J. mar. biol. Ass. U.K. (1985), 65, 951-968 951 Printed in Great Britain

ABUNDANCE, LIFE HISTORY AND LIGULOSIS IN THE GOBIES (TELEOSTEI) OF THE INNER SEVERN ESTUARY

P. N. CLARIDGE*, M. W. HARDISTY, I. C. POTTER AND C. V. WILLIAMS School of Biological Sciences, University of Bath, Claverton Down, Bath BA2 7AY

(Figs. 1-7)

Eight of the were recorded in weekly samples taken between July 1972 and June 1977 from the intake screens of Oldbury Power Station in the inner Severn Estuary. Buenia jeffreysii, Aphia minuta, Gobius paganellus and Gobius niger occurred infrequently and Crystallogobius linearis was only common in the late spring and summer of 1975 and 1976. microps, which peaked in numbers in the winter, increased in abundance each year between 1972 and 1977. The most numerous gobies were those belonging to the Pomatoschistus minutus complex which were separated into P. minutus and P. lozanoi only between June 1974 and July 1975. Seasonal trends in the abundance of these two species were similar, with elevated numbers occurring between July and September 1974 and in January 1975. Gonadosomatic indices and other data indicate that the decline in numbers after the latter month represented an emigration to spawning areas further down the estuary or in the Bristol Channel. Although P. minutus attained a larger body size than P. lozanoi, both these species and P. microps typically had a one year life cycle with only a small number of individuals surviving for a further few months. The fecundity of P. lozanoi, which ranged from 410-2453 (mean 1270), was lower than that reported for P. minutus in this and other studies. Analysis of stomach contents showed that the diet of both species was similar, consisting predominantly of gammarids and mysids. While both species were infected with Ligula intestinalis, the incidence of infection and the parasite index was greater in P. lozanoi than in P. minutus. There is evidence that ligulosis affected growth and may have led to an increased rate of mortality.

INTRODUCTION While the Gobiidae is a particularly successful teleost family in both tropical and temperate seas, it is also well represented in estuarine and fresh water environ- ments (Nelson, 1976; Wheeler, 1978). The most abundant species of gobies in the Mediterranean and on the Atlantic coast of north-west Europe are those belonging to the Pomatoschistus (Miller, 1973; Webb, 1980). The Poma- toschistus minutus complex contains three morphologically very similar species {Pomatoschistus minutus (Pallas), Pomatoschistus lozanoi (De Buen) and Pomato- schistus norvegicus (Collett)) whose validity has been the subject of some discussion (see Webb, 1980). However, unlike Swedmark (1968) who, for example, did not regard P. lozanoi as worthy even of subspecific status, the studies of more recent workers employing a combination of morphological, karyological and biochemical criteria have supported the validity of all three species (Fonds, 1973; Webb & * Present address: N.E.R.C. Institute for Marine Environmental Research, Prospect Place, The Hoe, Plymouth PLi 3DH. 952 P. N. CLARIDGE AND OTHERS Miller, 1975; Webb, 1980; Wallis & Beardmore, 1980,1984). Nevertheless, viable larvae can be produced by laboratory hybridisation of P. minutus and P. lozanoi (Fonds, 1973) and individuals have been found with morphological and bio- chemical characters intermediate between those of P. minutus and P. lozanoi or P. lozanoi and P. norvegicus (Swedmark, 1968; Fonds, 1973; Webb & Miller, 1975; Webb, 1980; Wallis & Beardmore, 1980). Although much information has been collected on the life cycle offish described as P. minutus (see e.g. Swedmark, 1958; Healey, 1971 a, b; Fonds, 1973; Hesthagen, 1971,1975,1977), it is possible that, in the period prior to the publication of the studies of Fonds (1973) and the detailed taxonomic work of Webb (1980), some populations assigned to P. minutus may sometimes also have contained P. lozanoi. Extensive sampling of the material collected from the intake screens of power stations in the Severn Estuary and inner Bristol Channel yielded large samples of lampreys and teleosts during a five year period in the mid-1970s. This has provided a wealth of information on such features as seasonal abundance, size, growth, reproductive condition and other aspects of the biology of species belonging to the Petromyzontidae (Hardisty & Huggins, 1973; Abou-Seedo & Potter, 1979), Clupeidae (Claridge & Gardner, 1978; Titmus, Claridge & Potter, 1978; Potter & Claridge, 1985), Gadidae (Badsha & Sainsbury, 1978a; Claridge & Gardner, 1977; Claridge & Potter, 1984), Serranidae (Claridge & Potter, 1983), Mugilidae (Claridge & Potter, 1985), Atherinidae (Palmer, Culley & Claridge, 1979; Palmer & Culley, 1983) and Liparidae (Badsha & Sainsbury, 19786). The large numbers of gobies collected during this period belonged predominantly to the P. minutus complex which was represented by both P. minutus and P. lozanoi but not by P. norvegicus. The two former species were heavily infested with the plerocercoid larva of the cestode parasite Ligula intestinalis (L.), a feature which had earlier been recognized by Bassindale (1941) in P. minutus populations in the Severn. The present study has used material obtained from power station screens to list the gobies found in the Severn Estuary and Bristol Channel and to provide data on the relative abundance, size, growth and gonadal status of the more abundant species. Particular attention has also been paid to comparing aspects of ligulosis in P. minutus and P. lozanoi.

