NOAA Technical Report NMFS 42 September 1986

Effects of Temperature on

the Biology of the Northern Shrimp,

Panda/us borealis,

in the Gulf of Maine

Spencer Apollonio

David K. Stevenson

Earl E. Dunton, Jr.

U.S. DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

National Marine Fisheries Service
NOAA TECHNICAL REPORT NMFS

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I. Synopsis of biological data on the Blue Crab, Callinectes sapidus Rathbun, by

Mark R. Millikin and Austin B. Williams. March 1984, 39 p.

2. Development of hexagrammids (Pisces: Scorpaeniformes) in the Northeastern

Pacific Ocean, by Arthur W. Kendall, Jr., and Beverly Vinter. March 1984, 44 p.

3. Configurations and relative efficiencies ofshrimp trawls employed in southeastern

United States waters, by John W. Watson, Jr., Ian K. Workman, Charles W. Taylor,

and Anthony F. Serra. March 1984, 12 p.

4. Management of nonhern fur seal, on the Pribilof Islands, Alaska, 1786-1981, by

Alton Y. Roppel. April 1984, 26 p.

5. Net phytoplankton and zooplankton in the New York Bight, January 1976 to

February 1978, with comments on the effects of wind, Gulf Stream eddies, and slope

water intrusions, by Daniel E. Smith and Jack W. Jossi. May 1984, 41 p.

6. Ichthyoplankton survey of the estuarine and inshore waters of the Florida Everglades, May 1971 to February 1972, by L. Alan Collins, and John H. Finucane. July

1984, 75 p.

7. The feeding ecology ofsome zooplankters that are important prey items of larval

fish, by Jefferson T. Turner. July 1984, 28 p.

8. Proceedings of the International Workshop on Age Determination of Oceanic

Pelagic Fishes: Thnas, Billfishes, and Sharks, by Eric D. Prince (convener and editor),

and Lynn M. Pulos (editor). December 1983, 211 p.

9. Sampling statistics in the Atlantic menhaden fishery, by Alexander J. Chester.

August 1984, 16 p.

10. Proceedings of the Seventh U.S.-Japan Meeting on Aquaculture, Marine Finfish

Culture, Tokyo, Japan, October 3-4, 1978, by Carl J. Sindermann (editor). August 1984,

3l p.

II. Taxonomy of Nonh American fish Eimeriidae, by Steve J. Upton, David W.

Reduker, William L. Current, and Donald W. Duszynski. August 1984, 18 p.

12. Soviet-American Cooperative Research on Marine Mammals. Volume I-PinDi'

peds, by Francis H. Fay, and Gennadli A. Fedoscev (edilors) September 1984. 104 p.

13. Guidelines for reducing porpoi,e mortality in tuna purse seining, by Jamb M

Coe. David B. Holts, and Richard W Butler. September 1984, 16 p.

14. Synopsis of biological data on sh,)nnose 'turgeon, AciperlSer brevirostrum LeSueur

1818, by Michael J. Dadswell, Bruce D. Tauben, Thomas S. Squiers, Donald Marchette, and Jack Buckley. October 1984, 45 p.

15. Chaetognatha of the Caribbean sea and adjacent areas, by Harding B. Michel.

October 1984, 33 p.

16. Proceedings of the Ninth and Tenth U.S.-Japan Meetings on Aquaculture, by Carl

J. Sindermann (editor). November 1984, 92 p.

17. Identification and estimation of size from the beaks of 18 species of cephalopods

from the Pacific Ocean, by Gary A. Wolff. November 1984, 50 p.

18. A temporal and spatial study of invenebrate communities associated with hardbottom habitats in the South Atlantic Bight, by E. L. Wenner, P. Hinde, D. M. Knott,

and R. F. Van Dolah. November 1984, 104 p.

19. Synopsis of biological data on spottail finfish, Diplodus hulbruoki (Pisces:

Sparidae), by George H. Darcy. January 1985, II p.

20. lchthyoplankton of the Continental Shelf near Kodiak Island, Ala,b, by Arthur

W. Kendall, Jr., and Jean R. Dunn. January 1985, 89 p.

21. Annotated bibliography on hypoxia and its effects on marine life, with emphasis

on the Gulf of Mexico, by Maurice L. Renaud. February 1985, 9 p.

22. Congrid eels of the eastern Pacific and key to their Leptocephali, by Solomon

N. Raju. February 1985, 19 p.

23. Synopsis of biological data on the pinfish, Lagodon rhomboides (Pisces:Sparidae),

by George H. Darcy. February 1985, 32 p.

24. Temperature conditions in the cold pool 1977-81: A comparison between southern

New England and New York transects, by Steven K. Cook. February 1985, 22 p.

25. Parasitology and pathology of marine organisms of the world ocean, by William

J. Hargis, Jr. (editor). March 1985, 135 p.

26. Synopsis of biological data on the sand perch, Diplectrum formosum (Pisces:

Serranidael, by George H. Darcy. March 1985, 21 p.

71. PrOCeedings of the Eleventh U.S.-Japan Meeting on Aquaculture, Salmon Enhancement, Tokyo, Japan, October 19-20, 1982, by Carl J. Sindermann (editor). March 1985.

102 p. .

28. Review of geographical stocks of tropical dolphins (Stenella spp. and Delphinus

delphis) in the eastern Pacific, by William F. Perrin, Michael D. Scott. G. Jay Walker,

and Virginia L. Casso March 1985, 28 p.

29. Prevalence, intensity, longevity, and persistence of Anisakis sp. larvae and LacisIOrhynchus tenuis metacestodes in San Francisco striped bass, by Mike Moser, Judy

A. Sakanari, Carol A. Reilly, and Jeannette Whipple. April 1985, 4 p.

30. Synopsis of biological data on the pink shrimp, Pandalus borealis Kr6yer, 1838,

by Sandra E. Shumway, Herben C. Perlons, Daniel F. Schick, and Alden P. Stickney.

May 1985, 57 p.

31. Shark catches from selected fisheries off the U.S. east coast, by Emory D. Anderson, John G. Casey, John J. Hoey, and W. N. Willell. July 1985, 22 p.

32. Nutrient Distributions for Georges Bank and adjacent waters in 1979, by A. F.

J. Draxler, A. Matte, R. Waldhauer, and J. E. O'Reilly. July 1985. 34 p.

33. Marine flora and fauna of the Northeastern United States. Echinodermata:

Echinoidea, by D. Keith Seraf)- and F. Julian Fell. September 1985, 71 p.

34. Additions to a revision of the shark genus Carcharhinus: Synonymy of Aprionodon and Hypoprion, and description of a new species of Carcharhinus (Carcharhinidae),

by J. A. F. Garrick. November 1985, 26 p.

35. Synoptic review of the literature on the Southern oyster drill Thais haemaslOlIla

floridana, by Philip A. Butler. November 1985, 9 p.
NOAA Technical Report NMFS 42

Effects of Temperature on

the Biology of the Northern Shrimp,

Panda/us borealis,

in the Gulf of Maine

Spencer Apollonio

David K. Stevenson

Earl E. Dunton, Jr.

September 1986

U.S. DEPARTMENT OF COMMERCE

Malcolm Baldrige, Secretary

National Oceanic and Atmospheric Administration

Anthony J. Calia, Administrator

National Marine Fisheries Service

William G. Gordon, Assistant Administrator for Fisheries
The National Marine Fisheries Service (NMFS) does not approve, recommend

or endorse any proprietary product or proprietary material mentioned in this

publication. No reference shall be made to NMFS, or to this publication furnished by NMFS, in any advertising or sales promotion which would indicate

or imply that NMFS approves, recommends or endorses any proprietary

product or proprietary material mentioned herein, or which has as its purpose

an intent to cause directly or indirectly the advertised product to be used or

purchased because of this NMFS publication.

ii
Contents

Introduction

Methods 3

Results 5

Temperature measurements 5

Migrations 5

Inshore-offshore migrations 5

Diurnal vertical migration 9

Temperature effects 9

Geographical distribution by season 10

Spawning time 11

Age-at-maturity 12

Food and feeding 12

Growth 12

Sex transition 12

Fecundity 14

Egg parasitism 15

Discussion 16

Correlation between temperature, population size, and landings 17

Offshore habitat preferences 18

Reproductive strategy 18

Effects of temperature on egg production 19

Population fluctuations and management implications 21

Citations 21

HI

Effects of Temperature

on the Biology of the

Northern Shrimp,

Pandalus borealis,

in the Gulf of Maine

SPENCER APOLLONIO

Maine Department of Marine Resources,

State House Station 21,

Augusta, ME 04333

DAVID K. STEVENSON

Center for Marine Studies,

University of Maine,

Orono, ME 04469 and

Maine Department of Marine Resources,

W. Boothbay Harbor, ME 04575.

EARL E. DUNTON, JR.

