Effects of domestic and industrial pollution on distribution and abundance of aquatic oligochaetes in the Forth estuary

Helgoland Marine Research, Mar 1980

The Forth estuary is a major estuary on the east coast of Scotland; it receives effluent from domestic and industrial (petro-chemical and distilling) sources. Following a study on the distribution of the macrofauna of the intertidal areas in relation to pollution (McLusky et al., 1978), this paper is concerned with the distribution and abundance of aquatic oligochaetes and the small polychaeteManayunkia aestuarina in relation to estuarine salinity, organic enrichment, and industrial effluent. In the most polluted parts of the estuary oligochaetes are the sole inhabitants of the mudflats; in other less polluted flats they are very abundant. In the least polluted parts the numbers of oligochaetes diminish as the numbers and diversity of macrofauna increase. Estimates of the production of oligochaetes are given.

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Effects of domestic and industrial pollution on distribution and abundance of aquatic oligochaetes in the Forth estuary

HELGOL.~,IDER MEERESUNTERSUCHUNGEN Helgol~nder Meeresunters. 0 Department of Biology, University of Stirling; Stirling , FK9 4LA, Scotland 1 Effects of d o m e s t i c a n d i n d u s t r i a l p o l l u t i o n o n d i s t r i b u t i o n a n d a b u n d a n c e of a q u a t i c o l i g o c h a e t e s i n t h e F o r t h e s t u a r y The Forth estuary is a major estuary on the east coast of Scotland; it receives effluent from domestic and industrial (petro-chemical and distilling) sources. Following a study on the distribution of the macrofauna of the intertidal areas in relation to pollution (McLusky et. al., 1978), this paper is concerned with the distribution and abundance of aquatic oligochaetes and the small polychaete Manayunkia aestuarina in relation to estuarine salinity, organic enrichment, and industrial effluent. In the most polluted paris of the estuary oligochaetes are the sole inhabitants of the mudflats; in other less polluted flats they are very abundant. In the least polluted parts the numbers of oligochaetes diminish as the numbers and diversity of macrofauna increase. Estimates of the production of oligochaetes are given. - INTRODUCTION The i n v e s t i g a t i o n has b e e n c o n d u c t e d i n two parts. Firstly a study was m a d e i n 1977 of the oligochaetes i n the intertidal areas of the Forth estuary b e t w e e n Stifling a n d K i n c a r d i n e Bridge, a n d secondly a study of the oligochaetes a n d small polychaetes was m a d e i n 1979 i n the l a r g e r i n t e r t i d a l area b e t w e e n K i n c a r d i n e Bridge a n d Bo'ness (Fig. 1). For the former study 8 stations were s a m p l e d in J u n e , July, S e p t e m b e r a n d N o v e m b e r 1977; on each occasion, two 5-cm3 cores were collected. Each s a m p l e was p a s s e d Fig. i. Estuaryof the Pirthof Forth, Scotland,showingplace namesmentionedin the text t h r o u g h a 0.25-mm sieve, a n d p r e s e r v e d i n 4 % f o r m a l d e h y d e solution. The sieved samples were e x a m i n e d u n d e r the microscope, a n d all a n i m a l s p r e s e n t r e m o v e d a n d identified; a r a n d o m s a m p l e was m e a s u r e d a n d w e i g h e d on a B e c k m a n m i c r o b a l a n c e after h a v i n g b e e n dried at 60 ~ The interstitial salinity (expressed as %0 NaC1) was d e t e r m i n e d for each station at each sampling. For the s e c o n d part of the study, 28 stations at Culross, Torry Bay, K i n n e i l a n d Skinflats w e r e s a m p l e d d u r i n g March 