Atlantic wolfish (Anarhichas lupus L.; Pisces: Anarhichidae) predation on green sea urchins (Strongylocentrotus droebachiensis (O.F. Mull.); Echinodermata: Echinoidea)

in eastern ~ewfoundlandl

D. W. KEATS AND D. H. STEELE Department of Biology, Memorial University of Newfoundland, St. John's, NJld., Canada AlB 3x9

AND

G. R. SOUTH* Department of Biology and Newfoundland Institute for Cold Ocean Science, Memorial University of Newfoundland,

St. John's, NJld., AlB 3x9

KEATS, D. W., D. H. STEELE, and G. R. SOUTH. 1986. Atlantic wolffish (Anarhichas lupus L.; Pisces: Anarhichidae) predation on green sea urchins (Strongylocentrotus droebachiensis (O.F. Mull.); Echinodermata: Echinoidea) in eastern Newfound- land. Can. J. Zool. 64: 1920-1925.

The diet of the Atlantic wolffish was studied by examining the contents of the gastrointestinal tracts of 90 individuals collected from the sea urchin dominated rocky subtidal in eastern Newfoundland. Green sea urchins comprised 75% of the overall diet by weight. Horse mussels ranked second but comprised only 9.5% of the diet. The remainder of the diet consisted of several species of invertebrates and fish. The average (over the whole season) wolffish contained 120 g of urchins, equivalent to the biomass of urchins on 0.23 m2 in the middle of the urchin-dominated zone. During April-September, prior to breeding, the average male wolffish contained 174 g of urchins, and the average female contained 85 g of urchins, biomass values representing, respectively, 0.33 and 0.16 m2. Assuming that the contents of the gastrointestinal tract turn over every 3 days, it was calculated that during May through August each wolffish consumes on average 5.29 kg of urchins (males, 7.09 kg; females, 3.50 kg). Based on these figures, a density of 1 wolffish pair per 20 m2 would be required to consume the mean biomass (532 g m-') of urchins present in the urchin-dominated zone in 1 year.

G A T S , D. W., D. H. STEELE et G. R. SOUTH. 1986. Atlantic wolffish (Anarhichas lupus L. ; Pisces: Anarhichidae) predation on green sea urchins (Strongylocentrotus droebachiensis (O.F. Mull .); Echinodermata: Echinoidea) in eastern Newfound- land. Can. J . Zool. 64: 1920-1925.

L'examen des contenus stomacaux de 90 individus a permis d'Ctudier le rCgime alimentaire du loup atlantique dans la zone subcotidale rocheuse dominCe par les oursins dans la partie orientale de I'lle de Terre-Neuve. Les oursins constituent 75% (masse) du rkgime alimentaire. Les moules Modiolus modiolus viennent en second, mais ils ne constituent que 9,5% de tout le rCgime. Le reste du rCgime contient plusieurs espkces d'invertCbrCs et de poissons. Au cours de la saison, un loup atlantique contient en moyenne 120 g d'oursins, ce qui Cquivaut a la biomasse d'oursins contenus dans 0,23 m2 au milieu de la zone dominee par les oursins. D'avril a septembre, avant la fraye, un mQle moyen contient 174 g d'oursins (biomasse contenue dans 0,33 m2) et une femelle moyenne, 85 g d'oursins (biomasse contenue dans 0,16 m2). En supposant que les contenus stomacaux sont remplacCs tous les 3 jours, il est possible d'Cvaluer qu'un loup atlantique consomme en moyenne 5,29 kg d'oursins de mai a la fin d'aoQt (7,09 kg par mQle, 3,50 kg par femelle). D'aprks ces chiffres, il faudrait un couple de loups atlantiques par 20 m2 pour consommer la biomasse moyenne totale (532 g mP2) d'oursins prCsents en 1 annCe dans la zone dominCe par les oursins.