Maine Department of Marine Resources,

W. Boothbay Harbor, ME 04575

ABSTRACT

Length-frequency data collected from inshore and offshore locations in the Gulf

of Maine in 1966-1968 indicated that ovigerous female northern shrimp (Pandatus borealis) first appeared offshore in August and September and migrated

inshore in the fall and winter. Once eggs hatched, surviving females returned

offshore. Juveniles and males migrated offshore during their first two years of

life. Sex transition occurred in both inshore and oll'shore waters, but most males

changed sex offshore during their third and fourth years. Most shrimp changed

sex and matured as females for the first time in their fourth year. Smaller females

and females exposed to colder bottom temperatures spawned first. The incidence

of egg parasitism peaked in January and was higher for shrimp exposed to warmer

bottom temperatures. Accelerated growth at higher temperatures appeared to

result in earlier or more rapid sex transition. Males and non-ovigerous females

were observed to make diurnal vertical migrations, but were not found in near~

surface waters where the temperature exceeded 6°C. Ovigerous females fed more

heavily on benthic molluscs in inshore waters in the winter, presumably because

the egg masses they were carrying prevented them from migrating vertically at

nigh!.

Northern shrimp were more abundant in the southwestern region of the Gulf

of Maine where bottom temperatures remain low throughout the year. Bottom

trawl catch rates were highest in Jeffreys Basin where bottom temperatures were

lower than at any other sampling location. Catch rates throughout the study area

were inversely related to bottom temperature and reached a maximum at 3°C.

An increase of 40% in fecundity between 1973 and 1979 was associated with

a decline of 2-3°C in April-July offshore bottom temperatures. Furthermore, a

decrease in mean fecundity per 25 mm female between 1965 and 1970 was linearly related to reduced landings between 1969 and 1974. It is hypothesized that

temperature-induced changes in fecundity and, possibly, in the extent of egg mortality due to parasitism, may provide a mechanism which could partially account

for changes in the size of the Gulf of Maine northern shrimp population during

the last thirty years.

INTRODUCTION-----------

The northern or pink shrimp, Pandalus borealis Kr¢yer, supports

sizeable otter trawl fisheries throughout much of its range within

boreal and sub-arctic waters of the northern hemisphere. In 1980,

a total world catch of 164,000 metric tons (mt) of pandalid shrimp

was reported, of which 35 % came from the northeast Atlantic, 25 %

from the northwest Atlantic, and 27% from the northeast Pacific

(FAG 1981). Total world catch doubled between 1970 and 1980

and increased by 19% between 1979 and 1980 (FAG 1976, 1981).

Major pandalid shrimp fisheries (60% P. borealis in 1980) are conducted on the west coast of North America from California to

Alaska, in the Canadian maritime provinces, on the west coast of

Greenland, and in the Norwegian and North Seas (Balsiger 1981).

In the Atlantic, P. borealis reaches its southernmost limit in the

Gulf of Maine where it has supported a commercial fishery ofsome

importance for the last four decades. Historically, the Gulf of Maine

shrimp fishery has been characterized by marked variations in annual

landings. In the first 17 years after statistics were first systematically

recorded (1938), landings were modest and reached a maximum

of 255 mt in 1945 (Fig. 1), but declined thereafter. No landings

were recorded during 1954-57, even though fishermen continued

to look for shrimp. The fishery revived in 1958 and, beginning in

1962, landings increased dramatically every year, reaching a peak

of 12,800 mt in 1969 (Table 1). Maine fishermen accounted for

nearly all landings in the Gulf during 1940-68 and for 72 % of total

landings during the height of the fishery (1966-75). Maine landings peaked at 10,990 mt in 1969 (Fig. 2). Harvesting efforts in

Maine have traditionally been directed at the capture of egg-bearing

females which migrate inshore in the winter. Massachusetts

fishermen began harvesting shrimp on a large scale in inshore and

offshore waters in 1969. A gradual decline in landings which began

after 1972 accelerated rapidly in the mid-1970s; less than 1000 mt

a year were landed in 1977, 1979, and 1980. (The fishery was closed

completely by regulation in 1978.) Catches exceeded 1000 mt per

year after 1980, reaching 3900 mt in the winter of 1984-85 (Table 1).

Examination of catch, catch-per-unit-effort (CPUE), and annual

mean sea-surface temperatures during the period of rapid growth

and decline of the fishery (Fig. 3) indicate that increased catches

in the late 1960s were preceded by a rapid increase in population

250

_ 200

'"

c

;:

Ul 150

t.?

Z

0

Z 100

<{

--'

50

0

1935 1955 1960

Figure I.-Annual Maine landings of Panda/us borealis, 1938-59.
12,--------------- ---,

8

1970 1975

13

'. 30 .

.:'.\ 12

"1 ,

( ~, LANDINGS II

, \, 10

\ -= , 9 , 0 , 2.0 8 c . 0

'.-+,;" '" 7 Q , 0 +. , :;; (/) \ 6 '"' \ 2

.€ 5 0 UJ 2

<l

10 ::;) ...J Q. 4 u

CPUE

1965

YEA RS

1955

3

:LTO~TI---rl,'-fr:....r;·...,··--r-r-,--,-,r-r---r....,-,-,-,-,---r-l-_---I

2

1960

1965 1970 1975 !980 1985

YEAR S

Figure 2.-Annual Maine landings of Pandalus borealis. 1960-85.

2

oL---;"'"""i'==;:==;--.,,,,---,-,-,-.,-r'--'-T

1960

c

o

"Q

10

(/)

6

o

2

<l

4

size (as inferred from CPUE data). Catch remained high from 1969

to 1972 despite a fairly dramatic reduction in population size. The

rapid increase in population size in the mid-1960s was preceded

by a drop of 3°C in mean annual sea surface temperatures in the

late 1950s. The relation of these three variables after 1969 is not

quite so clear, but the implication is that both fishing pressure and

temperature changes may affect population size.

Dow (1977) reported a significant negative correlation between

annual mean surface temperatures at Boothbay Harbor. Maine, and

the log of shrimp landings 4 years later for the period 1939-671•

Earlier attempts by Dow (1963, 1964, 1966) to forecast shrimp landings in the Gulf of Maine were based on an assumed 2-year lag

between spawning and exploitation, according to length-at-age

information reported by Rasmussen (1953) for P. borealis in Norway. He was handicapped, however, by the lack of specific biological data for the Gulf of Maine population, particularly the ageat-maturity and the age-at-first-capture. It was to provide specific

information on life history characteristics, to relate them if possible to changes in temperature, and to provide a sound biological

basis for managing the increasingly valuable winter shrimp fishery.

that in 1966 Maine's Department of Sea and Shore Fisheries (now

the Maine Department of Marine Resources), in cooperation with

the U.S. Bureau of Commercial Fisheries (now the National Marine

Fisheries Service), undertook a study of Pandalus borealis in the

Gulf of Maine.

The objective of this study was to examine various aspects of

the biology of P. borealis in the Gulf of Maine and their relation

to temperature in order to determine what biological mechanisms

could explain how temperature changes affect population abundance

and therefore, indirectly, the commercial catch. This paper presents

the results of work conducted between 1966 and 1968 on migrations, seasonal distributions, growth rates, sex transition, spawning times, feeding habits, and egg production and survival in relation to water temperatures recorded when samples were collected

'Dow, in subsequent articles published in Fishing News lmemarional in 1981 and

1985, reported a correlation coefficient of -0.950 between annual mean Boothbay

Harbor sea surface temperatures and log landings 4 yr later for a shorter period,

1949-68. It was not stated whether or not this strong negative correlation was statistically significant.

Figure 3.-Mean annual 1950-73 sea surface temperatures (lagged 4 years) at

Boothbay Harbor, Maine, total 1962-77 catch, and 1964-77 catch-per-unit-effort

(CPUE) data estimated from commercial landings of 34-50 GT vessels in

Gloucester and Portland for which shrimp accounted for 50% or more ofthe catch.

Sources: Temperature data from Welch and Churchill (1985); catch and CPUE

data frum Schick et al. (1981).

Table I.-Commercial landings (metric tons)

of northern shrimp in the Gulf of Maine, by

state, 1958-85.

Year Maine N.H. Mass. Total

1958 2 0 2

1959 5 2 8

1960 40 I 41

1961 30 I 31

1962 160 16 176

1963 244 10 254

1964 419 3 423

1965 947 8 955

1966 1,738 18 II 1,766

1967 3,141 20 10 3,171

1968 6,515 43 52 6,610

1969 10,993 58 1,773 12,824

1970 7,713 54 2,902 10,670

1971 8,355 51 2,724 11,129

1972 7,516 75 3,505 11,095

1973 5,477 60 3,868 9,405

1974 4,431 37 3,477 7,945

1975 3,177 30 2,080 5,287

1976 617 7 398 1,022

1977 148 2 237 387

1978

1979 33 2 451 487

1980 70 5 257 332

1981 529 5 538 1,071

1982' 853 22 659 1,531

1983' 892 46 460 1,399

1984'b 2,395 31 525 2,951

1985'b 2,946 216 968 4,131

Source: Diodati et al. (1985).

