31.9-32.2

30.3-30.6 31.9-32.1

Uright sun light SE 0148 from 1200

Intermittent Nil -loud 9;;: Bright sun Nil 0958

2305 30.1-30.7 30.4-30.5

30.7 31.8

23.9-30.4 31.9-32.0

no data no data

28.629.0 29.9-30.2

31.m31.9 31.7-31.8

Brqht sun light SE l&d Overcast moderate SE 0644

1906 Intermittent moderate SE 0703 cloud 1327 Intermittent light SE '3722 cloud 1950 Overcast, moderate NV 080/1 rain 2046 Bright sun, ,moderate NW 0058 rain In 2204 afternoon


stations (11-16 m) there was a thermocline at 5-7 m, below which was the normal decreasing gradient to the bottom (bottom not shown in Fig. 11).

Atmospheric pressure in the Port Moresby area decreased during the sampling period, reaching a minimum on the day when the diminishing red tides finally disappeared from the surface ( 19 April 1974). Reap- pearance of dense blooms 2 days later coin- cided with a marked reversal of pressure trends associated with the change of weather (Fig. 12).

Underwater observations of the red tide band in Port Moresby Harbor at various times indicated that although visible red tides when present generally covered a small fraction of the harbor surface, the band itself was distributed as a more or less continuous discrete layer over a more extensive area. Visible blooms occurred when portions of the layer came close enough to the surface to be seen. An example of this undulatory behavior in a transect of Port Moresby Harbor on 16 March 1973 is shown in Fig. 13 (site shown in Fig. 9). There was a discrete layer of Pyro- dinium, identical to that present during visible blooms, but too deep to be seen from surface vessels, throughout the harbor. The maximum variation in its depth across the transect was >l m. Other observations have shown that the undulations can exceed 2 m.

Reference to Table 7 shows that the extent and time of vertical migration during the day is not a constant behavioral feature of Pyrodinium in Port Moresby Harbor, The vertical distribution of Pyrodinium bands in the harbor provides a convenient mea- sure of the extent of vertical migration. In Table 7 bands are shown to have appeared at different times, rising to diffcrcnt levels on different days, to some extent indepen- dently of temperature and salinity gradients and degree of insolation, The time of

afternoon disappearance of visible red tides was related to the time of morning appear- ance. When blooms reached the surface before 0900 hours, they remained visible until after 1600 hours; a bloom appearing at 1045 disappeared around 1430, and one becoming visible at 1130 disappeared at about 1340.

Diurnal migration was investigated with a series of plankton hauls taken every 2 h over a 24-h period between two buoys in Port Moresby Harbor, at the surface and 5 m, 30-31 January 1973. The results (Fig. 14) showed a minimum presence of Pyro- dinium in the upper 5 m between 1800 and 2400 hours, followed by a gradual rise until dawn ( 0600 hours). The proportion and quantity of Pyrodinium then declined, with an anomalous peak in numbers at 5 m at 1400 hours, apparently due to the ingress into the sampling area of a subsurface concentration or band of Pyrodinium.

Life cycle-The percentages of dividing Pyrodinium cells in samples over 24 h in Port Moresby Harbor are shown in Fig. 15. Division rate reached a maximum during midmorning, 0800-1600 hours, and a minimum at 0200 hours. Maximum division ac- tivity ( 23,4% ) indicates a cell generation time of about 4 days.

In culture experiments an inoculum of Pyrodinium was introduced into a nonster- ile medium of filtered seawater (T = 29.5OC) containing 0.1% autolyzed yeast and illuminated by a 60-W globe. The generation time over the first 30 h was 9 h; after that, an unidentified ciliate protozoan began to overtake the Pyrodinium. A con- trol culture without yeast failed to grow.

In Port Moresby Harbor, Pyrodinium is catenate. Chains of up to eight thecate cells have been observed regularly (Fig. 16). Duplets and quadruplets were the mast common forms. During blooms, con- centrating the cells, as in plankton hauls,

-____--- --

3

Fig. 11. Representative examples of salinity and temperature gradients (in m) in Port Moresby Harbor, March-April 1974. Depth of Py~odinium bloom indicated by black boxes.