[Traduit par la revue]

Introduction stages (Hagen 1983; Himmelman and Steele 1971; Hooper

During the early 1970's extensive and highly productive kelp beds disappeared along much of the Nova Scotia coast (Mann 1977; Wharton and Mann 198 1). This was the result of grazing by green sea urchins, the density and biomass of which increased considerably at that time (Breen and Mann 1 9 7 6 ~ ) . In the early 1980's, after ca. 12 years in a sea urchin dominated state, the coastal ecosystem off Nova Scotia reverted to kelp beds following a disease-induced mass mortality of urchins (Moore and Miller 1983; Scheibling 1984; Miller 1985~) . It was hypothesized that the proximal cause of this urchin population ex~losion was a decrease in reda at ion bv lobsters. which

I .I

resulted from a decrease in lobster stocks due partly to overfishing and partly to the closure of the Canso Causeway (Breen and Mann 1976b; Wharton and Mann 1981). This hypothesis has recently been shown to lack empirical support (Miller 1985b). There are a number of vertebrate and inverte- brate predators, which feed on urchins at different developmental

'~ewfoundland Institute for Cold Ocean Science contribution No. 96.

'present address: Huntsman Marine Laboratory, Brandy Cove, St. Andrews, N.B . , Canada EOG 2x0.

1980; ~ i l l e r 1985b). An understanding of the actual and potential role of predation in controlling sea urchin populations requires the study of predation at each stage of development, and by each species of predator. Predation rates should be determined for both states of the coastal ecosystem, barrens and macroalgal beds, to determine the effects of predation in each state of the ecosystem.

The present study examines predation on urchins by Atlantic wolffish in the urchin dominated subtidal of eastern Newfound- land. Unlike the barrens in Nova Scotia, those in Newfoundland have been stable for 21 years or more (Hooper 1980; D. H. Steele, personal observation). Extensive Laminaria longicruris dominated kelp beds do not occur in eastern Newfoundland, nor did a kelp bed develop when urchins were removed experimen- tally (Keats 1986). Rather, the algal beds that developed when urchins were removed were dominated by Alaria esculenta in shallow water (0-2 m), and by Desmarestia aculeata in deeper water (6-9 m).

Atlantic wolffish migrate seasonally in Newfoundland (Keats et al. 1985~) . They appear in shallow water in the late winter and early spring, and occupy nesting holes during the summer. They deposit solitary egg masses in holes under rocks in

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

SAV

AN

NA

HR

IVN

AT

LA

BB

F on

11/

11/1

4Fo

r pe

rson

al u

se o

nly.

KEATS ET AL. 1921

September and October, and each egg mass is guarded by a male. Atlantic wolffish show reduced feeding during the breeding season. This is particularly true for females just prior to egg laying and for males guarding egg masses. Most wolffish are gone from shallow water by December. The influence of migration and reproduction on feeding is an important considera- tion in determining the effects of Atlantic wolffish predation on green sea urchins (Keats et al. 1985 a).

This study reports the diet, by wet weight and frequency, of Atlantic wolffish from urchin-dominated areas in eastern Newfoundland. The biomass of urchins consumed by fish of each sex during different stages (Keats et al. 1985a) of the reproductive season is estimated. The size structure of urchins from gastrointestinal tracts is examined and compared with the size and biomass structure of urchin populations from a typical barren site. These data are used to estimate the potential effects of wolffish predation on urchins in nature.

Materials and methods Ninety wolffish were collected at 5-15 m depth using spearguns

while scuba diving. Collections were made on the Avalon Peninsula, in the urchin dominated hard substratum typical of the open Atlantic coast of Newfoundland. Specimens were taken to the laboratory in coolers, and either dissected while fresh, or frozen for later dissection. Each fish was weighed (to nearest 10 g), and the contents of the gastrointestinal tract were identified and weighed to the nearest 0.1 g . Urchin tests that were not too crushed or digested were measured to the nearest 0.1 mm. A length frequency distribution for the fish used in this study was presented by Keats et al. (1986). Most of the wolffish were large (mean length, 79.7 cm; SE, 1.35), so size of fish was not considered in this study. An urchin size frequency and biomass distribution for the middle of the barren zone at a site in Conception Bay (46'40' N, 52'50.2' W) was calculated as the 5-year mean of samples from 6-9 m used by Keats et al. (1985 b) .

