Enchytraeid oligochaetes as marine pollution indicators

V o l u m e I 1 / N u m b e r 6 / J u n e 1980

birds acted as if oiled, there was no smell of oil on their feathers, nor was there a reported spill or any sign of a slick. In the first case, in Port Moody in February 1977, a leaking rail car containing soybean oil was identified as the source after several days of investigation. Twenty-six birds were recovered, although more were believed to have been affected. TABLE 2 Number of oil spills and number of birds affected at Vancouver Harbour between 1974and 1978"

Petroleum oils Spill size (barrels) Number of spills Birds oiled

< 10 167 -

Spill size (barrels) Number of spills Birds oiled

< 10 1 26 ~-

10-100 9 50

Non-petroleum oils 10-100 2 500

* All but one spill occurred during winter. I- Actual number of birds returned; no estimate of total number affected made at the time, but thought to be less than 50.

In the second case distressed birds began to appear on the night of 23 January 1978 on rocks adjacent to Stanley Park. Initially a petroleum product was suspected, but efforts made to link those birds to recent petroleum spills were unsuccessful. The peculiar odour of the affected birds eventually lead us to suspect a vegetable oil as the agent responsible. A possible source was identified when it was learned that bulk loading facilities had handled a small shipment of rapeseed oil the night of 22 January 1978. Gas chromatography of the affected bird's feathers later confirmed rapeseed oil as the pollutant. On 31 January 1978 the third vegetable oil spill occurred. It was reported by the spiller, the only Vancouver bulk shipper of rapeseed oil. Approximately seven barrels of oil were accidentally released when the wrong valve was opened. Presumably the previous rapeseed oil spill occurred in a similar manner but was undetected because loading occurred at night. What was not obvious initially was how a spill occurring inside the Harbour could explain distressed birds near the tip of Point Grey. Consultations with government hydrographers lead us to conclude, however, that tidal currents could carry light oil or distressed birds that distance within

two or three tide cycles. Thus a small spill could affect a very large number of birds if undetected.

Discussion It is remarkable that an estimated 35 barrels of rapeseed oil could have killed an estimated 500 birds while all petroleum oil spills of the past 5 years have resulted in less than 50 birds oiled (Table 2). Though there is no experimental evidence on this topic it is clear that the birds must react differently to different types of oil. It is possible that they can detect petroleum oil on the water more easily than vegetable oil. To the human observer, rapeseed oil is much less detectable than any petroleum oil, and in particular lacks eye-catching irridescence. Also, petroleum oils have a strong, often irritating odour, which is lacking in vegetable oils. Although the olfactory senses of birds are not well studied and may vary among taxa it is possible that the strong smell of petroleum oil may repel aquatic birds. A further possibility, though somewhat speculative, is that rapeseed oil might be more readily damaging than petroleum oils to the waterproofing ability of bird feathers. The point we wish to make is that of the potential danger to wildlife of vegetable oil spills. Although spills of fish oil have been recorded (Newman & Pollock, 1973; Anonymous, 1974) vegetable spills appear not to have occurred, or to have gone unnoticed. Sites of vegetable oil trans-shipments require consideration in oil spill contingency planning. Shippers may not be aware of the potential lethality of such oils since they are for the most part edible. Spill investigators may not look to them as pollution sources, since they do not act like petroleum oils when spilled, and tend at least in our experience to dissipate rapidly. However, even a small spill of vegetable oil can be far more damaging to acquatic birds than certain petroleum otis.

A n o n y m o u s (Percy F i t z p a t r i c k Inst.). (1974). Fish oil kills seabirds. A f r i c a n Wildl., 28 (4), 2 4 - 2 5 .

Campbell, R. W., Shepard, M. G., MacDonald, B. A. & Weber, W. C. (1974). VancouverBirds in 1972. VancouverNatural History Society, Vancouver. Newman, G. G. & Pollock, D. E. (1973). Organic pollution of marine environment by pelagic fish factoriesin the western Cape. S. Afr. J. Sci., 68 (1), 27-29.

.WarinePollution Bulletin, Vol. I I, pp. 171-174 ~Pergarnon Press Ltd. 1980.Prinled in Great Britain.

(X)25-326X/gO/0601-OI71 $02/)0/0

Enchytraeid Oiigochaetes as Marine Pollution Indicators KATHRYN COATES and DEREK V. ELLIS Biology Department, University o f Victoria, Victoria, British Columbia, Canada V8 W 2 Y2 Fifteen species of enchytraeid oligochaetes have been collected from a pulp mill waste receiving area. Of these, one species Lumbricillus lineatus which is a known stressresistant intertidal form is predominant within 1.5 km of the mill outfall. Beyond that distance the species is replaced by a

variable association of 14 other species from the genera Lumbricillus, Marionina and Enchytraeus. L. lineatus is c o m m o n in Europe and eastern North America in upper intertidal drift habitats, but on the Pacific Coast is not indigenous. In British Columbia it has only been collected

171

Marine Pollution Bulletin

adjacent to three pulp mills, not at five other such mill% nor at ten undisturbed intertidal stations at each of which a diverse association of Enchytraeid species occurs. L. lineatus can serve as an index of the impact of pulp mill effluent at the site investigated. The most practical index is percentage of total adult enchytraeids represented by L. lineatus.