MATERIALS AND METHODS Fish were collected from the intake screens of power stations at Berkeley and Oldbury in the inner Severn Estuary, at Uskmouth on the River Usk one km from where this river joins the outer Severn Estuary, and at Hinkley Point on the southern shore of the inner Bristol Channel. The reader is referred to Radford & Joint (1980) for the delineation of the regions within the Estuary and Channel. Sampling at Oldbury and Berkeley was carried out weekly from July 1972 and September 1974 respectively (48 collections per year) and monthly at Uskmouth and Hinkley Point from October 1975. Sampling at all sites was terminated at the end of June 1977. In addition to sampling the screens of power stations in the Severn Estuary and Bristol Channel, a total of five collections was obtained between September 1976 and February 1977 from Pembroke Power Station in Milford Haven on the south-west tip of Wales, westwards of the northern boundary of the Bristol Channel. While the samples at Berkeley, Uskmouth, Hinkley Point and Pembroke represented GOBIES OF THE SEVERN ESTUARY 953 collections over variable periods of time, those at Oldbury were accumulated over 24 h. Where necessary the data for Oldbury have been corrected to a constant water intake of 22 x io9l day"1, the volume that typically passed through the screens between the autumn and spring when the station was under full load and the catches offish were greatest. Thus, the annual numbers of gobies given in this paper for the five years of the study each correspond to the estimated numbers that would have been taken if the intake volume had always been maintained at 22 x io9l during the 24 h period prior to each of the series of 48 samples taken each year. When considering the significance of the numbers at Oldbury, it is important to recognize that the inlet at this station is situated in an inshore area and draws from shallow water at low tide. The mean monthly values for the temperature and salinity at Oldbury and for the discharge of fresh water at Gloucester in the river are given in Claridge & Potter (1984). Gobies were measured and weighed to the nearest 1 mm and 01 g immediately after capture, except for the P. minutus complex collected between June 1974 and July 1975, which were placed in 70 % alcohol for at least 24 h before separating into P. minutus and P. lozanoi and recording their lengths and weights. Whenever samples were large, measurements were made on a random subsample of at least 100 fish. The weights of the gonad, L. intestinalis, and the food items in the stomach of large subsamples of P. minutus and P. lozanoi were also recorded. The first two values were expressed as a ratio of the total body weight and multiplied by too to give the gonadosomatic index (GSI) and parasite index (PI). Fecundity was derived from counts of the large and discrete eggs in known weight subsamples of ovaries of mature fish (see Healey, 1971 b). Ovaries were placed in Gilson's fluid to facilitate separation of the large eggs from the mesovarium. The scales were examined for circuli similar to those described in the detailed study of age and growth of gobies by Fouda & Miller (1981).