'Landings computed on a seasonal basis,

e.g., 1982 includes December 1981, but not

December 1982.

bpreliminary estimates.

2
and to long-term trends in monthly and annual sea surface and bottom temperatures. Considerable emphasis was placed on the interrelationship between temperature and migrations, since migratory

behavior was believed to be a reproductive strategy with important management implications.

Previous studies of the biology and ecology of P. borealis have

been conducted by a number of workers: Wollebaek (1903) and

Hjort and Ruud (1938) in Norway, Rasmussen (1953) from southern Norway to Spitsbergen, Horsted and Smidt (1956) in Greenland, Allen (1959) in the North Sea, Butler (1964) in British Columbia, and Haynes and Wigley (1969) in the Gulf of Maine.

Reviews have been published by Butler (1971), Balsiger (1981),

and, most recently, by Shumway et aI. (1985).

METHODS _

Sampling from the chartered vessel Draggin Lady began in the early

summer of 1966 in inshore waters and on a few offshore grounds

such as Jordan Basin and Jeffreys Basin (see Table 2 and Figure

4). In the winter of 1966-67, stations 1 and 2 were sampled twice

a month and both sides of Jeffreys Ledge (stations 5 and 6) were

sampled once in midwinter. In the summer of 1967, a larger number of offshore areas were sampled several times. As the work progressed, it became obvious that more extensive and more frequent

sampling was necessary. Therefore, in the winter of 1967-68, sampling was carried out approximately once a month as weather permitted at stations 1-6: two additional samples were collected at station 7. ·In the summer of 1968 the same schedule was continued

at stations 1-6, and stations 7-12 were added to the monthly program. This expanded sampling program was carried out from June

Table 2.-Sampling locations for Pandalus borealis in the

Gulf of Maine, 1966-68.

Station Depth

no. Location (m) Latitude Longitude

I Cuckolds Light 60 43° 45' 69° 39'

2 10 miles south of

Boothbay Harbor 128 43° 34' 69° 35'

20 miles south of

Boothbay Harbor 165 43° 26' 69° 32'

4 West of Plalls Bank 178 43° 09' 69° 55'

5 West of

Jeffreys Ledge 165 43° 03' 70° II'

6 East of

Jeffreys Ledge 211 43° 02' 69° 55'

7 East of Three

Dory Ridge 188 43° 10' 69° 13'

West of

Fippennies Ledge 180 42° 44' 69° 31'

9 West of Cashes Ledge 192 42° 57' 69° 02'

10 Northeast of

Cashes Ledge 183 43° 03' 68° 53'

II 20 miles south of

Ml. Desert Rock 174 43° 37' 68° 03'

12 23 miles southeast of

Ml. Desert Rock 240 43° 38' 67° 51'

30'

30'

50 Km

70° 30' 69°

MATINICUS

~/IS.

50F

30' 68°

·~MT. DESERT.

ROCK

II 12 ,

30' 67°

30'

44°

30' 30'

,3

i

I••

67°

u· ,,~~ ...:-....._ ";"

..

I....

30'

,

r":

_,,' ;,.,'-----=':' ",,~:::::;;:::z:.. OJ ~~~~~ .,U

3 DORY RIDGE

\' . c' .7

,8 -'I

FIPPENNIES

LEDGE

30' 70° 69° 30'

JEFFREYS

LEDGE

I ,4

I PLATTS

BANK

1.... ~JEFFREYS /,\:'J BASIN

30'

43°

Figure 4.-Shrimp sampling locations in the Gulf of Maine in 1966-68 (see Table 2).

3
through September 1968. Occasionally, supplementary samples

were taken by the Draggin Lady in other inshore and offshore areas

or from commercial catches by Boothbay Harbor fishermen. (Commercial catches were sampled only to estimate the percentage frequency of normal and parasitized eggs carried by female shrimp.)

Beginning in the spring of 1967, continuous vertical temperature

recordings were made with a bathythermograph at each station except Cuckolds each time a sample was collected. The U.S. Bureau

of Commercial Fisheries made frequent measurements at Cuckolds

and, through the courtesy of Dr. 1. J. Graham, those data were

used in this study.

All shrimp samples aboard the Draggin Lady were collected using

a semiballoon otter trawl with a 7.6 m (25 ft) head rope and 9.4

m (31 ft) foot rope, with 38 mm (1. 5 in) mesh in the body, and

a cod end with 32 mm (1.25 in) mesh covered with a 13 mm (0.5

in) mesh liner. The net was fished from a single wire with 92 m

(100 ft) bridles. Towing speed was approximately 2 knots and all

tows lasted approximately 30 minutes. When catches were large,

four subsamples of about 100-125 shrimp were collected at random from the entire catch as it lay on the deck, preserved in 5%

formalin, and returned to the laboratory for analysis. For small

catches, all shrimp were saved. Total catches were recorded only

as estimated volume, not as numbers or weight.

Vertical migratory behavior was studied by deploying baited

shrimp pots at different depths. Successful experiments were conducted in Jeffreys Basin in August 1967, in the Sheepscot River

in March 1968, and at the 20-mile station in May and July 1968.

In each case, pots were hauled periodically and the contents of each

pot removed, sexed, and counted. The pots used were the same

design as those described by McBride and Barr (1967).

Shrimp were measured to the nearest O. 1 mm from the posterior

edge of the eye socket to the extreme posterior lateral edge of the

carapace in the manner of Horsted and Smidt (1956) and Allen

(1959;. (Measurements reported by Rasmussen (1953), Butler

(l96L), and Haynes and Wigley (1969) were made to the posterior

dorsal edge of the carapace.) Total lengths were measured to the

nearest millimeter from the tip of the rostrum to the posterior edge

of the telson. A total length (TL)/carapace length (CL) conversion

factor was derived from a linear regression model relating TL to

CL for 486 shrimp from four different samples2 . Length data were

compiled as total length frequency distributions (10 mm groups),

but [he original carapace measurements were used for fecundity

analyses and to estimate mean size-at-age. Sex was determined by

noting the conditions of the endopods of the first and second pair

of pleopods as described by Rasmussen (1953) and Allen (1959).

Stomach contents were removed from approximately 200 male,

transitional, and female shrimp within each sample and examined

under a dissecting microscope. Generally, the stomach contents of

O-group shrimp were not examined. Occasionally, when there was

little difference in stomach contents between individual shrimp, only

100 stomachs from a sample were examined. The contents ofstomachs which were not empty were grouped in the broad categories

of I) mud, including debris and unrecognizable material, 2)

polychaete remains, 3) pelycypod and gastropod shells, 4) crustacean remains, and 5) foraminifera. Individual shrimp were placed

in a single category since, with very few exceptions, their stomachs

were either empty or contained a single predominant type of food.

'The ratio (slope) of total length to carapace length was 4.95, a value which was

intermediate between those for Greenland (4.6-4.7. Horsted and Smidt 1956) and for

the North Sea (5.05, Allen 1959).

4

In order to describe size increments in general terms which

ignored possible spatial or temporal variations in growth rates, we

selected from each calendar month when samples were collected,

regardless of the year or sampling location, the length frequency

data which showed the most distinct, readily-separable size group

or groups. Mean lengths for each identifiable size group were

calculated from length frequency data, and mean, maximum, and

minimum lengths for each size group were plotted as a function

of the presumed age of the size group. The same approach was used

by Haynes and Wigley (1969). For size groups which overlapped

at intermediate lengths, half of the number of length measurements

in the intermediate length class were assigned to each adjacent size

group. Age determinations were based on an assumed I March birth

date3 . It was further assumed that each clearly defined size group

was composed of only one age group, and, since P. borealis

reproduces once a year, that each of these age groups represented

a year-class. (All references to the age ofsize groups in this report

will be to age groups, i.e., O-group, I-group, etc.). In order to avoid

problems caused by the overlap between older size groups, growth

was estimated only for shrimp in their first 3 years of life. No attempt was made to fit a growth curve to mean length-at-age data.

For fecundity studies, all eggs were removed from each ovigerous

female and weighed. Eggs collected in 1966 were weighed fresh

while those collected in 1968 were preserved in 5% formalin before

weighing. For each set of annual data, total egg weights were converted to total egg numbers by means of a linear regression equation which related egg number to egg weight for subsamples from

individual egg masses removed from females collected at different

locations and sampling dates during August and/or September of

each year4 • Estimated total egg numbers were verified by directly

counting all the eggs from a few females and comparing those counts

with total estimated egg counts. Allen's (1963) criteria were used

to describe stages of egg development. Size-specific fecundity was

estimated for shrimp collected during individual sampling occasions

at individual stations during the fall of 1966 and 1968. A composite

fecundity vs. size relationship was established by combining all data

(N = 202) for nine separate tows made in eight different locations

in August and September 1968.