1979. At each station three s a m p l e s w e r e collected with a core t u b e of 8 cm 2, to a d e p t h of 5 cm, a n d p l a c e d directly into 4 % f o r m a l d e h y d e solution, m a d e u p with sea water. For 5 stations at K i n n e i l a piston corer of 11 cm2 was used. S a m p l e s w e r e p a s s e d t h r o u g h a 0.125-mm sieve to r e m o v e fine particles a n d the s e d i m e n t r e t a i n e d was w a s h e d into beakers. Ludox TM (Du Pont) d i l u t e d to a SG of 1.10 with w a t e r was added, a n d after a l l o w i n g the s e d i m e n t to settle the s u p e r n a t a n t l i q u i d was d e c a n t e d t h r o u g h a 0.125-mm m e s h sieve to collect the animals. The d e c a n t a t i o n was r e p e a t e d two more times a n d the extraction efficiency was found to be over 96 %. Worms from one s a m p l e at each station w e r e identified, counted, dried to constant w e i g h t for 48 h at 60 ~ a n d w e i g h e d on a Mettler HL 52 b a l a n c e . Worms that could not be i d e n t i f i e d to species u s i n g a b i n o c u l a r microscope w e r e w e i g h e d together as a n "other sp." category. A n i m a l s i n this category from a n o t h e r s a m p l e were p l a c e d i n A m m a n s l a c t o p h e n o l on microscope slides prior to identification u s i n g a c o m p o u n d microscope. T h e ratio of each species i d e n t i f i e d from the "other sp." category was t h e n u s e d to c o m p u t e the n u m b e r s a n d w e i g h t of each species at that station. The n u m b e r s a n d b i o m a s s per m 2 of each species at each station w e r e c o m p u t e d a n d the m e a n n u m b e r a n d b i o m a s s per m 2 calculated b y d i v i d i n g the total for e a c h species b y the n u m b e r of stations sampled. D . S . M c L u s k y , M. T e a r e & P. P h i z a c k l e a F o r t h estuary. T h e u p p e r p a r t of t h e e s t u a r y (0-16 km, S t i r l i n g - C a m b u s ) is p r e d o m i n a n t l y f r e s h - w a t e r , w i t h t h e i n t e r s t i t i a l s a l i n i t y r a n g i n g f r o m 0.2 %o NaC1 at S t i f l i n g to a m a x i m u m of 4 . 1 % 0 at C a m b u s . In this part of t h e e s t u a r y t h e sole i n t e r t i d a l i n h a b i t a n t s w e r e t h e o l i g o c h a e t e s T u b i f e x tubifex a n d Limnodri]us hoffmeisteri. L a r g e n u m b e r s a n d b i o m a s s e s of t h e s e t w o s p e c i e s w e r e r e c o r d e d w i t h a m a x i m u m at t h e 10-kin s t a t i o n w h e r e t h e m e a n n u m b e r s w e r e 127,400 m -2 for T. tubifex a n d 105,800 m -2 for L. hoffmeisteri, a n d t h e m e a n b i o m a s s e s w e r e 57.663 a n d 22.154 g dry w t m -2 r e s p e c t i v e l y . B e t w e e n 16 a n d 18 k m T. tubifex a n d L hoffmeisteri w e r e r e p l a c e d b y T. costatus a n d Peloscolex benedeni. T h e i n t e r s t i t i a l s a l i n i t y in this a r e a r a n g e s f r o m 1.6 900 to a KILOMETRES FROM STIRLING Pig. 2. Distribution o'f the oligochaetes Tubifex ~bifex, Limnodrilus hoffmeisteri, Tubifex costatus, Peloscolex benedeni, Tubifex pseudogaster and the polychaetes Capitella capitata and Manayunkia aestuarina in relation to distance down the Porth estuary, measured as kilometres below Stirling, which is the upper tidal limit. Abundance is presented as mean number m -2, The maximum and minimum interstitial salinity at stations along the estuary is also presented Table 1. M e a n n u m b e r s a n d biomass of oligochaete species recorded from the intertidal estuarine Firth of Forth b e t w e e n Stifling and Kincardine Bridge in 1977 (8 stations, 0-28 k m from Stifling) *Subsequent to the