RESULTS Species of Gobiidae in the Estuary and Channel Eight species of Gobiidae were found in the Severn Estuary and inner Bristol Channel. The P. minutus/P. lozanoi complex was very common at Berkeley and Oldbury in the inner Severn Estuary, at Uskmouth in the outer Severn Estuary and at Hinkley Point in the inner Bristol Channel. The coloration, markings and dermal papillae characteristics subsequently described by Webb (1980), enabled a clear separation into P. lozanoi and P. minutus of all but five of the large number (5757) of the P. minutus complex collected from Oldbury between June 1974 and July 1975. While the common goby, P. microps, was also present at all three sites in the Estuary, it was not common at Hinkley Point in the Channel and was not found at Pembroke in south-west Wales outside the Channel. The crystal goby, Crystallogobius linearis (Duben) was caught at Oldbury during the late spring and summer, with catches between May and July reaching 64 in 1975 and 129 in 1976. The appreciable numbers of this species in the shallow waters of the inner Estuary are of interest since Wheeler (1978) has described it as a 'surface living fish in offshore water'. Moreover, Lloyd (1941) does not record it in his extensive check list of the marine fishes of the Bristol Channel and Severn Estuary based on his own studies and those of earlier workers such as Matthews (1933) and Day (1879). While the crystal goby was not collected at Berkeley or Uskmouth, two representatives of this species were obtained from Hinkley Point in the Channel. The remaining four species of goby were obtained infrequently or on only one occasion. Thus, while 25 Jeffreys goby, Buenia jeffreysii (Giinther), were taken at Oldbury in the winter of 1974/5, onty three other representatives of this species 954 P. N. CLARIDGE AND OTHERS were found at this location throughout the rest of the study and none were obtained from any of the other three power stations in the Severn Estuary and Bristol Channel. B. jeffreysii ranged in length from 32-48 mm ( = 0-4-1 9 g). The rock goby, Gobius paganellus L., with 14 individuals ranging in length from 37-75 mm ( =0-9-8-3 g), was taken at Oldbury and Berkeley and a single black

Pomatoschistus minutus complex

2 »

DC HI Q. 500

£0 iZ 25° •aw CO IT LJJ CD 26

3 Pomatoschistus microps

A

1972 1973 1976 1977 Fig. 1. The mean daily catch of sand gobies (Pomatoschistus minutus complex) and the common goby (Pomatoschistus microps) at Oldbury for each month between July 1972 and June 1977. The contribution of P. minutus to the total P. minutus complex between June 1974 and July 1975 is indicated by the hatched area. goby, Gobius niger L., of 104 mm ( = 203 g) was collected from Berkeley in June 1975. Two transparent gobies, Aphia minuta (Risso), were collected from Hinkley Point (April, May) and from Oldbury (June, July). The standard length of these four fish ranged from 38-48 mm ( =0-4-0-8 g).

Annual and seasonal catches The annual catches at Oldbury of fishbelongin g to the P. minutus/P. lozanoi complex varied considerably. Thus, the calculated total numbers for the 48 daily samples taken in each year ranged from 2232 in 1972/3 to 12521 in 1975/6. In the samples of P. minutus and P. lozanoi collected between June 1974 and July 1975, 806% were P. lozanoi and 194% P. minutus. The numbers of P. lozanoi were greater than those of P. minutus in every one of the weekly samples between June 1974 and July 1975. Initially, the numbers of both species followed similar trends, reaching maximum abundance in January GOBIES OF THE SEVERN ESTUARY 955 when the respective mean daily catches were 718 and 178 (Fig. 1). While P. minutus was present in only very small numbers from February to April and was absent in May and June, P. lozanoi was always present within this period and one catch of over 400 was taken in early May.

P. minutus

30 N = 307 1 20 A.. L O 20 111 § HI 20 DEC 0C

111 CD 20 < (- z o 20 oc LU 0. 0 20 MAR/APR 0 20

0 20

20 40 60 0 20 40 60 SO LENGTH(mm) Fig. 2. Length-frequency histograms for Pomatoschistus minutus and Pomatoschistus lozanoi in samples collected between August 1974 and July 1975.

The numbers of P. microps at Oldbury increased during the study, finally reaching 350 in the fifth year. A pronounced peak in abundance was observed in the December to March period of each of the years between 1973/4 and *976/7 (Fig. 1). However, the peaks in 1975/6 and 1976/7 were preceded by a much earlier increase in numbers which produced a second discrete peak in August in the first of these years and in November in the second (Fig. 1). Since the new 0+ recruits did not start arriving in numbers at Oldbury until August (Fig. 3), the increase in abundance that occurred at this site in the three months after April of 1975 was due to a return of older fish. 956 P. N. CLARIDGE AND OTHERS

Growth Scale analysis showed that only four 1 + representatives of P. lozanoi were present amongst the large numbers of this species taken in August 1974. The lengths of these fish (x = 48 5 mm) formed a discrete group at the upper end of the frequency histogram for this month (Fig. 2). A small number of 1 + P. lozanoi

30 JUN/JUL I f DEC . N=45 LI _ N=40 a

30 AU6 JAN > _ N=36 - N=49 o z LLJ o 30 LU SEP FEB DC N22 I U. - N 86 LLJ . M 30 LU OCT O N=29 cc LU Q. "A 30 r NOV APR/MAY - N=38