In this study, we describe the migrations of individual age groups

within and between years and the spatial distribution (inshore vs.

offshore) of different age groups at different times of year. Both

approaches were used in order to determine the movements of an

age group ofshrimp at different stages during its life cycle as well

as the spatial distributions of different age groups in the population

at given points in time. Migratory behavior was inferred by visually

comparing length frequency histograms compiled from data collected at inshore and offshore stations during various times of year.

It is recognized that the use of percent sample frequency data rather

than numerical density data (e.g., numbers ofshrimp per size group

caught per tow) increases the risk of making incorrect interpretations of migratory activity. To minimize this problem, the results

reported in this study were based as much as possible on interpretations of gross changes in sample length frequency data. In some

cases, reference is made to the effects of presumed increases or

decreases in the density of one size group (such as would result

from migratory movements) on the percent frequency of other size

groups in length frequency sample data.

]This birthdate was based on annual surveys ofshrimp larvae in the Sheepscot River

during early February to early April, 1978-82, reported in Stickney (1982).

4In 1968, subsamples were removed from the egg masses of 24 individuals collected in five different locations in August and September, and a statistically linear

regression equation (Y = 367 + 1037 X) was derived where X equals weight in grams.
6

5

JEFFREYS EAST ---------------'-_.-_0_.__._._._.--. (6)

f------------------------.------------

6

5

4 _.--------_._-----------._------......._/----- WEST OF PLATTS

(4 )

20 MILES

( 3) W

0:

::>

I-

<t

0:

W

0..

"

W

I5

4

3

2

6

5

4

3

2

I

/ -....... JEFFREYS WEST

_ _____------ IS)

--.---- -_........... / .--

I ._~~~- ./

-"",/--.------/'-,-----------1

_ . __.-J/-. 10MILES

--------~--- / (2)

-----.-----------\ /.--. .~/._-_.-./

1967

M A

1968

o N

CUCKOLDS

(I)

Figure 5.-Annual variations in bottom

temperature at certain sampling locations

in the Gulf of Maine, 1967-68 (see Table

2, Figure 4). Station numbers in parentheses.

RESULTS _ 3 4 6 8 9 10

a

--' a

----' ......---. ,/

/ S of MT_ DESE RT

i JUNE 10,1968 "

" (II)

1

'.

'\,

/

I 20 MI LES I

1 JU N E 13, 1968

//./ (3)

,I

\

\\

'\

./'

./ JEFFREYS WEST ! ./

I JUNE 13, 1968

/ 15)

T

!

f

1

180

150

120

90

60

z

- 150

30

90

180

150

120

60

3

I

t 180

w

o 30

(fl 60 a:

w

I- 90 w

::;; 120

Temperature measurements

Bottom temperature data collected during this study (Fig. 5) showed

a larger annual variation for inshore coastal waters than for offshore locations. Furthermore, inshore bottom temperatures more

closely reflected seasonal changes than did the offshore temperatures which lagged behind the calendar seasons by about 5 months.

In general, the annual variation in bottom temperatures decreased

and the maximum occurred later in the year as the distance offshore increased. Minimum offshore bottom temperatures were

recorded in late spring and early summer, and during the summer

were 2° -3°C colder than in inshore waters. In the winter, inshore

waters were 2° -3 °C colder than offshore water where the annual

maximum temperature was recorded in late December. Bottom

temperatures recorded throughout 1967 and 1968 west of Jeffreys

Ledge were lower than at offshore stations on Platts Bank and east

ofJeffreys Ledge, except in December and January. There was considerable variation in surface and bottom temperatures, the degree

of temperature stratification, and the minimum temperature depth

between different sampling locations in the Gulf (see, for example, Figure 6). The greatest degree of temperature stratification was

recorded in August each year in the area around Jeffreys Ledge,

particularly west of the Ledge in Jeffreys Basin. The lowest bottom temperatures recorded during this study generally occurred at

stations with the greatest degree of thermal stratification.

Migrations

2 3 4 5 6 7 8 9 10

TEM PERATURE 'c

Inshore-offshore migrations-It is convenient, in describing the

migrations of individual age groups, to begin in the winter of

1967-68 with the smallest (30-50 mm TL) size group which represented 40-45 % of the catch at Cuckolds and 5%or less ofthe catch

in the offshore locations (Fig. 7). These small shrimp were assumed

to be a O-group shrimp which hatched the previous spring (1967

year class). A few O-group shrimp belonging to the 1967 year class

Figure 6.-Vertical temPerature distributions at three sampling locations

in the Gulf of Maine in June 1968'(see Table 2, Figure 4). Station numbers

in parentheses.

5
50 50 CUCKOLDS CUCKOLDS

40 40

67

30 67 30

20 20 66

10 10

160 20U 80 120 160 200

50 50 50

10 MILES 10 MILES 10MILES

40 40 ,10

66

30 30 30 64

64

20 64 20 20

10 10 10 67 67

40 80 /20 160 200 40 40 120 160 200

50 50 50 20MILES 20 MI LES 20 MILES

40 40 40

30 30 30

65 66 65 64 65

UJ 20 20 20

-'

a. 10 10 10 ::E 67

<I

<J)

40 40 80 u. 40 80 120 160 200 120 160 200

0

I- WEST OF PLATTS 50 WEST OF PLATTS z 50 50 UJ WEST OF PLATTS u 40 40 65 40 <>:

UJ

a. 65 30 30 30

20 20 ., 20 66

10 10 10

67

40 80 120 160 200 40 160 200 40 160 200

50 50 50

JEFFREYS EAST JEFFREYS EAST JEFFREYS EAST

40 40 40

65 65 30 65 30 30 ..' 66

20 20 66 20

/0 10 10

6(;

40 80 120 160 40 80 120 160 200 40 160 200

TOTAL LENGTH (mm 1

Figure 7.-Length frequency distributions for Panda/us borealis sampled at inshore and offshore locations in the Gulf of Maine: from left to right, 30 Oct. -14

Nov. 1967,21-27 Dec. 1967, and 31 Jan.-l Feb. 1%8. 1963-67 year classes are labeled in cases where they were clearly identifiable. White = juveniles and

males; stippled = transitionals; black = females.

moved offshore during their first year, appearing at the 20-mile

station in November and late December and between Platts Bank

and Jeffreys Ledge (stations 4 and 6) in early February. These results

clearly indicated that most O-group shrimp remain within 20 miles

of the coast. The presence of a few O-group shrimp at stations 4

and 6 in early February (Fig. 7) indicated that some shrimp migrate

as far as 40 miles offshore during their first year.

The offshore migration ofsmall juvenile and male shrimp which

begins during an age group's first year of life continues during its

second year. The 1967 year class accounted for a rapidly growing

proportion of the inshore samples collected in the spring of 1968;

it included 70 % of all shrimp collected at Cuckolds in March and

May and >95% in June (Fig. 8). (The increasing percentage of

O-group shrimp in the samples collected later in the 1967-68 sampling period undoubtedly reflected their increasing retention in the

half-inch mesh sampling gear.) Inshore samples collected in the summers of 1966 and 1967 were composed almost entirely of I-group

shrimp (Fig. 9). Evidence for an offshore migration of I-group

shrimp was provided by length frequency data collected during the

summers of 1967 and 1968 (Figs. 10, II) and the winter of 1967-68

(Fig. 7). These data showed that I-group shrimp (50-80 mm TL)

accounted for up to 25 % of the offshore summer samples, but were

generally <10%. Percentages of I-group males (70-90 mm TL) were

higher in offshore samples collected in the winter of 1967, reaching

15-35 %, and reflected their increasing displacement from inshore

to offshore waters as well as the inshore migration of ovigerous

females. Shrimp belonging to the 1966 year class remained at

Cuckolds through May oftheir second year, but were almost gone

by June (Fig. 7).