246 Maclean

27.3.74

29.3'74

31 313 I

I :

I'

: IJ

I Sll I

I 1130 ;

25 2'9 310 3'1

P. bahamense in Papua New Guinea

T'C

19*4-74

S%, 31 32 33

O- I /

//

J’

J’

5-

st 2

33

I A

I ‘* )

I’ I

l : / / /’ / I I 2’9 do-----J

TOC

S%o

247

23*4*74(cont)

S%O

248 Maclean

Fig. 12. Atmospheric pressure (in millibars ) measured at sea level 0900 hours, March and April 1974. Relative abundance of red tide indicated by vertical bars. O-Absence of red tide.

provided a stimulus for ecdysis. The rate of thecae shedding was measured in a dense population taken by plankton net on 28 June 1973. The cells were held in a 2- liter beaker, aerated, at a density of 196 x 10G liter-l. Fifty percent ecdysis was ac- complished in about 3 h 20 min ( Fig. 17). In a less dense population, 68 x 10” liter-l, 50% thecae loss required 9 h 30 min. In the latter experiment the gymnodinioid cells resulting from thecae loss appeared to remain for over 3 h before developing thecate cells were seen. Ecdysis was not observed in natural blooms (maximum concentration observed 5 x lo6 liter-l).

,Salinity-The salinity range for Pyro- dinium in Papua New Guinea is 24.7-36.8%0. Blooms have been restricted to the range

OL 2

m

3

I I I I 1 A B C D E F

Fig. 13. Depth and thickness of a Pyrodinium layer at six stations (A-F, Fig. 9) in Port Moresby Harbor, 16 March 1973. Spacing of vertical lines indicates visually evaluated relative concentration of cells.

I lb00 0 1800 2200 0200

1 0600 1000 IL00

Fig. 14. Percentage (upper) and estimated number per liter (lower ) of Pyrodinium in plankton over 24 h, Port Moresby Harbor, 30-31 Janu- ary 1973. Solid line-surface hauls; broken line- 5-m hauls.

28.5-36.8%0, except for the outbreak in Morobe Lagoon, when there was a dense Pyrodinium population near the surface at .24.7%0.

The phototactic behavior of Pyrodinium was used to determine its lower salinity limit in vitro. Cells were introduced into a vertical 6-cm-diameter Perspex tube containing filtered seawater illuminated from

L I I I I I I

1400 1800 2200 0200 0600 1000 1400

Fig. 15. Percentage of Pyrodinium cells dividing at different times over 24-h period, 3031 January 1973.

250 Maclean

non-motile

MOHE UYPNOIDS

Fig. 18. Stages in Pyrodinium bahamense life cycle.

Unique features of the Papua New Guinea variety of Pyrodinium include the ability to produce paralytic shellfish poison (saxitoxin?) and the formation of long (up to 8 cell) chains during division. The New Guinea Pyrodinium differs in some behavioral patterns as well. The swimming speed of P. bahamense in Puerto Rico is 30 cm h-l, and the cell population is mixed through the water column by even light winds ( 5-8 km h-l) ( Seliger et al. 1971). Ceratium furca, which occurs with P. bahamense there, swims at about 60 cm h-l and maintains its distribution under these conditions ( Seligcr et al. 1971). In Port Moresby, Pyrodinium can swim at least as fast as 60 cm h-l and can maintain its near- surface presence in strong ( 15 knot) winds.

The previous best in vitro division time of P. bahamense ( 4-5 days : Biggley et al. 1969) has been exceeded dramatically in a culture experiment during the present study. Division rate is an important factor in the maintenance of Pyrodinium popula-

tions in Oyster Bay, Jamaica (Scliger et al. 1970)) and in Phosphorescent Bay, Puerto Rico ( Seliger et al. 1971). The division rate when combined with phototaxis and diurnal winds is just sufficient to bal- ance loss of cells from these luminescent bays as a result of water currents, How- ever, if the species can approach in vivo the nutrient-induced in vitro division time of 9 h, then complex survival patterns in Pa- pua New Guinea are not necessary,

Another possible behavioral anomaly noted here is the duration of the gymnodinioid phase. Buchanan ( lQ68) found that naked cells of P. bahamense persisted for about 30 min in Jamaica. They can remain for at least 3 h in overcrowded suspen- sions in Papua New Guinea.