A. 1 J1 l1 0 20 40 60 0 20 40 60 LENGTH (mm) Fig. 3. Length-frequency histograms for Pomatoschistus microps based on pooled data for the period 1972-7. were also caught in some of the succeeding months. The bimodality in the wide range of lengths for 0+ P. lozanoi in August and September 1974 may represent either the progeny of successive spawnings in the same year (see Miller, 1984) or individuals derived from different spawning areas. The main modal class for P. lozanoi in August 1974 lay at 34-35 mm (Fig. 2). The corresponding modal class can be traced through subsequent histograms to December 1974, at which time it had reached 40-41 mm. Little shift could be observed in the modal class in the following five months. The 0+ recruits resulting from the 1975 breeding season first appeared in numbers in July. Examination of scales showed that all P. minutus caught in August 1974 were in their first year of life. While a few 1 + fish were obtained in the following six GOBIES OF THE SEVERN ESTUARY 957 months, the lengths of these tended to lie relatively discretely at the upper end of the range in the length-frequency histograms (Fig. 2). The modal class of the o + fish could be traced through sequential histograms from 38-39 mm in August 1974 to between 48 and 52 mm in November and December of 1974 and January of 1975 (Fig. 2). While the numbers of P. minutus declined dramatically in subsequent months (Fig. 1), the size range of the few remaining P. minutus that were caught in February, March and April fell within that recorded in January. The standard lengths of all P. microps caught in June and July during this study lay between 31 and 43 mm, with a modal class at 34-35 mm (Fig. 3). Fish with lengths less than 30 mm started to appear in August and even more conspicuously in September when one individual of only 14 mm was collected. The modal length class of these new o + recruits increased from 28-29mm m August and September to 30-31 mm in October and November. A modal class could be seen between 30 and 35 mm in most subsequent histograms through to April and May. Moreover, this modal class corresponds to one at 34-35 mm in June/July and 38-39 mm in August. While there is no information on the breeding time of the P. microps population that spends at least part of its life-cycle in the inner Severn Estuary, there is good evidence that it occurs at a similar time to that recorded by Fouda & Miller (1981) for other populations in south-western England, i.e. April to August, with a peak in June and July. This view is based on similarities between both the month when the first new 0+ recruits appeared (July or August depending on year) and also on their lengths at this time. Assuming that spawning is completed in August, the second modal length class (39-40 mm) in this month, which has been traced through from that corresponding to the new o + age class twelve months earlier, must represent which have recently entered or are entering their second year of life. This view is consistent with the pattern of circuli on the scales. Although the numbers of these 1 + fish declined after August, some remained into the winter, thereby contributing to the upper end of the range in length-frequency histograms. The largest P. microps collected during the study measured 52 mm and had a wet weight of 20 g. The mean standard length of o + P. minutus in weekly samples from each of the four months between December and March, at the end of which time these fish would have been approaching the completion of their first year of life, always lay between 52-1 and 53 o mm. By contrast, the mean length of 0+ P. lozanoi between December and June was much smaller, lying between 41 2 and 420 mm. These values are greater, however, than the 32-36 mm standard length reached by P. microps in the late winter and spring. The body weights of P. minutus and P. lozanoi reflect the differences in their standard lengths. Thus, after preservation in 70% alcohol, the maximum mean weekly weights ranged from 1-8-2-3 g in P. minutus in January and from 1-0-1-3 S m P- lozanoi in late February/early March. Pooled length-frequency data for C. linearis collected between May and July was markedly bimodal, with peaks occurring at approximately 30 and 40 mm in 1975 and 27 and 37 mm in 1976. Since this species has a life which 'only just 958 P. N. CLARIDGE AND OTHERS exceeds one year' (Wheeler, 1978), these peaks could correspond to the new 0 + recruits and to fish which have just entered their second year of life and will shortly die. However, as this species is said to reach sexual maturity between March and August (Collett, 1878), this would imply that it has an unusually fast rate of growth during the early part of life. Alternatively, therefore, the bimodality

20r

FEMALE

15 P. minutus X m za o

10 o FEMALE w P. lozanoi o Q < z o C5

MALE P. lozanoi N D F M 1974 1975 Fig. 4. The mean gonadosomatic index (GSI) for samples of males and females of Pomatoschistus minutus and Pomatoschistus lozanoi. may reflect the recruitment of two cohorts which had been spawned at different times within the long breeding season that characterises C. linearis and many other species of goby with a relatively short life span (Miller, 1984). Bimodality was present in some samples of a single age class of P. lozanoi in this study (Fig. 2) and has also been reported in P. microps (Miller, 1975; Fouda & Miller, 1981). The lengths of crystal goby caught during the current study ranged from 17 to 46 mm ( = 0-07-0-31 g).