Based on the above information alone, one would conclude that

the offshore migration of males (and juveniles), which begins in

an age group's first year, is completed by its third summer. Interpretation of length frequency data for the older age groups, however, casts doubt on this conclusion. Shrimp belonging to the 1965

year class were present as 2 and 3-group shrimp at most inshore

and offshore sampling locations during the 1967-68 sampling season

(Figs. 7, 8) and at offshore stations during the summers of 1967

and 1968 (Figs. 10. II). On some occasions, however, this year

6
67

50 67 50 CUCKOLDS 50

CUCKOLDS 67 CUCKOLDS

400 40 40

30 30 30

20 20

10 10 10

63

160 200 160 200 40 80 120 160 200

50 50 50

10 MILES 10 MILES 40 40 40 10 MILES

30 66 30 30

20 20 64 20 67 66

10 10 10 63

w 160 200 40 80 120 160 200 40 160 200

--' "-

::;:

<l 50

1 50 (/) 20 MILES 20 MILES 40 40 40 "'- 20 MILES 0 66 30 30 30 66 >--

z 20 20 64 20

a:

u

w

/0 10~ 10

w

"- 160 200 40 80 120 160 200 40 160 200

50 WEST OF PLATTS 50 50 WEST OF PLATTS WEST OF PLATTS

40 40 40

30 66 65 30 30

66

20 0' 20 20

10 10 10

160 200 40 160 200 40 80 160 200

50 50 50

40 JEFFREYS EAST JEFFREYS EAST 40 JEFFREYS EAST 40

66 30 64 65 30 65 30

20 " 20 2 66 65

10 10 10

40 160 200 40 40 80 200

Figure 8.-Length frequency distributions for Panda/us borealis sampled at inshore and offshore locations in the Gulf of Maine: from left to right, 5-6 March 1968,

14-15 May 1968, and 12 June-I July 1968. 1963-67 year classes are labeled in cases where they were clearly identifiable. White = juveniles and males; stippled = transitionals; black = females.

class could not be distinguished from younger and/or older year

classes. A significant percentage of the 2 and 3-group shrimp belonging to this year class which were sampled during 1967-68 were in

various stages of sexual transition; thus, length frequency data for

this year class, particularly data collected in May at Cuckolds and

at Platts and Jeffreys East in June (Fig. 8), included male, transitional, and female shrimp. The identity of the 1965 year class was

further obscured by overlap with length frequency data for the 1964

year class in some samples. On the occasions when the 1965 year

class was clearly distinguishable, it made up approximately 40-60%

of the Platts and Jeffreys East samples and also accounted for a

significant proportion of the shrimp collected at 10 and 20 miles.

A small proportion of the shrimp which were collected at Cuckolds

in late December and early February apparently belonged to this

year class. If so, the offshore migration of younger shrimp was

not completed by the third summer, since a few 2-group shrimp

remained in inshore waters, and, judging by the presence of transitional individuals, changed sex during their third winter. The alternative hypothesis is that offshore migration is indeed completed by

the third summer (note the almost complete absence ofshrimp >80

mm TL in inshore waters in the summers of 1966 and 1967 in Figure

9), and that shrimp >100 mm TL at Cuckolds in the winter represented transitionals and females which migrated offshore as males

or juveniles sometime during their first 2 years of life and then

returned inshore. Such a migration is inferred for the females based

on the interpretation of length frequency data for the 1964 year class,

but not for transitionals.

Even though it was not possible to determine from these data at

what time of year sex transition begins, it is clear that it begins

in the third year of life and continues into the fourth year. It also

takes place in both inshore and offshore waters. The low proportion of transitional individuals at Cuckolds, however, and their increased proportions in the offshore samples (Figs. 7, 8, 10, II)

indicated that most sex transition takes place following the offshore

migration of the males. Transitional shrimp appeared in length frequency data either as 2 or 3-group shrimp during 1967-68.

7
66

50 CUCKOLDS

40

50

NASH I. 30

40 1966 20

30

10 20

10 40 80 120 160 200

-,

40 80 120 160 200

50 JEFFREYS WEST

50 40

SCHOODIC

40 1966 30 65 64 w 20 30 --'

a.

20 ::< 10 <t 66

10 Ul

I "- 40 80 120 160 200 0

40 80 120 160 200 fZ 50 WEST OF PLATTS w w 65

50 u

0:: 40

2 CUCKOLDS w

a. <l 40 1967 30 Ul

"- 30 20 0

20 I- 10 Z 10 66 w

l u

0:: 40 80 120 160 200 w 40 80 120 160 200 "'-

50 WEST OF CASHES LEDGE 50

CUCKOLDS 40 64

40 1966

30

30

20

20

r 1 10

10 63

40 60 120 160 200 40 80 120 160 200

TOTAL LENGTH (mm) TOTAL LENGTH (mm)

Figure 9.-Length frequency distributions for I-group juvenile and

male Panda/us borealis sampled in various inshore waters during

the summers of 1966 and 1967. White = juveniles and males;

stippled = transitionals; black = females.

Figure to.-Characteristic length frequency distrihutions for Panda/us borealis collected in the summer of 1967 from four distinct

inshore and offshore areas in the Gulf of Maine. Clearly identifiable

year classes are labeled. White = juveniles and males; stippled =

transitionals; black = females.

The 1964 year class was represented at all sampling locations

as 3-group females in the winter of 1967-68 and in May and June

1968 as 4-group females (Figs. 7, 8). The proportion of females

collected at Cuckolds, 10, and 20 miles in March was very low.

Females were present offshore in the summers of 1967 and 1968

(Figs. 10, 11), but were entirely absent from inshore stations in

the summers of 1966 and 1967 (Figs. 9, 10). Some of the smaller

females that appeared after March were presumably new 3-group

(1965 year class) females which underwent sex transition during

the winter and spring. Most of the females which spawned during

1967 belonged to the 1964 year class (age 3) but there were also

a few older (1963 year class) females collected at Cuckolds and

10 miles in March. At least some of these older females were

presumed to be repeat spawners which spawned originally in 1966.

An inshore spawning migration of females during the winter was

deduced from the observed changes in the proportions of females

sampled at the various sampling locations visited during 1967-68

(Figs. 7, 8, 10, 11). Female shrimp belonging to the 1964 year

class accounted for 50% of the Jeffreys East sample in November.

The relative abundance of this age group at this location declined

dramatically to <10 % in late December and early February, partially in response to the arrival of I-group shrimp from inshore

waters. Meanwhile, the percentage of 4-group females remained

stable at Platts and 20 miles throughout the winter, but increased

at 10 miles from November through February (at the same time

that I-group shrimp were diminishing in importance). There was

no discernible change in the percentage of females at Cuckolds between late December (no sample was collected in November) and

May. The low proportions of 3-group females at the inshore station was in large part due to the large numbers of 0- and I-group

shrimp in the samples. By June, however, there were almost no

females at Cuckolds. No females were collected inshore in either

the summer of 1966 or 1967 (Figs. 9, 10). The absence of females

from Platts and Jeffreys East in March and their reappearance in

8
1967 1968

200

200

200

160

160

160

JEFFREYS 'WEST

JULY 31

WEST OF PLATTS

AUG 21

120

120

120

66

'I

40 80

40 80

I WEST OF CASHES

JULY 17

65

L----,----,--,--rbdlrl

40 80

TOTAL LENGTH (mm)

160 200

WEST OF CASHES

64 JULY 12

80 120

66

40

63

40 80 120 160 200

JEFFREYS WEST

AUG 7

65 64

66

40 80 120 160 200

WEST OF PLATTS

AUG 10

50

40

30

20

10

w

-' 50 "-

::;;:

<1 40 Ul

lL 30 0

f- 20

z

w 10 u

0::

W

"-

50

40

30

20

10

Figure n.-Length frequency distributions

for Pandalus borealis collected in offshore

areas of the Gulf of Maine in the summers

of 1967 and 1968. Clearly identifiable year

classes are labeled. White = juveniles and

males; stippled = transilionals; black = females.

May (Fig. 8) are attributed to both the return offshore migration

ofsurviving "spent" females (1964 year class) and the sexual transition of younger (1965 year class) shrimp in the spring,

Diurnal vertical migration-No shrimp were taken at any depth

in Jeffreys Basin in August during daylight hours, but immediately after sunset a few shrimp were caught at 180 m; by midnight,

large numbers of shrimp were caught between 45 and 120 m at

temperatures of 3°-4°C (Fig. 12). Shrimp were caught from 45

m to the bottom at 0400 hours. At no time were any shrimp caught

in the upper pot (25 m). Except for one female, all the shrimp caught

were males. Females captured in bottom trawls at the same time

of year had full ovaries and were on the verge of spawning.

Females were caught in pots also fished at 9 m intervals on March

20-21 1968 in 83 m of water in the Sheepscot River. The maximum number was taken in the pot nearest the surface at midnight.

Females caught in the pots had shed almost all their eggs, but a

substantial number in a bottom trawl sample still retained eggs. A

total of only three males were caught in pots and a trawl sample

showed there were few males present on the bottom.

Male, transitional, and female shrimp were caught in pots fished

at 18 m intervals in 165 m of water 20 miles south of Boothbay

Harbor on 13-14 May 1968. Once again, the largest number was

taken near the surface at midnight. Two similar trials in July 1968

at the same location showed that males, transitionals, and females

rose toward the surface at night, but the thermocline was well

developed and, as in August 1967, no shrimp were taken in the

nearsurface waters where temperatures were higher than 5-6°C.