A life cycle of the species based on the findings OF Buchanan ( 1968), Wall and Dale ( 1969), and my observations is illus- trated in Fig. 18. Cysts have not been observed in Papua New Guinea populations, however.

Finally, the Papua New Guinea red tide organism is evidently not as stringent as the Caribbean red tide organism in its require- ments for bloom conditions. The environ- mental conditions which produce Pyrodin- ium phosphorescent bays in the Caribbean are shallow basins (l-2 m deep) lined by mangroves with a confined shallow en- trance to the sea and prevailing daily winds blowing perpendicular to the en- trance or into the bay ( Seliger et al. 1971). These conditions eminently describe Mo- robe Lagoon, New Guinea, where Pyrodin- ium red tides occur annually (Maclean 1975). Phosphorescence is associated with the blooms. The mangrove-lined lagoon is shallow (2 m) and connected to the outer harbor by a very narrow channel. Phosphorescence is also a feature of Tro- briand Island red tides in a shallow mangrove-lined lagoon area ( Maclean 1973). However, it is evident that these conditions are not necessary for seasonal blooms in Papua New Guinea, where red tides occur in more exposed areas.

The absence of nocturnal displays in deep bays like Port Moresby Harbor indi-


cates that such displays are an artifact of shallow waters where the dinoflagellate is prevented from sinking below surface influence or disturbance at night. Indeed vil- lagers at Tupusclea, a village built over shallow reefflats in Bootless Bay, adjacent to Port Moresby, often wade through strongly phosphorescent water at night during the red tide season. Taylor et al. (1966) noted that P. bahumense rose to the surface at night in Jamaica unless rain-induced stratification prevented it.

Most research on dinoflagellate blooms has favored a mechanism involving seasonal enrichment of coastal waters by land runoff directly from shore or in river discharge, although localized upwelling is said to be responsible for some offshore blooms (IIela 1955; Bainbridge 1957; Bra- arud and Heimdal 1970).

Recently, more attention has been paid to the role of bottom sediments. Iizuka (1972) found that the Japanese dinoflagellate Gymnodinium type-‘65 tolerates anoxic or near anoxic conditions in Omura Bay and utilizes sulfide from the sediments. Uyeno and Nagai (1973) found that mud extracts promoted growth of Heterosigmu inlundica but only during the period of the year when natural blooms occurred, Iwasaki (1973) con- cluded that most Japanese neritic red tide species required trace metals, iron or manganese, and special organic compounds, both of which Honjo (1974) felt were derived from bottom scdimcnts leaking through the discontinuity layer or directly by wind-induced mixing,

Both low salinity and organic enrichment of coastal waters are usually required for blooms of armored dinoflagellates, such as those of Gonyaulax tamarensis in eastern Canada (Prakash et al. 1971). These conditions occur during monsoon seasons in the tropics (Qasim ct al. 1972). However, Pyrodinium is atypical, having an optimum salinity of around 35.7g0 (Wall and Dale 1969).

Since some of the red tide prone areas of Papua New Guinea are not directly connected with rivers (Port Morcsby IIarbor

is a drowned valley), organic enrichment would presumably come from local sources, mangroves or land runoff. In view of the salinity prcfcrencc of Pyrodinium it is un- likely that land runoff is an important factor, but the coincidence of red tides with the rainy season on the south coast of the New Guinea mainland suggests such an as- sociation. Peaks in river discharge on the Morobe coast (north mainland) occur during the red tide season there. There is evidence that substances from land are of little significance in promoting Pyrodinium blooms. In Phosphorescent Bay, Jamaica, the nutrient source for P. bahumense blooms is said to be sediments mixed into the shallow water column by daily turbu- lent diffusion (Seliger et al. 1970). Sweeney (1975) commented that a bloom of P. bahamense which she witnessed near Ma- dang (see Fig. 1) in 1969 was during the dry season, when there was no runoff.