preparation of this paper, certain changes in the nomenclature of the oligochaetes u n d e r discussion have occurred (Brinkhurst & Baker, 1979). Accordingly, Tubifex pseudogaster is now Tubificoides pseudogaster (Dahl, 1969), and Peloscolex benedeni is now Tubificoides benedeni (Udekem, 1855) m a x i m u m of 7.7 %o. 7". c o s t a t u s w a s t h e d o m i n a n t o l i g o c h a e t e f r o m 18 k m ( C a m b u s ) to 30 k m , w i t h a m a x i m u m m e a n a b u n d a n c e of 4 4 4 , 9 3 3 m -2 at 18 k m , r e p r e s e n t i n g a m e a n b i o m a s s of 78.044 g d r y w t m -2. d o m i n a n t , a n d P. b e n e d e n i h e r e o n l y r e a c h e d a m e a n a b u n d a n c e of 2 6 7 9 m -2. B e l o w K i n c a r d i n e B r i d g e (28 kin) T. costatus n u m b e r s d i m i n i s h e d u n t i l it w a s n o l o n g e r p r e s e n t b e l o w 30 k m , w h i l s t P. b e n e d e n i n u m b e r s i n c r e a s e d to a m e a n a b u n d a n c e of 19,894 m -2 r e p r e s e n t i n g 3.629 g dry wt m -2. The most a b u n d a n t P. benedeni p o p u l a t i o n s were at 36 k m from Stirling with 100,000 m -2 r e p r e s e n t i n g 13.0 g dry wt m -2. The second most a b u n d a n t oligochaete b e l o w K i n c a r d i n e Bridge was Amphichaeta sannio with a m e a n a b u n d a n c e of 45?0 m -2. These a n i m a l s w e r e h o w e v e r very small a n d this n u m b e r only r e p r e s e n t s 0.029 g dry wt m -2. The second most i m p o r t a n t oligochaete i n this area i n terms of biomass was the l a r g e r Tubifex pseudogaster at 0.109 g dry wt m -2. Other oligochaetes (Paranais litoralis, Lumbricillus lineatus a n d Enchytraid sp.) were all less t h a n 0.03 g dry wt m -2. No small p o l y c h a e t e s w e r e recorded b e t w e e n Stirling a n d K i n c a r d i n e Bridge {0-28 km}~ h o w e v e r b e l o w K i n c a r d i n e Bridge large n u m b e r s of Manayunkia aestuarina occurred with a m a x i m u m of 281,254 m -2 at 33 km, r e p r e s e n t i n g a biomass of 6.274 g dry wt m -2. Capitefla capitata was p r e s e n t at the K i n n e i l area (33-37 km) with a m a x i m u m of 3809 m -2 at 33 km, r e p r e s e n t i n g 0.287 g dry wt m -2. Cirratulus cirratus was restricted to the Culross/Torry Bay area, a n d t~giospio elegans was t h i n l y scattered t h r o u g h o u t the area. The full data from i n d i v i d u a l s a m p l i n g stations are t a b u l a t e d i n Phizacklea (1978) a n d Teare (1979). The Forth estuary can b e c o n v e n i e n t l y d i v i d e d into two areas, a narrow u p p e r estuary from Stifling to K i n c a r d i n e Bridge (0-28 k m from Stifling) w h e r e the interstitial salinity r a n g e s from 0 to 26 %0, a n d a b r o a d lower estuary from K i n c a r d i n e Bridge to the sea w h e r e the interstitial salinity is greater t h a n 26 %0 (Fig. 1). The s a m p l i n g p r o g r a m m e a n d the results reflect this difference. In the first 16 k m the estuary, a l t h o u g h tidal, is d o m i n a t e d b y fresh-water conditions. Over the first 10 k m the interstitial s a l i n i t y is always less t h a n 1%o, at 10 k m it is b e t w e e n 1.0 a n d 1.9 %0, a n d at 16 k m it is b e t w e e n 1.6 a n d 4.1%o. The i n t e r t i d a l f a u n a was f o u n d to be exclusively the fresh-water oligochaetes T. tubifex a n d L. hoffmeisteri. Stczynska-Jurewicz (1972) found that the m a x i m u m salinity at w h i c h T. tubifex could survive was 9 %0 a n d the m a x i m u m at which n a t u r a l egg l a y i n g a n d d e v e l o p m e n t occurred was 4 %0. K e n n e d y (1965) stated that salinity controlled the d i s t r i b u t i o n of