Gut contents data are given as overall means (data from all fish col- lected) and are also presented by sex and seasonal reproductive state as described by Keats et al. ( 1 9 8 5 ~ ) . Keats et al. ( 1 9 8 5 ~ ) found no significant difference between feeding indices of individual fish collected in April-June and those collected in July-September. These data have therefore been combined here as category A (individual fish collected during April-September). The other categories are paired fish collected during August-September, prior to spawning (B), and males guarding eggs (C).

To calculate the biomass of urchins that the average Atlantic wolffish consumes annually, it is necessary to know the turnover time for the gut contents and the number of days during which the fish is present in the inshore habitat. The whole gastrointestinal tract must be considered for wolffish because the stomach and gastric digestion are reduced, with most digestion taking place in the intestine (Verigina 1974). Gastro- intestinal evacuation rates have not been studied for Anarhichas lupus, so we have assumed a turnover time for the contents of the digestive tract of approximately 3 d. This is probably conservative for fish feeding on macrobenthic prey in the 5- 13°C range (Fang and Grove 1979; MacDonald et al. 1982). This can be corrected, and more accurate models (Jobling 1981) applied, when more detailed informa- tion becomes available. Only the period from May to August is considered in calculating potential predation, because wolffish were uncommon before May, and because the percentage of the population involved in breeding during the autumn and the time that they remain in shallow water following spawning are not known. Data on the biomass of urchins at the Conception Bay site were used to estimate the minimum area required to supply the biomass of urchins consumed between Mgy and August.

Results Twenty-three of the 90 fish examined contained no food

(Table 1). Green sea urchins comprised 76% of the diet by

weight and were present in 96% of the wolffish that contained food. Horse mussels (Modiolus modiolus) ranked second but constituted only 9.5% of the diet by weight and occurred in only 14 fish. Blue mussels (Mytilus edulis) made up 1.6% and occurred in 21 guts. Crabs (Hyas araneus and Pagurus spp.) totaled 4.4% of the diet. The 3.7% for codfish (Gadus morhua) was the result of a single large individual present in a single wolffish. Similarly, a cunner (Tautogolabrus adspersus) oc- curred in one digestive tract. The 1.9% for wolffish eggs was due to the gut contents of one male, captured from a nesting hole.

Solitary females contained an average of 85.4 g of urchins; solitary males contained an average of 174 g, although this difference was not significant (t-test, p > 0.05; Table 2). This decreased to 21.6 g for females and 109 g for males in nesting pairs, although these decreases were not significant (t-test, p > 0.05). Males guarding egg masses had little or no food in their gastrointestinal tracts.

An estimate of the minimum area from which the average wolffish could have obtained the given biomass of urchins present in its digestive tract was made (Table 3). During April-September the average wolffish digestive tract (assuming a 1: 1 sex ratio) contained a biomass of urchins equivalent to that found in 0.24 m2 of bottom. Assuming a 3-d turnover time, the average wolffish would consume a biomass of urchins equiva- lent to that present in 9.94 m2 during the period from May to August. Therefore, a density of 1 wolffish pair per 20 m2 would be required to consume the mean biomass of urchins present in the urchin-dominated zone in 1 year.

The size-frequency distribution for urchins from wolffish guts (less than 20% of the urchins were intact enough to measure) shows that wolffish feed mainly on urchins larger than 20 mm test diameter (Fig. I). The 5-year mean size frequency and biomass distribution for the middle of the urchin-dominated zone show that this is the size range which is least abundant in nature, but which accounts for most of the biomass (Fig. 1).