The 1974 observations of red tides in Port Moresby Harbor indicate that wind is at least as important as rainfall in promoting and sustaining Pyrodinium blooms .there. The monsoon or rainy season is ac- companied by almost continuous northwesterly winds on the south coast. During the 1974 observations, a southeasterly set characteristic of the dry season, evidently caused a decrease in the occurrence of red tides in Port Moresby Harbor. Rainfall during this set (10-19 April) was negligi- ble. The massive upsurge in bloom ap- pearance took place later following the re- turn of the monsoonal northwesterly winds, before rain began to fall, When salinity- temperature data were gathered 2 days later (23 April), 16 mm of rain had fallen. The unusual gradients on that day (Fig. 11) indicate that more than simple mixing was involved.

The lowered salinity and the dramatic effect on Pyrodinium density suggest that cnrichmcnt of the water column to at least 10 m was combined with dilution by freshwater, mainly from the inner (northwest) end of the harbor, carried down the harbor under the influence of offshore wind. The main red tide arca of the harbor was in wa-

252 Maclean

ters of 10-m depth and less, so that mixing of bottom sediment is clearly important. Since Pyrodinium favors relatively salinc water, as noted above, the lower salinities and reversed temperature gradient associated with runoff were merely indicators of the source of nutrient and not catalysts of the widespread blooms. The important factor was clearly mixing of water derived from the inner shallows of the harbor, its influence weakening with distance from the windward end. This hypothesis explains the occurrences of red tide in the inner part of the main harbor and their absence from its outer parts.

The cause of the wane in red tides toward the end of the southeasterly set during the 1974 observations can be explained in terms of the mechanism proposed by Seliger et al. (1970) for Pyrodinium in Ja- maica. There, nutrients are apparently obtained during vertical diurnal migration, since there would be insufficient nutrients to support bloom concentrations of cells otherwise. Holmes et al. (1967) proposed a similar mechanism for blooms of Gonyaulax polyedra. The southeasterly set in April 1974 which carried oceanic influence into Port Moresby Harbor gradually caused Pyrodinium to exhaust the water column of nutrients, resulting at first in a decrease in the extent and duration of visible red tides and finally in a failure of the Pyro- dinium population to migrate upward in the absence of nutrients in the upper lay- ers. In essence it appears that phototactic behavior in P. bahamense is a facultative response to nutrient availability rather than an obligatory species behavior pattern.

The following hypothesis is put forward to explain the overall pattern of red tide seasonality in the Port Moresby area. Con- stant southeasterly winds from May/June to November/December result in the harbor and coastal areas being filled with offshore water, typically nutrient-poor in the tropics. Nevertheless, salinity and temperature patterns can support Pyrodinium blooms. From December/ January, northwesterly winds become continuous, bringing rainy periods until April/May. This wind rc-

leases nutrients necessary to Pyrodinium blooms from the inner harbor shallows, especially from mangrove areas, causing spreading, diffusion, and mixing of nutrient-rich water. Rain-induced runoff may add to the nutrient supply. During the monsoon season, mainly toward the latter end, the northwesterly sets alernate with those from the southeast. During these latter periods of onshore winds, the blooms are cut off from nutrient sources and decline until the next offshore set. Finally southeasterly winds set in for the dry, tradewind season and blooms disappear as offshore-derived water again permeates inshore areas. This explanation of the red tide season would apply equally to all red tide areas of the south coast. The other affected areas of the mainland and islands have not been stud- ied in sufficient detail to confirm that the pattern is general.

Some workers have doubted the capacity of nutrient-poor waters to support bloom concentrations of dinoflagellates and have found accumulation mechanisms necessary to explain the phenomenon (Rounsefell and Nelson 1966)) especially since some species do not undertake significant diurnal migrations. Gymnodinium breve remains at the surface at night as well as by day (Se- liger et al. 1975). Wyatt (1975) summarized the limitations of models which would produce lines, slicks, or patches of red tide; Eppley and Harrison ( 1975), citing Kamy- kowski, noted that semidiurnal internal tides above a discontinuity layer would produce lines of red tide parallel to shore.