Gonadosomatic indices and fecundity The GSIs of both sexes of P. minutus and P. lozanoi started to increase during December (Fig. 4). The mean GSI for female P. minutus rose from less than 1 in early December to 174 at the end of February. The male GSIs showed a less dramatic rise, with mean values rising from 05 in early December to 31-41 GOBIES OF THE SEVERN ESTUARY 959 between mid-February and mid-March. The mean GSIs for female and male P. lozanoi rose from less than 05 to respective maxima of 78 and 29 in April. It is important to recognise that, since the numbers of both species declined sharply over this period (Fig. 1), the maximum values are based on gonadal weights obtained from only a small residual group of animals.

P. lozanoi

x UJ Q

CO <

P. minutus

N D F M 1974 1975 Fig. 5. The percentage incidence of ligulosis and the mean parasite index (±95% confidence limits) for samples of Pomatoschistus minutus and Pomatoschistus lozanoi.

The fecundity of 28 P. lozanoi with lengths between 292 and 395 mm ranged from 410 to 2453 with a mean of 1270. The fecundities of the only two mature P. minutus collected from the inner Estuary and measuring 48 and 50 mm were 5231 and 5603. Parasitism by Ligula intestinalis and Contracaecum aduncum The incidence of infestation by L. intestinalis in each weekly sample was almost invariably greater in P. lozanoi than in P. minutus (Fig. 5). In samples collected between early November and late February, the percentage of P. lozanoi with ligulosis ranged from 53-1 to 968 %, compared with 127 to 542 % in P. minutus. In March and April, when P. minutus was either absent or present only in small numbers in the weekly samples, the incidence of infestation of P. lozanoi ranged 960 P. N. CLARIDGE AND OTHERS from 31 4 to 795 %. The relative numbers offish with ligulosis tended to decline in P. lozanoi over the sampling period. In both goby species, the parasite index, reflecting the relative weight of the parasite, declined through the winter and spring (Fig. 5). The parasite index was greater in P. lozanoi than P. minutus in all but one of 17 corresponding samples and in 13 of these the difference was significant at the 95 % level. In samples taken in late November and early

P. minutus Unparasitised

Parasitised; 3 HI

Q tr

P. lozanoi Parasitised

N D J F M 1974 1975 Fig. 6. The mean lengths (+ 95 % confidence limits) for Pomatoschistus minutus and Pomatoschistus lozanoi with and without Ligula intestinalis.

December, the mean contribution of L. intestinalis to the body weight of both P. lozanoi and P. minutus exceeded 16% on one occasion. In almost all samples, the mean lengths of ligulised P. lozanoi and P. minutus were less than those of their unparasitised counterparts (Fig. 6) and in many instances these differences were significant at the 95 % level. Moreover, in the few cases where the mean values for parasitized fish were greater than those of the unparasitized group, the differences were not significant (P > 05). The morphological expression of the effects of ligulosis was more apparent in P. lozanoi than in P. minutus. In extreme cases, the body cavity of the former species was extremely distended, the vertebral column curved (kyphosis) and the alimentary canal at least partially occluded. The nematode Contracaecum aduncum (Rud.) was found in the body cavity of 92 % of P. minutus and 146 % of P. lozanoi in the Severn Estuary. This parasite has also been recorded from gobies in the North and Wadden Seas (Fonds, 1973), in the English Channel off Plymouth (Lee, 1975) and in Polish coastal waters (Markowski, 1935). GOBIES OF THE SEVERN ESTUARY 961

Diet of Pomatoschistus minutus and Pomatoschistus lozanoi Examination of the stomach contents of P. minutus and P. lozanoi demonstrated that between early November and late February the diet of these two species consisted almost entirely of gammarids and mysids (Fig. 7). In general, the relative amount of Neomysis integer Leach ingested by both species was pro-

P. minutus P. lozanoi

Neomysls Integer

Other food Item*

• — - » ^ ••• •*- Empty stomach

P. minutu

Niomyil* Integer

Other food item

• Empty stomach

NDJF NOJF 1974 1975 1974 1975 Fig. 7. The percentage contribution of food items to the total weight of the stomach contents of Pomatoschistus minutus and Pomatoschistus lozanoi with and without Ligula intestinalis, together with the percentage number of stomachs which were empty. portionately greater in the earlier weeks of this period, whereas the reverse trend was seen with Gammarus salinus Spooner. Although the trends shown by the numbers of these two species of crustacean in the water at Oldbury fluctuated considerably during this period (Moore, Moore & Claridge, 1979), it is probably relevant that the abundance of G. salinus rose progressively from early February to mid-March. In neither species of goby were conspicuous differences observed between the diet of unparasitized fish and those infested with Ligula. However, the parasitized fish showed a higher frequency of empty stomachs and, in some instances where infestation was severe, the gut appeared to have been at least partially occluded. Amongst the very small numbers of food organisms other than gammarids and mysids in sand gobies were an unidentified goby in a large specimen of P. minutus measuring 72 mm and the remnants of a (Nereis sp.). 962 P. N.CLARIDGE AND OTHERS