Wolffish were observed feeding on seven occasions. They are visual predators, and it is possible to predict which urchin a wolffish will consume from the direction in which the eyes are pointed. When an urchin is "sighted" the wolffish generally turns slightly on its side and grasps the urchin with its canine teeth, while its body is at a 45' angle laterally to the bottom. A side-to-side motion is sometimes used to remove the urchin from the substratum. On two occasions the urchin was dropped briefly, then picked up again and eaten. There is a violent dorsoventral jerking of the wolffish as the urchin test is being crushed. One fish, near a nesting site, remained within a 10-m radius and consumed five urchins. All seven of ,the fish observed feeding travelled at least 2-3 m between consuming individual urchins. On two separate occasions, however, wolffish with full digestive tracts were captured near ca. 0. 1-m2 patches with no urchins, indicating that they may have removed all of the urchins from the patches.

Discussion Although the diet of Atlantic wolffish in eastern Newfound-

land was dominated by green sea urchins, other studies indicate that its diet varies depending on prey availability. It apparently feeds on the more abundant shelled prey, but may also take fish (Albikovskaya 1982, 1983; Templeman 1984). Templeman (1984) found that molluscs, primarily whelks and Iceland scallops (Chlamys islandicus), were the most important prey in deeper, offshore areas. Ophiuroids and sea urchins were next in importance. There was also a high incidence of fish (mainly

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

SAV

AN

NA

HR

IVN

AT

LA

BB

F on

11/

11/1

4Fo

r pe

rson

al u

se o

nly.

CAN. J. ZOOL. VOL. 64. 1986

TABLE 1 . Gastrointestinal tract contents of all 90 wolffish collected during 1983- 1984

Mean % of % occurrence weight 2 SE diet by Frequency in guts that

(g) weight (N> contained food Taxon

H ydrozoa Abientinaria bietina

Crustacea Hyas araneus Pagurus spp.

Gastropoda Buccinum spp. Colus spitzbergensis Margarites groenlandicus Nucella lapillus

Bivalvia Chlamys islandicus Hiatella arctica Mytlius edulis Modiolus modiolus

Polychaeta Pectinaria sp.

Stelleroidea Ophiopholus aculeata

Echinoidea Strongylocentrotus

droebachiensis

Ascidiacea Halocynthia pyriformis

Pisces Anarhichas lupus (eggs) Gadus morhua Tautogolabrus adspersus

Other Unidentifiable material Inorganic material Coralline algae Fleshy algae

Total

Empty guts

Sebastes sp.) in wolffish guts (15% by volume). Albikovskaya (1982, 1983) also found a high incidence of Sebastes in Atlantic wolffish from deep water off Newfoundland, but echinoderms (asteroids, echinoids, ophiuroids) and decapods (Hyas and others) were more important. Jonsson (1982) reported that at locations in Iceland where sea urchins were abundant wolffish guts contained little else, and where horse mussels were very abundant wolffish contained entirely horse mussels. At other sites ophiuroids or the bivalve Arctica islandica predominated (Jonsson 1982). The low importance of horse mussels in the wolffish examined during the present study is surprising, because they are abundant in eastern Newfoundland. Possibly, the occurrence of horse mussels in dense beds may confer protection from wolffish predation.

Our estimate of wolffish predation on urchins has several biases. (i) The weight of urchins consumed will be greater than the weight of the urchins remaining in the digestive tract. To correct this bias the effects of digestion must be determined. (ii) The gastrointestinal evacuation rate for Atlantic wolffish is unknown, so it should be determined and used with the

appropriate model (Jobling 198 1) to calculate a more accurate estimate of annual consumption. (iii) Only the May-August period was considered in calculating consumption. Consump- tion prior to May, and in the autumn by females that have spawned and males that have finished guarding eggs, should be determined. (iv) Wolffish do not usually eliminate all of the urchins from a given area, but rather they select large individuals that have the greatest grazing impact. Thus their effect is probably greater than indicated by the bottom area containing a biomass equivalent to the biomass eaten.