Not shown in the tables are records of immatures, which were often abundant but usually impossible to identify; 1150 core- 1of immature Lumbricillus were collected near the outfall on occasions. Very few of these (1-3 core-~), could be provisionally identified as species other than L. lineatus, which is in agreement with the distributional pattern of the mature forms.

Enchytraeid oligochaetes have been suggested as indicators of pulp mill pollution in the littoral zone (Levings et al., 1975). We have investigated this possibility by a series of surveys over four years, 1976-79, initiated to resolve the taxonomy of these forms in British Columbia (Coates, 1979). From 1978 Rayonler Canada (B.C.) Ltd. has supported a detailed investigation at the Port Alice pulp mill (Fig. 1) to develop measures for monitoring ecosystem recovery following application of pollution control procedures (Ellis etal., 1978).

Discussion

Methods Samples in 1978 and 1979, after a preliminary nonquantitative survey in 1976, consisted of 3-10 hand-driven cores (inner diameter 50 mm, penetration 60 mm) per station. These were taken during five surveys from finegrained but often poorly-sorted muds near high-tide. It was often necessary to remove stones to permit coring, and randomization was not possible. Samples were stored in plastic bags in ice, and subsequently in a refrigerator until specimens could be separated from the sediment. Initially specimens were prepared for identification under light microscopy by staining with Grenacher's alcoholic borax carmine. Concurrently a taxonomic study which developed an identification key was in progress, and eventually this led to identifications from live specimens. The taxonomic study involved the description and naming of several new species, about which material is now being prepared for publication. Coincident collections and records of shoreline algae, invertebrates and their spatial patterns around the discharge were made and will be detailed separately. Environmental records were made available from routine surveys by the mill' s environmental staff. Results Preliminary analyses of 3-10 cores from each station gave very high variance estimates for species abundances, and there was accordingly high variability between surveys at each station. Distributional data is therefore summarized by the number of surveys in which each species is present at each station (Table 1). A single link cluster analysis using Jaccard's Coefficient of Community, and simultaneous grouping by station and by species using manual ZttrichMontpellier methods revealed only one consistent distributional pattern between surveys. Lumbricillus lineatus persisted as the predominant species (1-100 core-l), in a block of stations within 1.5 km of the outfall, i.e. Stations S6A, S6B, $7, $8 1, and Cayuse. The pattern is shown in Table 1 but is clearest when expressed as the percentage adult L. lineatus represents of total adult enchytraeids per station (Table 2). The species with the most similar distribution, Marionina n. sp. 1, also recurs at stations near the outfall but not in such high numbers, (1-3 core- ~), and occurred frequently further from the outfall. 172

Stations S6A and S6B are in the area immediately adjacent to the mill (within 0.5 km of the outfall). The shoreline ecosystem is reduced to dark slime growths of the f'flamentous algae Ulothrix and Oscillatoria. Three tubificid oligochaetes (Monophylephorus n. sp., M. rubroniveus and M. Pacificus) also occur under stones with the enchytraeids. Between 0.5 and 1-2 km distant a less reduced shoreline ecosystem is present dominated by a broad zone of the green filamentous alga Enteromorpha intestinalis above mid-tide. Beyond 1-2 km the rockweed Fucus distichus and other algae appear in the littoral, although initially the Fucus epifauna contains a reduced amphipod species association (Ellis et al., 1978). Environmental records show low oxygen levels in surface waters near the mill (means 1.0, 1.7 and 3.3 mg 1_ 1 in 1969, 1973-77, and 1978, respectively). The increasing oxygen levels with time coincide with the application of a series of pollution controls from 1973. The spatial distribution of L. lineatus close to the mill corresponds with oxygen levels reduced well below saturation, and visible but fluctuating levels of mill effluent. Thus the species has the potential at this site to index the area showing substantial impact of the discharge on the shoreline ecosystem. The percentage data in Table 2 suggests that since 1978 L. lineatus has been constrained closer to the mill than it was in 1976. This suggestion is now being tested by an expanded sampling programme to determine whether the documented population change from predominant L. lineatus to a diverse association of enchytraeid species shifts progressively closer to the mill as the pollution controls improve the quality of the discharge. L. lineatus is a widely spread species of high-tide drift habitats in Europe and the Atlantic coast of North America (Lasserre, 1971). It is an opportunistic species, with an interesting biology, including occurrence of parthenogenetic polyploid forms (Christensen et al., 1978) and resistance to hydrocarbon contamination (Giere & Hauschildt, 1979). During our surveys in British Columbia, ranging over 800 km of coast from Victoria to Prince Rupert (Fig. 1), L. lineatus was only collected near three pulp mills, but not at five others, and not at any of the ten undisturbed stations from which specimens have been identified and which have a diverse array of species (Coates, 1979). L. lineatus appears to not have been found elsewhere in Pacific North America, and it can be concluded that it is not indigenous to the coast but has been introduced at these mills by international ship traffic. The identification system now developed permits utilization of the species in the Pacific region as a pollutant indicator. At Port Alice the surveys will continue, to determine whether the introduced species will maintain its dominance in the effluent regime, or whether progressive recovery of the shoreline will increasingly restrain the