DISCUSSION Abundance in estuary and possible spawning locations The large numbers of the Gobiidae collected from the inshore waters at Oldbury in the inner Severn Estuary, predominantly due to a massive contribution by the P. minutus/P. lozanoi complex, was rivalled only by fish representing the Gadidae. In terms of total numbers, the P. minutus/P. lozanoi complex ranked first in 1972/3,1973/4 and !976/7 and second in 1974/5 and *975/6 when it was superseded by the whiting, Merlangius merlangus (L.) (Claridge & Potter, 1984). Had P. lozanoi predominated at Oldbury to the same extent in the other four years as in 1974/5, when it constituted 806 % of the total catch of the complex, it would have ranked amongst the top three species in all years. This emphasises the importance to P. lozanoi of habitats provide by the shallows in the inner Estuary. The decline in the numbers of P. minutus in the Severn Estuary during the winter closely parallels the situation described for this species in the Medway Estuary (van den Broek, 1979) and in the Ythan Estuary and two of its tributaries (Healey, 1971a). While Healey (1971a) believed that this reflected a movement from the upper estuary and tributaries towards areas where they would subse- quently spawn, both Fonds (1973) and Hesthagen (1975, 1977) considered that a similar decline in numbers was brought about by an offshore movement towards warmer waters as the temperature in the shallows fell to a low level. Since the decline in numbers in the Severn occurred between January and February of 1975, when the gonads were developing rapidly and temperatures were ap- proaching their lowest values (Claridge & Potter, 1984), it is difficult to assess whether temperature or gonadal maturation was the prime factor responsible for inducing the movement. However, unlike P. minutus in the Wadden Sea (Fonds, 1973) and Oslofjorden (Hesthagen, 1975,1977), this species of sand goby did not return to the inner Severn Estuary in the spring when temperatures started to rise. This feature, together with the capture of only two mature P. minutus at Oldbury, suggests that this sand goby breeds further downstream in the outer Estuary or Bristol Channel. A breeding locality in the Bristol Channel would be consistent with the fact that, in the course of extensive studies on the biology of British gobies, P. J. Miller (personal communication) has never observed P. minutus spawning in an estuarine environment. Although P. lozanoi underwent similar seasonal changes at Oldbury to those of P. minutus, this species was still conspicuous in samples taken in late winter and early spring when GSIs were rising and a number of mature females were collected. While these features might imply that P. lozanoi sometimes breeds in the inner Severn Estuary, it should be borne in mind that, as with P. minutus, the numbers of P. lozanoi still showed a marked decline at the time when gonads were developing. Moreover, this species is also known to be abundant in the Bristol Channel (Wallis & Beardmore, 1980, 1984). The question of determining where P. minutus and P. lozanoi typically breed is complicated by apparently contradictory observations in the literature. For GOBIES OF THE SEVERN ESTUARY 963 example, while Healey (1971a) found that P. minutus eggs survived better in salinities of 10-25 %0 than at either 05 %o or 35 %o, Fonds (1973) stated that this species showed a greater tendency to spawn in the North Sea than in the reduced salinities of the inshore Wadden Sea. The latter finding is consistent with the fact that Lee (1975) discovered P. minutus spawning off Plymouth at salinities of an< 3°~35%o ^ Hesthagen (1975) records P. minutus breeding at 26%O in Oslof- jorden. Moreover, goby eggs, which almost certainly belonged to P. minutus (J. M. Gee, personal communication), were found by Russell (1980) in the Bristol Channel at salinities close to full strength sea water. From the above observations, it would seem reasonable at the present time to regard P. minutus and P. lozanoi at least provisionally, as marine species, which nevertheless spend considerable periods within the Severn Estuary. However, the possibility that the latter species may also breed in the lower reaches of the estuary cannot be excluded. Irrespective of where P. minutus and P. lozanoi breed, the consistently much higher catches of the latter species throughout the year at Oldbury in the inner Severn