In Papua New Guinea, lines of red tide were regularly observed in Bootless Bay, adjacent to Port Moresby, where such lines were irregular and patches were common. Patches were the most common form in other areas also. However, these different forms appear to be simply a reflection of two behavioral features of Pyrodinium noted during this study-day-to-day variations in diurnal migration, and undulation. The combination of these two characteris- tics explains the diffuse edges of patches that arc often observed. A bloom can be present below the surface over a very wide


area with little or no visible display. The windrows seen occasionally are no doubt due to an accumulation mechanism (Lang- muir cell formation), but the lines are derived from a subsurface population of the same order of cell concentration. In fact, artificial windrows were often observed when subsurface blooms, invisible or barely visible from the surface or aircraft, were churned upward by propellors of passing boats to produce a rust red wake. It appears that the extent of Pyrodinium blooms is independent of their shape as viewed from the surface, patches being an artifact of undulation while lines or streaks are an artifact of an accumulation mechanism, not the cause of blooms per se.

References

BAKVBRIDGE, R. 1957. The size, shape and density of marine phytoplankton concentrations. Biol. Rev. 32: 91-115.

BIGGLEY, W. I-I., I% SWIFT, J. J, BUCHANAN, AND H. H. SELIGER. 1969. Stimulable and spon- taneous bioluminescence in the marine dinoflagellates, Pyrodinium bahamense, Gony- aulax polyedra and Pyrocystis lunula. J. Gen. Physiol. 54 : 96-122.

BRAARUD, T., AND B. R. HEIMDAL. 1970. Brown water on the Norwegian coast in Autumn, 1966. Nytt Mag. Bot. 17: 91-97.

BUCEIANAN, R. J. 1968. Studies at Oyster Bay in Jamaica, West Indies 4. Observations on the morphology and asexual cycle of Pyro- dinium bahamense Plate. J. Phycol. 4: 272- 277.

-. 1971. Studies at Oyster Bay in Ja- maica, West Indies, 5. Qualitative observations on the planktonic algae and protozoa. Bull. Mar. Sci. Gulf Caribb. 21: 914-937.

EPPLEY, R. W., AND W. G. HAJUUSON. 1975. Physiological ecology of Gonyaulax polyedra, a red water dinoflagellate of southern Cali- fornia, p. 11-22. In Toxic dinoflagellate blooms. Proc. Int. Conf. (1st). Mass. Sci. Technol. Found.

HELA, I. 1955, Ecological observations on a locally limited red tide bloom. Bull. Mar. Sci. Gulf Caribb. 5: 269-291.

HOLMES, R. W., P. M. WILLIAMS, AND R. W. EPPLEY. 1967. Red water in La Jolla Bay, 1964-1966. Limnol. Oceanogr. 12: 503- 512.

IIONJO, T. 1974. Studies on the mechanisms of red tide occurrence in Hakata Bay-4. Bull. Tokai Reg. Fish. Res. Lab. 79, p. 77- 121.

II'LUKA, S. 1972. Gymnodinium type-‘65 red tide in occurring anoxic environment of Omura Bay. Bull. Plankton Sot. Jap. 19( 1) : 22-23.

IWASAKT, I-1. 1973. The physiological charac- teristics of neritic red tide flagellates. Bull. Plankton Sot. Jap. 19( 2) : 46-56.

MACLEAN, J. L. 1973. Red tides and paralytic shellfish poisoning in Papua New Guinea. Papua New Guinea Agric. J. 24( 4) : 131- 138.

-. 1975. Red tide in the Morobe Dis- trict of Papua New Guinea. Pac. Sci. 29: 7-13.

MARGALEF, R. 1957. Fitoplancton de las cos- tas de Puerto Rico. Invest. Pesq. 6: 39-52.

-. 1961. Hidrografia y fitoplancton de un area marina de la costa meridional de Puerto Rico. Invest. Pcsq. 18: 33-96.