Volume I 1/Number 6/June 1980

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173

,

Marine Pollution Bulletin TABLE 1

Number of occasions on which Enchytraeid species were present at various stations during five surveys, 1978-79. Cayeghle

0

Lumbricillus lineatus (M~iller, 1774) Lumbricillus qualicumensis (Tynen, 1969)

1

1

Lumbricillus tuba (Stephenson, 1911)

1

1

Stations Cay$8 use IA

1

S6A

S6B

$7

1

4

2

1

1

2

1

2

1

1

3

1

2

2

2

1

U1

1

Lumbricillus helgolandicus (Michaelsen, 1927) (aff. Nielsen & Christensen, 1959)

1

1

1

3

1 2

4

5

1

1

Quatsino

1

3

1

Lumbricillus annulatus (Eisen, 1904) Lumbricillus pagenstecheri (Ratzel, 1869)

U2

1

2

2

3

1

1

1

1

1

Lumbricillus n. sp. 1 Lumbricillus n. sp. 2

1

1

Lumbricillus n. sp. 3

1

Marionina sjaelandica (Nielsen & Christensen, 1961)

1

1

Marionina appendiculata (Nielsen & Christensen, 1959)

3

2

1

1

I

1

3

3

1

3

1

Marionina n. sp. 1

1

Marionina n. sp. 2 Enchytraeus kincaidi (Eisen, 1904)

1

1

1

3

1

1 1

1

1

2

1

1

1

1

1

1

1

2

Enchytraeus multiannulatus (Altman, 1936)

1

1

1

TABLE 2 Lumbricillus lineatus as a percentage of total enchytraeids sampled. Blanks indicate no sample. Station

Distance from out fall (km)

Compass direction

4.5 3.5

S S

0.7

S

0 0.2 0.4 0.6 1.4 5.2 7.6 l0 14 19 20

N N N N N N N N N N

Cayeghle 0 l

S6A S6B $7 $8 Cayuse Ul U2 3 4 5 Quatsino

June 1976

May 1978

June 1978

April 1979

July 1979

0 0 42

86 22 0

97 73 0 11 Immatures 4 2 0 50*

99 90

97 93

75 Immatures

0

0 0 0 0

0 4

0 0 0 0

0

*One specimen only.

s p e c i e s ' a b u n d a n c e u n t i l it d i s a p p e a r s as t h e n o r m a l d i v e r s e a r r a y o f species r e t u r n s . T h e t u b i f i c i d o l i g o c h a e t e M o n o p y l e p h o r u s irroratus m e n t i o n e d as a s s o c i a t e d w i t h L . lineatus is a n e w species a n d will b e d e s c r i b e d e l s e w h e r e ( B r i n k h u r s t & B a k e r , personal communication).

Christensen, B., Jelnes, O. & Beng, U. (1978). Long-term isozyme variation in parthogenetic polyploid forms of Lumbricillus lineatus (Enchytraeidae, Oligochaeta) in recently established environments. Hereditas, 88, 65-73. Coates, K. (1979). Revision of the taxonomy of intertidal enchytraeidae t n,nnelida, Oligochaeta) of British Columbia with a preliminary dis-

174

cussion regarding use of intertidal species associations to assess pollutant impacts. University of Victoria, MSc. thesis, 394 pp. Ellis, D. V., Cross, S. F., Coates, K. & McKinnell, S. (1978). Assessment of shoreline rehabilitation at the Port Alice pulp mill. Vol. 4. In Environmental Improvement at Neroutsos Inlet, B.C. Rayonier Canada, 92 pp. Giere, O. & Hauschildt, D. (1979). Experimental studies on the life cycle and production of the littoral Oligochaete Lumbricillus lineatus and its response to oil pollution. In Cyclic Phenomena in Marine Plants and Animals. Edited by Nayler, E. and Hartnall, R. G. Pergamon Press, Oxford. Laserre, P. (1971). The marine enchytraeidae (Annelida, Oligochaeta) of the eastern coast of North America with notes on geographical distribution and habitat. Biol. Bull., 140,440--460. Levings, C. D., Pomeroy, W. M. & Prange, R. (1975). Sampling locations for intertidal biota and preliminary observations of habitats at some British Columbia estuaries. Fish. Res. Bd Can. Ms. Rep. Ser. 1345, 20pp.