It appeared that isothermal conditions permitted males and nonovigerous females to reach surface waters in March and May, but

that the well developed thermocline in July and August limited the

upward migration of male and female shrimp.

These observations indicated that male shrimp carry on nocturnal vertical migration throughout the year, and that female shrimp

migrate through the water column when not carrying eggs. Since

the egg mass on the swimming legs must be a handicap in swimming, it is not surprising that ovigerous females do not migrate far

from the bottom. Lack of vertical migration by females, rather than

lack of attraction to baited pots, is the likely explanation for absences of females in these vertically deployed pots, since females

were feeding at the time of these trials.

Temperature effects-Our results showed a correlation between

temperature and the horizontal and vertical migrations of P. borealis

in the Gulf of Maine. Some shrimp migrate offshore during their

first year oflife; others remain inshore until sometime during their

second or third years of life. During the inshore phase of the life

cycle, they are subjected to a wide range of temperatures. Mean

monthly bottom temperatures at Cuckolds in 1967-68, for instance,

varied from 1° to 9°C, whereas bottom temperatures recorded at

offshore stations ranged from 2° to 6°C (Fig. 5). Similarly, the

daily vertical migrations of shrimp collected in August 1967 were

limited to temperatures of not more than 5-6°C (Fig. 12). These

data suggest that northern shrimp, after a certain stage in their life

cycle, are less tolerant of warmer temperatures. Avoidance of

warmer temperatures by older shrimp which have migrated offshore is also indicated by results which showed an inverse relation

between relative catch rates and bottom temperatures between 1.5°

and 6°C in June and July 1968 (Fig. 13): highest catch rates in

July were obtained at 3°C. (No attempts were made to fit a linear

9
:3 4 5 6

BOTTOM TEMPERATURE,oC

2

JUNE /968

0 5 0

:3

00 0 0 0

I 0 0

JULY /968 0

0

0 0 0

0 0

I

0 0

4

2

7

6

5

4

2

:3

7

6

o

la:

w

a.

a.

::E

ii'

:I:

(/)

LL

o

(/)

w

i=

lZ

«

:::>

o

w

>

i=

«

..J

w

a:

TEMPERATURE ° C

3 4 5 6 7 8 9 10 II 12

• 5 SHRIMP

_ 10 SHRIMP

_ 20 SHRIMP

40 SHRIMP

0

POT DEPTH

15 .-----. /.----- G

30

45 I e

60 i

i e :::1' 75 / :I:

l- / 90 a. I 0 w

0

i 105

I 0 120 i 135 \ El \ 150 \

\ e 165

180 I I I e

16 20 00 04 08

HOURS

8 AUGUST 9 AUGUST

Figure 12.-Vertical distributions of Pandalus borealis and temperature profile

in Jeffreys Basin in August 1967. Widths of bars indicate number ofshrimp caught

per pot at hour indicated.

Figure B.-The relation between bottom temperature and the relative quantities

of Pandalus borealis collected at all sampling locations in the Gulf of Maine, June

and July 1968.

regression to these data since there was no reason to suspect that

catch rates continue to increase below 3°C.)

In their third winter, after mating, male shrimp remain offshore

and undergo transition to female shrimp. In 1967-68, bottom temperatures in offshore waters in midwinter did not generally fall below

4-5°C, and remained 2-3°C warmer than in inshore waters (Fig.

5); thus, the majority of the transitional shrimp were concentrated

in the warmest areas to be found at that time of year. The inshore

migration of ovigerous females in the late fall and early winter may

be triggered by declining bottom water temperatures in some offshore locations, such as west of Jeffreys Ledge (Fig. 5); in other

offshore locations (Platts, Jeffreys East), however, bottom temperatures remain more or less constant throughout the year. Whatever

the role temperature changes may play in stimulating inshore and

offshore migrations of P. borealis in the Gulf of Maine, one of

the consequences of the inshore spawning migration is that eggbearing females and hatching larvae are exposed to colder bottom

water temperatures (I ° -2°C) than exist elsewhere in the Gulf during the winter and early spring.

Geographical distribution by season

In the summer, the smallest age group (I-goup) was found almost

exclusively inshore (Figs. 9, 10). These young shrimp were found

offsqore only in small numbers, in most cases not exceeding 10%

of the offshore samples. The samples from Three Dory Ridge (Fig.

14) showed what appeared to be the typical change in age composition offshore during the summer and early fall. Similar conclusions were drawn from data collected at other offshore locations

(e.g.. stations 6, 8, and 9), although size distributions from different locations did not always show the same patterns at the same

time. Offshore samples early in the summer tended to be dominated

by 3-group transitionals and 4-group females. As the summer progressed, however, 2-group males made up a growing proportion

of the samples, reflecting their continuing offshore migration that

began in the previous winter, until they dominated samples taken

at the end of the summer. At most offshore stations during the summer, I-group shrimp either were not collected at all or made up

a relatively small percentage of the samples (Figs. 10, 11, 14).

Three size groups dominated inshore samples collected during

the winter and early spring at Cuckolds (Figs. 7, 8), as compared

with inshore summer samples which contained, almost exclusively, I-group male shrimp (Figs. 9, 10). As many as five age groups

may have been present at Cuckolds in the winter of 1967-68. Most

of these shrimp were males (or juveniles), but some were also transitionals and females. Two size groups of females were present in

March, presumably 4 and 5-group shrimp (1 March birthday)

belonging to the 1963 and 1964 year classes. As noted previously,

the growing percentage of O-group shrimp at Cuckolds during the

winter was believed to be a consequence of increasing retention

of smaller shrimp in the trawl as they grew larger, as well as a

continuing offshore migration of I-group males, the winter mortality (partly from fishing) of ovigerous females, and the return offshore migration of the surviving females which no longer carried

eggs.

10
AUGUST 1968

SEPTEMBER 1967

SEPTEMBER 1968

'Since these samples were processed, McCrary (1971) has described a more reliable

method for distinguishing between non-ovigerous females which have or have not carried eggs previously. based upon the presence or absence of slernal spines.

of 2-group males during the summer and fall and the absence of

females in February. These changes reflect the same migratory

movements of males and females noted previously.

Spawning time

10

L_c!-:-~~~~~-----!--::----:'-:c--+::--+-:-=--::'---:!-::--' 32 3.4 36 3.8 40 4.2 .4.4 4.6 48 50 52 54 5b ~8

TEMPERATURE,oC

The timing of egg extrusion appears to be influenced by prevailing

water temperatures. Eggs first appeared on the pleopods of some

females collected in mid-August 1966, 1967, and 1968 at various

sampling locations. The percent of ovigerous females in samples

from different locations varied from <5% to 55% in August 1968

and exceeded 90 % for all but two samples in September of the same

year (Fig. 15). The data indicated that the time of egg extrusion

was inversely related to bottom water temperature: the predicted

frequency of ovigerous females in August declined from 40% at

3.6°C to 20% at SoC. In September, over 90% of the females collected at stations with bottom temperatures <SoC were ovigerous.

Of all the females collected at all stations in August 1968 and

September 1967, a significantly larger percentage of those < 150

mm TL were ovigerous than were females >150 mm TL (66.1 %

vs. 61.3% in September, and 30.1 % vs. 20.6% in August). Females

<150 mm TL were presumed to be a year younger than females

> 150 mm TL (see the March 1968 length frequency data in Figure

8)5. The data therefore suggest that the older (5-group) females

90

80

70

60

50

<fl

W 40 ..J

<I

::; 3U w

u..

<fl 20

::J

0

a::

w

'"> IUO

0

u.. 90

0

I- 80

z

w

u 70 a::

w

Q. GO

5(J

40

30

20

200

200

160 200

160 200

JULY 17

JANUARY 18

JUNE 12

AUGUST 20

SEPTEMBER 18

65

65

65

FEBRUARY 28

66

66

66 65

40

40

40

40

40

40 80 120 160 200

TO TAL L E NG TH (mm)

50

40

30

20

50

40

30

20

50

40

10

10

10

40

30

20

30

20

10

so

10

IZ

W

u 50 a::

40

30

20

50

40

30 Q.

::l; 2 ..

lI) 10

"-o

Three size groups were also present in samples from a number

of offshore stations during the summer and winter, but the summer samples were dominated by the older size groups (Figs. 10,

II) and the winter samples by the two younger groups (Fig. 7).

This difference in age composition is attributed to the continuous

offshore migration of males and the inshore migration of females

in the fall and winter. At Three Dory Ridge, on the other hand,

most of the shrimp collected between January and September (Fig.

14) belonged to two size groups (rather than three). Aside from

changes in the mean size due to growth, the major changes between

winter and summer at this station were the increasing importance

Figure 14.-Length frequency distributions for Pandalus

borealis sampled east ofThree Dory Ridge (station 7) on

various dates in 1968. Clearly identifiable year classes are

labeled. White = juveniles and males; stippled = transitionals; black =:' females.