Estuary, including those periods when salinities were at their lowest levels, conflict with the views expressed by Fonds (1973) who considered P. lozanoi to be physiologically less well adapted than P. minutus to the reduced salinities of estuaries. Furthermore, Fonds also believed that P. lozanoi was adapted towards 'a more neritic environment and a nekto-benthic food supply' than P. mtnutus which in turn was better suited to exploiting the' benthic food supply of estuaries'. These views have not been substantiated by our observations which have failed to demonstrate conspicuous differences between the dominant food organisms ingested by P. minutus and P. lozanoi in the shallows of the inner Severn Estuary at Oldbury. As with P. minutus and P. lozanoi in the Severn Estuary, amphipods and mysids were major contributors to the diet of P. minutus in other waters in Europe (Kuhl, 1961; Casabianca & Kiener, 1969; Hesthagen, 1971; Healey, 1971a; Fonds, 1973)- Peak annual catches of P. microps were taken in February 1974, in January of 1975 and 1976 and in February and March of 1977 at times when the mean salinities fell to their lowest levels in those years (Claridge & Potter, 1984). This independence from the influence of low salinities in the inner Severn Estuary in the winter is consistent with the conclusion of Fonds (1973) that P. microps was even more euryhaline than P. lozanoi and P. minutus which, as this study has shown, can spend considerable periods in estuaries. While large catches of P. microps were taken when temperatures fell to their lowest levels in the winter of 1975 and 1976, the numbers were considerably lower in January of 1977 than in either the preceding or following month. It may thus be significant that the mean monthly temperature in January 1977 fell almost to 40 °C, with individual values as low as 34 °C, whereas the minimum monthly means in 1975 and 1976 were 67 and 48 °C respectively (Claridge & Potter, 1984). This recalls the observations of Jones & Miller (1966) that in several different localities P. microps started to migrate towards offshore and warmer water as temperatures fell below 5°C. 964 P. N.CLARIDGE AND OTHERS As concluded earlier, the peak spawning of the population of P. microps that gives rise to the representatives of this species found at Oldbury, probably occurs at the same time, i.e. June and July, as that recorded by Fouda & Miller (1981) for the common goby in the Teign Estuary. While few P. microps were found in the inner Estuary at this time in 1974 and 1976, several fish near or at the end of their first year of life were caught in mid-summer in 1975 and 1977. Although this does not resolve the question of whether the common goby spawns in the inner Estuary, this species has been found breeding in the lower reaches of estuaries in Devon (J. M. Gee, personal communication) and on the Isle of Man (Miller, 1963). The latter study showed that as P. microps matured, it moved out of upper estuarine and low salinity areas to downstream breeding regions where salinities ranged from 6-1 o%o at low tide to nearly full strength sea water at high tide. From these observations, it thus seems likely that the common goby would be capable of spawning in at least the outer Estuary of the Severn. Since breeding can take place in areas where salinities consistently approach full strength sea water (see e.g. Jones & Miller, 1966), it would also appear to be well adapted to breeding in suitable spawning sites within the Bristol Channel. It is worth noting, however, that limited numbers of P. microps were taken during this study at Hinkley Power Station in the inner Channel. The trends shown by the 0+ age class in the length-frequency data for P. minutus, P. lozanoi and P. microps, show that all three species typically grow most rapidly in the summer and autumn after hatching and have only one breeding season. While spawning occurs at the end of the first year of life, some fish do survive for a further few months. These conclusions are essentially the same as those described for some other populations of P. minutus and P. microps (Healey, 19716; Miller, 1975; Fouda & Miller, 1981). However, Hesthagen (1977) considers that an appreciable number of P. minutus in Oslofjorden have a second breeding season towards the end of their second year of life, thereby paralleling the situation reported for P. norvegicus in west coast Scottish waters (Gibson & Ezzi, 1981).