L. hoffmeisteri, b u t did not give precise limits. In the p r e s e n t study T. tubifex was found in localities with a m a x i m u m salinity of 4.1%0, a n d L. hoffmeisteri has occurred at salinities of up to 7.7 %0, c o n f i r m i n g the limits n o t e d above. This stretch of the Forth is subject to organic pollution, a n d it m a y be n o t e d that m a x i m u m n u m b e r s a n d biomass occurred at the 10-km station w h i c h is d o w n s t r e a m of the discharge from Stifling s e w a g e works. Brinkhurst (1965) n o t e d that i n fresh-water e n v i r o m e n t s these two species were the last species to r e m a i n w h e n p o l l u t i o n b e c a m e severe, a n d Eyres et al. (1978) n o t e d that these 2 species r e a c h e d their greatest n u m b e r s i n the o r g a n i c a l l y p o l l u t e d stretches of the River Irwell. B e t w e e n 16 a n d 28 k m the interstitial salinity increases progressively from a m e a n of 3.2 %0 to a m e a n of 26.4 %o. Over this stretch of the estuary the d o m i n a n t oligochaete was T. costatus. M a x i m u m biomass a n d n u m b e r s were reported at 18 k m from Stifling w h i c h is a n area which receives large v o l u m e s of effluent from w h i s k y distilling i n d u s t r i e s as w e l l as domestic effluent. This area e x p e r i e n c e s m a r k e d o x y g e n d e p l e t i o n (Stout, 1976; Forth River Purification Board, 1978), w h i c h results i n a n a b s e n c e of all f a u n a except Domestic and industrial pollution oligochaetes. It is evident however that T. costatus was thriving in this environment. Twenty-one km from Stifling other macrobenthic animals occurred in the mudflats, e s p e c i a l l y Nereis diversicolor and Corophium volutator {McLusky et al., 1978). From the data on salinity it might have b e e n expected that these two species could have lived as far upstream as 16 km; however the organic pollution and oxygen depletion in the 16-21 km region of the estuary has excluded these macrobenthic animals, whilst permitting T. costatus to thrive. Peloscolex benedeni was present in the Forth estuary from 18 km from Stirling onwards. Numbers r e m a i n e d low, however, until b e y o n d Kincardine Bridge (29 km), as in the 18-29 km section it was overshadowed by T. costatus. The estuarine succession of T. tubifex and L. hoffmeisteri, then T. costatus, then P. benedeni, was also found by Hunter and Arthur (1978) in the Thames estuary. In the lower part of the estuary (29 km from Stirling onwards) P. benedeni b e c a m e the dominant oligochaete in the estuary, and together with the polychaete Manayunkia aestuarina accounted for 92 % of the biomass of small worms in the large intertidal mudflats which characterise this part of the estuary {Fig. 1). The mudflats of this area {30-38 km} comprise 65 % of the total intertidal area of the Forth estuary, and are recognised as the main b i r d f e e d i n g areas in the estuary (McLusky et al. 1976}. P. benedeni was w i d e l y s p r e a d in this area, b e i n g present at 25 out of 28 stations sampled. The only stations from which it was absent were 2 stations situated within % km of the effluent from the G r a n g e m o u t h petro-chemical complex, and 1 station on the sandy part of Torry Bay. The absence of P. benedeni from sandy sediments is in a g r e e m e n t with the observations of Wharfe (1975) at the Isle of Grain. Lepp~koski (1975) noted in Saltkalle Fjord that P. benedeni could only tolerate slight pollution, but e x p a n d e d both in area and quantitatively with an increasing d e g r e e of pollution. In the present study its absence from the most polluted parts of the