The high importance of urchins in the diet of Atlantic wolffish and the calculated predation of individual wolffish during May-August shows that they potentially influence urchin populations. Wolffish densities as high as the calculated densi- ties needed to eliminate all large urchins have been observed at localities where breeding sites are abundant (P. W. Keats, personal observations). In Bay Bulls (47' 19' N, 52'46' W), at a site with abundant wolffish, there were numerous patches of large algae (Desmarestia spp., Laminaria digitata, Agarum cribrosum). Nearby sites in the same area, without wolffish,

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

SAV

AN

NA

HR

IVN

AT

LA

BB

F on

11/

11/1

4Fo

r pe

rson

al u

se o

nly.

KEATS ET AL. 1923

TABLE 2. Gastrointestinal tract contents of all 90 wolffish collected during 1983- 1984, arranged by breeding category. Numbers are arithmetic mean weight (grams) k standard error

Solitary fish, April-September Nesting pairs

Males guarding Taxon Female Male Female Male egg mass

Hydrozoa Abientinaria abietina

Crustacea Hyas araneus Pagurus spp.

Gastropoda Buccinum spp. Colus spitzbergensis Margarites groenlandicus Nucella lapillus

Bivalvia Chlamys islandicus Hiatella arctica Mytilus edulis Modiolus modiolus

Polychaeta Pectinaria sp.

Stelleroidea Ophiopholus aculeata

Echinoidea Strongylocentrotus

droebachiensis

Ascidiacea Halocynthia pyriformis

Pisces Anarhichas lupus k eggs Gadus morhua Tautogolabrus adspersus

Other Unidentifiable material Inorganic material Coralline algae Fleshy algae

No. of wolffish sampled

TABLE 3. Estimates of the minimum area from which a wolffish could have obtained the mean biomass of urchins present in its digestive tract, the consumption of urchins between May 1 and August 31, and the minimum area from which the total biomass of urchins consumed during that

period could have been obtained

Biomass of Estimated consumption Estimated minimum area urchins in Equivalent of urchins between sampled between

Category (sex) GI tract area (m2) May and August (kg)* May and August (m2)*

Overall 120.0 0.23 4.92 A (male) 173.7 0.33 7.09 A (female) 85.4 0.16 3.50 Average A t 129.6 0.24 5.29 B (male) 109.2 0.20 NCS B (female) 21.6 0.04 NC C (male) 21.7 0.04 NC

NOTE: Urchin biomass in barrens is 532.0 2 76.5 (SE) g m-2 (5-year mean from data used by Keats (1986)). Categories: A , solitary, prebreeding fish; B , nesting pairs; C, males guarding egg mass.

*Based on an assumption of a turnover time of 3 days for the contents of the GI tract. tAssuming a 1 : 1 sex ratio. $Not calculated (see text).

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

SAV

AN

NA

HR

IVN

AT

LA

BB

F on

11/

11/1

4Fo

r pe

rson

al u

se o

nly.

1924 CAN. J. ZOOL. VOL. 64, 1986

estimated from field samples. Data on wolffish abundance and feeding in kelp beds are also needed to complete our knowledge

Atlantic wolffish GI t rac ts of the role of wolffish predation in controlling urchin popula- N = 1 8 2 u r c h i n s tions. If their diet depends on prey availability, as suggested

above, then determining the predation rate on urchins in healthy kelp beds may not be sufficient to enable an assessment of the potential for wolfish to contribute to the control of incipient urchin outbreaks. This potential can only be determined, with certainty, by the appropriate stocking experiments.

Acknowledgements

dominated

I I I 1 I I I I I 1

T e s t d i a m e t e r ( m m )

FIG. 1. Size-frequency distribution for urchins from wolffish gastrointestinal (GI) tracts (upper graph), and the 5-year mean size-frequency and biomass distribution for the middle of the urchin- dominated zone at a site in Conception Bay (lower graph).

lacked fleshy macrophytes. It is possible that wolffish predation on urchins may have reduced urchin grazing sufficiently to allow macroalgal growth.