Gonadosomatic indices, spawning times and fecundity While P. minutus and P. lozanoi have not been observed breeding in either the Severn Estuary or Bristol Channel, a good indication of when spawning com- mences can be gained from the trends shown by the GSIs and the time when mature females were caught. Since the mean GSIs of female P. minutus rose very sharply during January and February, with the few remaining fish in the estuary attaining a mean of 174 by the end of the latter month, it seems likely that spawning was imminent. This view would be consistent with the capture of two mature females in March and with the spawning times estimated by Swedmark (1958), Healey (1971 a) and Hesthagen (1977). While Healey (1971 a) obtained a number of sand gobies throughout the late winter and spring from the more northern Ythan Estuary, his GSIs for female fish did not peak until May and at this time were appreciably lower (< 12) than those of P. minutus in the inner Severn Estuary GOBIES OF THE SEVERN ESTUARY 965 in February. Since the two highest mean GSIs for female P. lozanoi were recorded in late April, during which month the majority of the 28 mature females were caught, this species may start spawning slightly later than P. minutus. Such a view would be consistent with the data obtained by Fonds (1973) and would partly explain the greater modal length of juvenile P. minutus compared with P. lozanoi in August. The range in fecundities for P. lozanoi in this paper (410-2453) are apparently the first published for this species. The low mean fecundity of P. lozanoi (1270) compared with the two mature P. minutus (5380) is almost certainly related in part to a smaller size at maturity. However, it is also probably relevant that the mean GSIs of females of P. minutus in mid to late February were much greater than those attained at any time by P. lozanoi. In other words, P. minutus appears to divert a greater amount of its energy into gonadal development than P. lozanoi. While the egg counts for the two ripe P. minutus were much greater than the means of 2556 and 2749 recorded for sand gobies collected in two successive years by Healey (19716), a greater fecundity in the Severn fish is consistent with the fact that their GSIs were approximately twice the maximum monthly mean GSI given for female P. minutus in the Ythan population (Healey, 1971a). It is also worth noting that the mean egg numbers of P. minutus taken off Plymouth in two consecutive years (2383 and 2577) were comparable with those given by Healey (1971a). Ligulosis in Pomatoschistus minutus and Pomatoschistus lozanoi The data on parasite index and percentage infestation and the morphology of heavily infected fish show that in comparison with P. minutus the population of P. lozanoi in the Severn Estuary in 1974/5 suffered to a greater extent from ligulosis. Since there was, however, a trend towards smaller mean lengths and higher frequencies of empty stomachs among the infected representatives of P. minutus and P. lozanoi, there are indications that Ligula affects feeding be- haviour, food intake and growth rates in both species. The decline in the parasite index in both species between late autumn and early spring could be due to higher mortality among the more heavily infected fish, either as a direct result of infection or through increased susceptibility to predation. Increased mortality of heavily ligulised fish would be consistent with the tendency for the incidence of parasitism to decline until early March in P. lozanoi and less conspicuously so in P. minutus until mid-January. A decline in the incidence of ligulosis with body size and age class in bleak, Alburnus alburnus (L.) and roach, Rutilus rutilus (L.) has been attributed to higher mortality, as well as to a change in diet away from the primary copepod hosts of the parasite (Harris & Wheeler, 1974; Kennedy & Burrough, 1981). The possibility that raised mortality rates may be due to higher predation is supported by the observations of Croll (1968) on the adverse affects of Ligula infestation on the swimming abilities of heavily parasitized rudd, Scardinius erythrophthalmus (L.). Similarly, Hass (1939) has drawn attention to the clumsy movements of P. minutus and P. microps infected by the cestode 966 P. N.CLARIDGE AND OTHERS Schistocephalus dimorphus Creplin and commented that these must increase susceptibility to predation by piscivorous birds such as gulls. The initial period of decline in the incidence of ligulosis shown by both species of goby in the Severn Estuary was followed by an increased incidence in P. minutus and, on at least two subsequent occasions, in the case of P. lozanoi. Since these changing trends were seen at a time when the numbers of both species were declining from their high winter levels, they could reflect a tendency for ligulised fish to remain in the Oldbury region after most of the unparasitized fish had emigrated. Such a possibility recalls the case described in the Australian migratory teleost, Galaxias maculatus (Jenyns), where fish with Ligula tended not to undertake their normal upstream spawning migration (Pollard, 1974). The extreme inhibitory effects of Ligula infestation on gonadal maturation documented for several teleosts (Kerr, 1948; Arme, 1968; Arme & Owen, 1968; Pollard, 1974) have not been observed in the present studies. Although, infected females of P. lozanoi tended to have lower GSIs in January and February, similar differences were not noted in the following two months. Likewise, the mean GSIs of females of P. minutus, although consistently lower in ligulised fish when the gonads were approaching maturity, nevertheless remained high and ultimately exceeded the maximum mean monthly means recorded by Healey (1971 a) for this species in the Ythan Estuary.

Our gratitude is expressed to R. J. Huggins, J. Knight, D. C. Gardner and R. A. Milne who helped with the collection of animals and to R. J. Manning for drawing the figures. We are also most grateful to Dr P. J. Miller and Dr C. J. Webb for helpful discussions. Financial support was provided by the Leverhulme Foundation.

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