Figure 15.-The relation between bottom temperature and the relative abundance

of ovigerous female Panda/us borealis from various locations in the Gulf of Maine,

August 1968 and September 1967 and 1968. Linear regressions for September

were fit by eye; the regression for August was calculated.

II
spawned later than the younger (4-group) females. The time delay

in spawning between the two age groups could not be estimated.

Age-at-maturity

Length frequency data compiled for male, transitional, and female

shrimp during this study (Figs. 7, 8, 10, 11, 14) suggested that

P. borealis in the western Gulf of Maine mature and spawn for

the first time as females in their fourth year. As indicated by sample length frequency data for March and May 1968 (Fig. 8), some

females apparently survive their fourth birthday to spawn a second

time during their fifth year. Clearly, however, the majority of the

females sampled during this study matured for the first time during their fourth year. It is not known if sex transition is delayed

for some individuals until the fifth year; if so, this would also account for the presence ofthe older age group of females in inshore

waters in the spring.

Food and feeding

Most of the shrimp stomachs examined in this study were either

empty or contained mud, or mud and unrecognizable debris. The

percent of empty stomachs in all samples varied between 3% and

67% (commonly 20-40%); stomachs with only mud, or mud debris,

were found in 8-55% of the shrimp examined (commonly 30-40%).

Polychaete remains were found in up to 15 % of the stomachs examined in anyone sample, but most commonly occurred in 3%

or less of the stomachs examined. Generally, less than 1% of the

stomachs examined contained foraminifera as the major food item.

There was a significant seasonal variation in the consumption of

the two major food items (Table 3): molluscs (primarily benthic

species) predominated in the winter while crustaceans (primarily

pelagic species) formed most of the food in the spring and summer. There were no clear differences in the fall. Diet also depended

on location. From the end of December 1967 through early March

1968, there were significant differences in the proportion ofshrimp

feeding on molluscs and crustaceans at Cuckolds and 20 miles:

14.2 % of the stomachs contained shells at the inshore station and

4% at the offshore station, while 9.6% contained crustacean remains offshore and 5 % inshore.

Table 3.-Seasonal differences in the relative abundance (percent occurrence)

of shells and crustaceans in the stomachs of Pandalus borealis in the Gulf of

Maine, 1966-68.

1966 1967 1968

% % % % % %

Season shells crustaceans shells crustaceans shells crustaceans

Winter 16.9 8.8 13.1 9.9

Spring 7.4 14.6 5.7 15.0

Summer 5.7 18.4 2.9 11.5 2.5 13.9

Fall 14.1 13.4 9.\ 9.2 6.8 4.5

The difference in the relative abundance of shrimp feeding on

molluscs and crustaceans at inshore and offshore stations in the

winter was attributed to differences in feeding habits offemale and

non-female shrimp rather than differences in availability of the two

food sourres. Significantly more females (15.6%) collected at

Cuckolds and 20 miles in the winter of 1967-68 contained mollusc

shells than did non-females (5.5 %). Since females and non-females

12

were present at both stations in the winter (Fig. 7), the possible

effect of prey availability at the two locations was ruled out. A more

plausible explanation is that since female shrimp are bearing eggs

in the winter, and since they do not migrate vertically when ovigerous, they are restricted to benthic food. Non-females migrate vertically and thus are less likely to feed on benthic molluscs. Females

presumably resume feeding in the water column once the eggs hatch,

thus explaining why the entire population shifts from a predominantly benthic (molluscan) diet in the winter to a pelagic (crustacean)

diet in the spring and summer.

Growth

Size-at-age estimates compiled from 1966-68 length frequency data

(Fig. 16) revealed a three-fold increase in length from an age of

7 months through the end of the third year. Growth was much more

rapid in the first 2 years (12 and 9 mm CL, respectively) than in

the third year (3 mm CL), and was more rapid during the fall

(October-November) and the spring (May-July) than during the

winter or summer. Rapid growth in the fall was associated with

maximum bottom water temperatures at inshore and offshore locations (Fig. 5).

Differences of approximately 1-2 mm CL (5-10 mm TL) were

evident in length frequency data for the same age groups sampled

at different locations in the spring and summer of 1968 (Figs. 17,

18) and in March 1967 and 1968 west ofJeffreys Ledge (Fig. 19).

Comparison of water temperatures recorded at different depths at

Three Dory Ridge and west of Jeffreys Ledge 4 months prior to

collection (Fig. 18) and west of Jeffreys in May of 1967 and 1968

(Fig. 20) revealed that increased size-at-age is correlated with higher

temperatures and suggested that growth is positively related to

temperature.

Sex transition

Length frequency data collected from Jeffreys West in March 1967

not only provided evidence for more rapid growth compared with

March 1968 data, but also showed an increased proportion oftransitional and female shrimp (Fig. 19). Bottom temperatures were

1°C warmer in May 1967 than in March, April, or May 1968 (Figs.

18, 20). These results suggested that either the rate of sex transition was reduced or sex transition was delayed at lower temperatures, and that the increased percentage of transitional and female

shrimp was associated with increased growth rates at higher temperatures.

The same conclusion was reached after comparing the proportion of transitional shrimp on the east and west sides of Jeffreys

Ledge in the spring of 1968. In April of that year the bottom water

on the east side of the Ledge was about 3°C warmer and the whole

water column between 50 and 140 m was approximately 1°C

warmer than on the west side (Fig. 20). The percentage frequency

of transitional shrimp east of the Ledge was significantly greater

on two occasions during March and April 1968 (29.9% vs. 19.7%

in March, and 19.3% vs. 10.7% in April). Similar differences in

the proportion of transitional and female shrimp west of Jeffreys

Ledge and east of Three Dory Ridge in July 1968 were positively

associated with a 1°C difference in spring water temperatures

between 80 and 180 m (Fig. 18). In contrast, the difference in the

proportion of transitionals sampled during March 1968 between

Platts Bank (26.3%) and east ofJeffreys Ledge (29.9%), two locations where temperature differences were small, was not significant.
26 130

E 24 120

.s 22 -110

I E

f- 20 E 100

'"

z 18 I 90 w f16 '" 80 w z u w 70 tt 14 -' « 12 --' a:: « 60 « f- U 10 0 50 f8 40

30

4

F'! j 1 lsi YEAR 2nd YEAR

n--II jIr~'1 III

3'd YEAR

3 4 6 7 8 9 10 II 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36

AGE IN MONTHS

! 1 4 5 6 7 8 9 10 II 12 2 3 4 5 6 7 8 9 10 II 12 2 3 4 5 6 8 9 10 II 12 2 3

A M J J A S 0 N D F M A M J J A S 0 N D F M A M J A S 0 N D F M

CALENDAR MONTHS

Figure 16.-Pandalus borealis mean length-at-age and growth history for the first three years of life estimated from length frequency data collected at various

locations in the Gulf of Maine during 1966-68. Periods of more rapid growth are indicated by dashed lines.

230

Figure 17.-The growth of 2-group Pandalus borealis at three locations in the

Gulf of Maine in the spring and summer of 1968.

Figure 18.-Panda/us borealis length frequency distributions

and year classes from west ofJeffreys Ledge and east of Three

Dory Ridge in July of 1968 with vertical temperature profiles

from the same two locations in February and March ofthe same

year.

50 JEFFREYS WEST

40 JULY 18,I96B

30 65

w 20

-'

a. 10 ::<

«

en 200 LL 40 160

0

fz 50 THREE DORY RIDGE w

u 40 JULY 17,I96B a:

w

a. 65 30

20

10

67

40 80 120 160 200

TOTAL LENGTH (mm)

TEMPERATURE (0 C)

0 I 2 3

20 if 40

60 i\

I

\

E \

80 \

i i

I I

I f- lO i , a.

w I

a 120 I

\ i

I

140 !

I I

160

IBO

20

_. - JEFFREYS WEST

MARCH 6,1968

THREE DORY RIDGE

FE8RUARY 28,1968

15

SEP

15

AUG

15

JULY

15

JUNE

15

MAY

15

APR

21.0

19,0

E

E

w

u

«

a.

« 20,0 a:

«

u

I 22,0

f-

'"Z

'W

13
MARCH 20 1967

Fecundity

Figure 19.-Length frequency distributions and year classes of

Pandalus borealis coUected west ofJeffreys Ledge in March 1967

and 1968.