Kinneil mudflats, coupled with its abundance in the less polluted areas would confirm this observation. Pearson & Rosenberg (1978) have r e v i e w e d benthic succession in relation to organic enrichment, and point to P. benedem" as b e i n g the most conspicuous oligochaete in the polluted parts of the Gothenburg estuary. They also list many records of P. benedeni b e i n g a b u n d a n t in polluted localities, especially on the e d g e of abiotic zones. This part of the Forth estuary is polluted by petro-chemical industries, s e w a g e discharge, and discharge from the polluted Rivers Carton and Avon. The w i d e s p r e a d distribution and a b u n d a n c e of P. benedeni in all except abiotic environments emphasises the impact of pollution in this part of the Forth estuary. The small size of Amphichaeta sannio r e d u c e d its importance in biomass terms and p r o b a b l y helps to e x p l a i n the paucity of records for this species. It has b e e n recorded from Danish fjords and estuaries (Dahl, 1960~ Muus, 1967), and the Baltic (Laasko, 1969) but this appears to be the first British record. Paranais 1itoralls is another common estuarine oligochaete but has quite a patchy distribution on the Forth and was never recorded in very large numbers. The most important polychaete in the Forth was the common estuarine species Manayukia aestuarina which - with a wide distribution and high biomass - was second in importance to P. beneden/. This species was first observed in the Forth in J a n u a r y 1979 (observed by authors) and it was not certain whether it h a d previously b e e n overlooked or was a g e n u i n e new species. In view of the w i d e distribution and large n u m b e r s it appears more likely that the s a m p l i n g methods u s e d previously h a d not collected this fairly small a n i m a l . M. aestuarlna r e a c h e d m a x i m u m n u m b e r s at 33 k m from Stifling close to a domestic s e w a g e outfall b u t it is i n t e r e s t i n g that the n u m b e r s w e r e lower a n d the a n i m a l dry w e i g h t significantly lower on Skinflats (29-30 km) t h a n K i n n e i l (32-36 km). The r e a s o n for this is not k n o w n b u t could p r e s u m a b l y be a n effect of r e d u c e d salinity, poorer food s u p p l y due to less organic e n r i c h m e n t , more c o m p e t i t i o n for food or h i g h e r p r e d a t i o n on Skinflats. The deposit feeder Capitella capitata w h i c h was the s e c o n d most i m p o r t a n t p o l y c h a e t e species a n d third most i m p o r t a n t a n n e l i d i n terms of b i o m a s s on the lower Forth estuary was m a i n l y c o n f i n e d to Kinneil. It is possible that the p r e s e n c e of C. capitata on K i n n e i l reflected a large organic load to this area as the a n i m a l is reported to flourish i n areas w i t h a h i g h organic i n p u t (Reish, 1957; Reish 8, Barnard, 1960}. H o w e v e r M u u s (1967} did not find the a n i m a l s particularly associated with p o l l u t e d localities. In this survey C. capitata was always associated w i t h other species: u s u a l l y h i g h densities of M. aestuarina a n d P. benedenl. Pygospio elegans occurred sporadically, b u t g e n e r a l l y closer to the low-water m a r k on Torry Bay w h e r e water flow is faster. M u u s (1967) observed that this species was not found i n areas w h e r e water m o v e m e n t was slow. O n e i m p o r t a n t feature of the study was the complete a b s e n c e of a n y a n n e l i d s from stations close to the outfall from the p e t r o - c h e m i c a l complex at G r a n g e m o u t h . The only a n i m a l s o b s e r v e d