MARKINA, N. P. 1972. Special features of plankton distribution around the north coasts of Australia during different seasons of 196% 1969 [in Russian]. Pac. Ocean Sci. Res. Inst. Fish. Oceanogr. 81: 57-68.

PRAKASEI, A., J. C. MEDCOF, AND A. D. TENNANT. 1971. Paralytic shellfish poisoning in eastern Canada. Bull. Fish. Res. Bd. Can. 177.

QASIM, S. Z., P. M. BHATTATHIRI, AND V. P. D~ASSY. 1972. The influence of salinity on the rate of photosynthesis and abundance of some tropical phytoplankton. Mar. Biol. 12: 200-206.

QUAYLE, D. B. 1969. Paralytic shellfish poisoning in British Columbia. Bull. Fish. Res. Bd. Can. 168.

ROUNSEFELL, G. A., AND W. R. NELSON. 1966. Red tide research summarized to 1964 including an annotated bibliography. U.S. Fish. Wildl. Serv. Spcc. Sci. Rep. Fish. 535.

SELIGER, I-1. I-I., J. H. CARPENTER, M. LOFTUS, W. H. BIGGLEY, AND W. D. MCELROY. 1971. Bioluminescence and phytoplankton succes- sions in Bahia Fosforescente, Puerto Rico. Limnol. Oceanogr. 16 : 608-622.

- P - AND W. D. MCELROY. lS?O. Medhanisms ‘for the accumulation of high concentrations of dinoflagellates in a bioluminescent bay. Limnol. Oceanogr. 15 : 234-245.

-, M. LOFTUS, AND D.V. SUBBA RAO. 1975. Dinoflagellate accumulations in Chesapeake Bay, p, 181-205. In Toxic dinoflagellate blooms. Proc. Int. Conf. (1st). Mass. Sci. Technol. I’ound.

STEIDINGER, K. A., AND J. WILLIAMS. 1970. Memoirs of the Hourglass cruises. V. 2. Dinoflagellates. Mar. Rcs. Lab. Fla. Dep. Nat. Resour.

SWEENEY, B. 1975. Red tides I have known, p. 225-234. In Toxic dinoflagellate blooms, Proc. Int. Conf. ( 1st). Mass. Sci. Tcchnol. Found.

254 Maclean

TAYLOR, W. R., H. H. SELIGER, W. G. FASTIE, AND W. D. MCELROY. 1966. Biological and physical observations on a phosphorescent bay in Falmouth Harbour, Jamaica, W. I. J. Mar. Res. 24: 28-43.

UYENO, F., AND K. NAGAI. 1973. Seasonal changes of growth promoting effect of mud extracts and seawater collected during various seasons at the Ise Bay on a red tide flagellate E..&erosigma inlandica Hada. Bull. Plankton Sot. Jap. 19( 2) : 39-45.

WALL, D., AND B. DALE. 1969. The “hystricho- sphaerid” resting spore of the dinoflagellate Pyrodinium bahamense, Plate, 1906. J. Phycol. 5: 149-149.

WOOD, E. J. 1954. Dinoflagellates in the Aus-

tralian region. Aust. J, Mar. Freshwater Res. 5: 171351.

-. 1963a,b. Dinoflagellates in the Aus- tralian region. 2. Recent collections. 3. Further collections. Aust. CSIRO Div. Fish. Oceanogr. Tech. Pap. 14 and 17.

WORTH, G. K., J. L. MACLEAN, AND M. J. PRICE. 1975. Paralytic shellfish poisoning in Papua New Guinea. Pac. Sci. 29: l-5.

WYATT, T. 1975. The limitations of physical models for red tides, p. 81-93. In Toxic dinoflagellate blooms. Proc. Int. Conf. (1st). Mass. Sci. Technol. Found.

Submitted: 7 May 1976 Accepted: 14 September 1976

Observations on Pyrodinium bahamense Plate, a toxic dinoflagellate, in Papua New Guinea

Documents

Transcript of Observations on Pyrodinium bahamense Plate, a toxic dinoflagellate, in Papua New Guinea