Although Breen and Mann (1976b) concluded from a com- puter simulation that wolffish had little or no effect on sea urchin populations, it has since been suggested that fish predation could be important in controlling urchin densities in Nova Scotia (Bernstein et al. 198 1 ), Newfoundland (Hooper 1980), and Norway (Sivertsen and Bjorge 1980). Bernstein et al. (1981) noted that urchins occurred in Atlantic wolffish and American plaice (Hippoglossoides platessoides) and suggested that such predators could be important in determining urchin behaviour as well as density. They noted that in summer, when these fish are common inshore, urchins tend to hide during the day and feed mainly at night. In the winter, when these fish are absent, however, urchins forage during the day and night. If this behavior is an adaptation to predation, then it suggests that diurnal predators such as fish, rather than nocturnal predators such as lobsters, have been important in selecting for evolution of the urchin behaviour.

The observed size selectivity of wolffish predation on urchins is likely due to two factors. Firstly, since wolffish select their prey visually and feed on urchins individually, it is energetically more profitable to feed on larger urchins. It is therefore unlikely that they would chose a small urchin when larger prey is available. Secondly, the smaller urchins (< 10 mm) generally occupy cryptic microhabitat among coralline algae, in crevices, among horse mussels, and under rocks (Keats et al. 1985 b).

This study indicates that predation on urchins by Atlantic wolffish is important and must be considered in modelling the nearshore rocky subtidal ecosystem. The present status of Atlantic wolffish populations should be determined by examin- ing historical catch records, and their density should be

We acknowledge the financial support of Natural Sciences and Engineering Research Council of Canada strategic grant G-0233 and operating grants A-4648 and A- 1732. The follow- ing persons gave technical and diving assistance: Don Chafe, Clyde Collier, Steve Dawson, Peter Noble, Ian Roy, and Pierre Ryan. Thanks are due to Bob Hooper for stimulating discussion and for always being ready and willing to dive. We thank J. Himmelman for his critical review of an earlier draft of this manuscript.

ALBIKOVSKAYA, L. K. 1982. Characteristics of feeding of three species of wolffishes in the northwest Atlantic. NAFO SCR Doc. 82/VI/69. Ser. No. N562.

1983. Feeding characteristics of wolffishes in the Labrador- Newfoundland region. NAFO Sci. Coun. Stud. 6: 35-38.

BERNSTEIN, B. B., B. E. WILLIAMS, and K. H. MANN. 1981. The role of behavioral responses to predators in modifying urchins' (Strongylocentrotus droebachiensis) destructive grazing and sea- sonal foraging patterns. Mar. Biol. (Berlin), 63: 39-49.

BREEN, P. A., and K. H. MANN. 1976a. Destructive grazing of kelp by sea urchins in eastern Canada. J. Fish. Res. Board Can. 33: 1278- 1283.

1976b. Changing lobster abundance and the destruction of kelp beds by sea urchins. Mar. Biol. (Berlin), 34: 137- 142.

FANG, R., and D. GROVE. 1979. Digestion. In Fish physiology. Vol. 8. Bioenergetics and growth. Edited by W. S. Hoar, D. J. Randall, and J. R. Brett. Academic Press, New York. pp. 161-260.

HAGEN, N. T. 1983. Destructive grazing of kelp beds by sea urchins in Vestfjorden, northern Norway. Sarsia, 68: 177- 190.

HIMMELMAN, J. H., and D. H. STEELE. 197 1. Foods and predators of the green sea urchin Strongylocentrotus droebachiensis in New- foundland waters. Mar. Biol. (Berlin), 9: 3 15-322.

HOOPER, R. 1980. Observations on algal-grazer interactions in Newfoundland and Labrador. Can. Tech. Rep. Fish. Aquat. Sci. 954: 92-1 19.

JOBLING, M. 198 1 . Mathematical models of gastric emptying and the estimation of daily rates of food consumption for fish. J. Fish. Biol. 19: 245-257.