i n these samples w e r e occasional n e m a t o d e s a n d a few s p e c i m e n s of a harpacticoid Platychellpus sp. This abiotic zone has b e e n reported i n previous surveys of the r e g i o n (McLusky et al., 1976, 1978). The a n n e l i d f a u n a s a m p l e d i n this study comprised a m e a n biomass of 27.97 g dry wt m -2 for the Stirling to K i n c a r d i n e Bridge area, a n d 6.30 g dry wt m -2 for the area b e l o w K i n c a r d i n e Bridge. In the former area oligochaetes are often the sole fauna, b u t i n the latter area they share the mudflats w i t h other macrofauna, l~lliott (1979) has recorded the m e a n m a c r o f a u n a l biomass of 15.0 g flesh dry wt m -2 (excluding O l i g o c h a e t a a n d Mytilus) from Torry Bay. H a k a et al. (1974) a n d Giere (1975) have c a l c u l a t e d P:B ratios of 3:1 for oligochaetes a n d W a r w i c k et al. (1979) a s s u m e d that m e i o f a u n a l polychaetes h a v e the same P:B as a short lived m a c r o f a u n a l polychaete, Ampharete acutifrons, i. e. 5.5:1. U s i n g these P:B ratios the p r o d u c t i o n of oligochaetes on the u p p e r Forth estuary w o u l d b e 83.91 g dry wt m -2 yr-1, a n d on the lower Forth estuary w o u l d be 11.59 g dry wt m -2 yr-1 for oligochaetes a n d 13.40 g dry wt m -2 yr-1 for small polychaetes. The total p r o d u c t i o n of small worms on the lower Forth estuary of 25 g dry wt m -2 compares with the p r o d u c t i o n of i n f a u n a l m a c r o f a u n a (principally molluscs) for this area c a l c u l a t e d b y Elliott (1979) as 20.6 g flesh dry wt m -2 yr-~. The e s t i m a t e d total i n f a u n a l p r o d u c t i o n of 45.6 g flesh dry wt m -2 for the Forth estuary compares closely w i t h Wolff & de Wolf's {1977) estimate of 39.8 - 3 2 . 7 g for the G r e v e l i n g e n estuary. Oligochaetes h a v e b e e n s e e n to be most a b u n d a n t i n the Forth i n areas of organic e n r i c h m e n t (except abiotic zones), a n d the above m e a n estimates w o u l d be greater i n areas of pollution, a n d less i n less p o l l u t e d zones. A l t h o u g h there m a y be i m p o r t a n t s e a s o n a l fluctuations i n b i o m a s s w h i c h w i l l alter the p r o d u c t i o n estimates these calculations do suggest that o l i g o c h a e t e s a n d small polychaetes will b e at least as i m p o r t a n t e n e r g e t i c a l l y as the m a c r o f a u n a of these mudflats. To study this i n greater detail a m o n t h l y s a m p l i n g p r o g r a m m e has b e e n e s t a b l i s h e d at selected stations to e x a m i n e t e m p o r a l c h a n g e s i n n u m b e r s a n d biomass of the a n n e l i d f a u n a a n d to use more precise m e t h o d s to e s t i m a t e t h e p r o d u c t i o n of t h i s i m p o r t a n t p o r t i o n of t h e i n t e r t i d a l e s t u a r i n e f a u n a , a n d t h e i m p a c t of p o l l u t i o n u p o n it. Acknowledgements. This work was supported in part by the Natural Environment Research Council. It is a pleasure to t h a n k A. H e n d e r s o n for assistance with oligochaete identification, and K. McKeown for help with sample collection. L I T E R A T U R E C I T E D Brinkhurst , R. O. , 1965 . Observations on the recovery of a British river from gross organic pollution . - Hydrobiologia 25 , 9 - 51 . Brinkhurst , R. O. & Baker , H. R. , 1979 . 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D. S. McLusky, M. Teare, P. Phizacklea. Effects of domestic and industrial pollution on distribution and abundance of aquatic oligochaetes in the Forth estuary, Helgoland Marine Research, 1980, 384-392, DOI: 10.1007/BF02414763