JONSSON, G. 1982. Contribution to the biology of catfish (Anarhichas lupus) at Iceland. Rit Fiskideildar, 6: 2-26.

KEATS, D. W. 1986. The effects of the experimental removal of green sea urchins, and of ice-scour on sublittoral benthic macro-algal communities in eastern Newfoundland. Ph.D. thesis, Memorial University of Newfoundland, St. John's.

KEATS, D. W., G. R. SOUTH, and D. H. STEELE. 1985a. Reproduction and egg guarding by Atlantic wolffish (Anarhichas lupus: Anarhi- chidae) and ocean pout (Macrozoarces americanus: Zoarcidae) in Newfoundland waters. Can. J . Zool. 63: 2565-2568.

1985b. The ecology of juvenile green sea urchins (Strongyloc- entrotus droebachiensis) at an urchin dominated sublittoral site. In Proceedings of the Fifth International Echinoderm Conference, Galway, Ireland, 24-29 September 1984. Edited by B. F. Keegan and B. D. S. O'Connor. A. A. Balkema, Boston, MA. pp. 295-302.

1986. Where do juvenile Atlantic wolffish live? Can. Field- Nat. In press.

MACDONALD, J. S., K. G. WAIWOOD, and R. H. GREEN. 1982. Rates of digestion of different prey in Atlantic cod (Gadus morhua), ocean

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

SAV

AN

NA

HR

IVN

AT

LA

BB

F on

11/

11/1

4Fo

r pe

rson

al u

se o

nly.

KEATS ET AL. 1925

pout (Macrozoarces americanus) and American plaice (Hippoglos- soides platessoides). Can. J. Fish. Aquat. Sci. 39: 65 1-659.

MANN, K. H. 1977. Destruction of kelp beds by sea urchins: a cyclical phenomenon or irreversible degradation. Helgol. Wiss. Meere- sunters. 30: 455-467.

MILLER, R. J. 1985a. Succession in sea urchin and seaweed abundance in Nova Scotia, Canada. Mar. Biol. (Berlin), 84: 275-286.

1985 b. Seaweeds, sea urchins, and lobsters: a reappraisal. Can. J. Fish. Aquat. Sci. 42: 2061-2072.

MOORE, D. S., and R. J. MILLER. 1983. Recovery of macroalgae following widespread sea urchin mortality with a description of the nearshore hard-bottom habitat on the Atlantic coast of Nova Scotia. Can. Tech. Rep. Fish. Aquat. Sci. 1230: 1-94.

SCHEIBLING, R. E. 1984. Echinoids, epizootics and ecological stability in the rocky subtidal off Nova Scotia, Canada. Helgol. Wiss. Meeresunters. 37: 233-242.

SIVERTSEN, K., and A. BJORGE. 1980. Reduction of algal vegetation in Helgeland coastal waters. Fisken Havet, 4: 1-9.

TEMPLEMAN, W. 1984. Stomach contents of the Atlantic wolffish, Anarhichas lupus, from the Northwest Atlantic. NAFO SCR Doc. 84/VI/12, Ser. No. N785.

VERIGINA, I. A. 1974. The structure of the alimentary canal in some of the northern Blennioidei. I. The alimentary canal of the Atlantic wolffish (Anarhichas lupus). J. Ichthyol. (Engl. Trans1 .), 14: 954-968.

WHARTON, W. G. , and K. H. MANN. 1981. Relationship be- tween destructive grazing by the sea urchin (Strongylocentrotus droebachiensis), and the abundance of American lobster, Homarus americanus, on the Atlantic coast of Nova Scotia. Can. J. Fish. Aquat. Sci. 38: 1339-1349.

Can

. J. Z

ool.

Dow

nloa

ded

from

ww

w.n

rcre

sear

chpr

ess.

com

by

SAV

AN

NA

HR

IVN

AT

LA

BB

F on

11/

11/1

4Fo

r pe

rson

al u

se o

nly.