66

TOTAL LENGTH (mm)

Linear regressions were fitted to nine sets of fecundity data compiled for eight different locations in August and September 1968,

but covariance analysis revealed that among locations within each

month neither intercepts nor slopes were significantly different. The

predicted mean fecundities of intermediate-sized (30.25 mm CL

or 150 mm TL) shrimp were greater (P < 0.10) in August west

and east of Jeffreys Ledge than at 20 miles or Fippennies (Table

4). In September, 150 mm TL shrimp collected from Three Dory

Ridge were more fecund (P < 0.10) than shrimp of the same size

from Cashes Ledge, but not from west of Jeffreys and two other

locations. There were no differences in fecundity between samples

for smaller or larger shrimp in either month, even at the 90% confidence level. These weak differences in fecundity between locations could not be correlated with differences in bottom water

temperatures during the period of egg development (May-August).

The apparent difference in predicted mean egg numbers for 150

mm TL shrimp collected west of Jeffreys Ledge between August

(1875) and September (1740) was not significant even at P = 0.10,

nor was the difference between August 1966 (1980) and August

1968 (1875).

Results of fecundity estimates for all ovigerous shrimp (N = 202)

collected in 1968 were quite variable: there was as much as a twofold

difference in observed egg numbers among individual shrimp of

a given length. Despite this variability, statistically significant (P

< 0.05) linear and log linear regressions were fitted to the combined data set. Predicted mean egg numbers (linear model) ranged

from 1,000 for 25 mm CL (124 mm TL) females to 2,400 for 35

mm CL (173 mm TL) females (Fig. 21).

200

160 200

160

65

66

MARCH 61968

67

40

40

50

40

10

30

20

w 30

-'

a.. 20

10

[La

fz

50

40 a..

TEMPERATURE, 0 C

234561234 5 6

Figure 20.-Vertical temperature profiles west of Jeffreys Ledge in May 1967

and May 1968 (A) and on each side of Jeffreys Ledge in April 1968 (B).

B Table 4.-Predicted mean number of eggs per 150 mm

TL (30.25 mm eL) female Panda/us borealis collected in

eight different locations in the Gulfof Maine, August and

September 1968.

Figure 21.-Fecundity data for 202 Panda/us borealis collected in eight

different locations in the Gulf of Maine, August and September 1968

(see Table 7) with least squares linear regression model Y = - 2633.9

+ 145.1 X, where X equals lateral carapace length.

Predicted mean number

Location (Station) n of eggsl150 mm female

August

20 miles south (3) 19 1,535

Fippennies (8) 9 1,575

East Jeffreys (6) 18 1.825

West Jeffreys (5) 17 1.875

September

Cashes Ledge (10) 39 1,680

West Jeffreys (5) 50 1,740

Wesl of Platts (4) 23 1,815

10 miles south (2) 12 1.880

3 Dory Ridge (7) 15 1,925

./1"

/ / //.

1/

A

i \ APRIL23,1968

i j

i I

i i

i it-z JEFFREYS EAST

i \

i \ \ . . \

I \

i \ ~F~REYS WEST'\

\

i

./'~

j/

/1

/ I

i i

i i i i~MAY24,1967

i I

i i

i i

i I

i I

i i

I i

) ~MAYI5,1968

!

A

70

60

140

50

170

130

40

160

30

150

10

180

20

z

-100

I

5: 110 LU

o

120

Vl

80

>-

90

14
2600-

3000--,------------------------,

Egg parasitism

'The fact that colder temperatures are associated with slower rates of parasite

development explains why the percentage frequency of infected eggs would be higher

at any point in time on females in colder water (Stickney 1981). Egg mortality may

be more severe in warmer water due to increased parasite development rates.

carried some wllite eggs. In early December, all eggs had reached

the eye pigment stage and 70% of the females carried at least a

few white eggs. At this time, an unidentified stalked and vorticellid

protozoan appeared in 6 % of the egg masses which already included

internally parasitized eggs. On 19 December, a sample from inshore waters contained 87% females with some white eggs, and

15 % of the egg masses containing white eggs were also infested

with the stalked protozoan. Off Platts Bank on 21 December 1967,

30-40% of the females sampled carried some white eggs, but no

vorticellids were found. On 27 December, close inshore, 46% of

the females carried eggs infested with vorticellids.

By late December it was obvious that many females were carrying fewer than the expected number of eggs. Egg loss was attributed

in part to the continuous proliferation of internal parasites and

perhaps also to the increased incidence of the external (vorticellid)

protozoans, although the effect of the vorticellids on egg viability

is unknown. Vorticellid infestation and internal parasitism appeared

to peak in January; a sample from inshore waters on 19 January

1968 showed 49% females with internally parasitized eggs, and 61 %

of these were infested with protozoans. At the same time, egg losses

appeared to be reduced.

White eggs and vorticellid infestations were still observed during February and March 1968, but at reduced incidence; a sample

taken inshore on 5 February showed 12% females with white eggs,

and 10% of these were also infested with external protozoans. At

this time, most of the non-parasitized eggs had reached early stage

4 with about a month of development remaining. A few females

had shed almost all their eggs, and these invariably had many protozoans attached to the pleopods. On 29 February, 2% carried white

eggs and 4% of these carried protozoans. In mid- and late March,

both afflictions were extremely rare.

It is clear that ovigerous shrimp migrating inshore from October

through December in 1967 and 1968 moved from colder to warmer

waters (see Figure 5). Average offshore fall bottom temperatures

were about 4° -5°C, while inshore fall bottom temperatures reached

7°C at Cuckolds and probably higher further inshore. The development of egg parasites may be associated with this rise in temperature encountered during inshore migration. There was an apparent relationship in late December 1967 and in November and

December 1968 between bottom water temperatures and the percentage of females with externally parasitized eggs collected in

various locations (Table 5). It appeared that there was little or no

infestation at temperatures of 5.5°C or less, and considerable infestation (3-48%) at temperatures above 5.5°C. The highest incidence ofinfestation occurred at temperatures of 7° -9°C. A clear

relation between external egg infestation and temperature was not

evident after December 1967 when inshore bottom temperatures

dropped rapidly, but it is very likely that infested eggs which were

still being carried by female shrimp after December had been infested earlier when temperatures were higher. The progressive

reduction in infestation and the nearly total absence of parasitized

eggs in February and March, when low temperatures prevailed,

support this hypothesis.

The same sequence of events, i.e., the development of internal

egg parasites in ovigerous shrimp migrating into inshore waters

followed by infestations of the egg mass by epizoic vorticellids and

egg loss was again observed in the following year (October to

December 1968). The effect was apparently even more intense than

in 1967, possibly as a result of the warmer inshore water temperatures which prevailed in 1968 (see Figure 5).

..

:

,///

/

'/.

° / • • 0 .... 0

0 ° // • •

. -.; .~ .~.: . o. ~.y

. ;·o·b>o o' -.. . .. ::.-.

i?o~;: ..::..... . . .

-_... -.- - . . . -: ..- . . ..

/.

21500-

1l00-

lIJ.OO2000-

2200

2~OO

1200-

1000-

Once eggs are spawned, they are susceptible to infestation by a

number of epizoic organisms (e.g., ftIamentous bacteria, suctorians,

and peritrich protozoa) which attach externally to the egg mass and

by an internal peridinian dinoflagellate parasite (Stickney 1978).

This internal parasite causes egg mortalities which are indicated

by the appearance of large, white (or opaque) eggs.

Two ovigerous females were collected 7 August 1967 in Jeffreys

Basin. By the first half of September, many females collected in

offshore waters were ovigerous. Egg development, then in stage

I, appeared normal on all females examined. By early October,

when 99 % of all females were ovigerous and when eggs were in

early Stage 2, large, opaque eggs appeared in the egg masses and

the proportion ofsampled females carrying infected eggs was progressively higher further west along the coast, increasing from 23 %

of all females examined south of Matinicus Island to 63 % in Jeffreys Basin (see Figure 4). Although temperature measurements

were not made at these locations in October 1967, this trend was

inversely related to the usual trend in fall bottom water temperatures which generally decline by 1° _2°C from east to west along

the Maine coast (Colton and Stoddard 1973)6. In late October, all

egg development had reached Stage 2 and, while the proportion

of females with at least a few white eggs west of Platts Bank remained between 40% and 50%, the proportion of females at the

20 mile station carrying internally parasitized eggs increased from

30% early in October to 83 % at the end of the month.

In mid-November, as females moved to within 10 miles of the

coast (station 2), about 6% of the eggs sampled at that location had

reached the eye pigment stage and 73 % of the ovigerous females

C)

w 1800 .......

C>

«: 11500

1500-::2rll--.-----=2L15--.-----=2Le-,----:gT:o--.---g,-2---,r--g..-l.I---,r----jge

CARAPACE LENGTH fHHl

15
Table s.-Bottom temperatures and percent of female

Panda/us borealis with epizoic protozoans on their

eggs at various locations in the Gulf of Maine,

1967-68.

Station Temp. % females

no. Date (0C) with infested eggs

5 7 Nov. 1968 4.3 0

6 6 Nov. 1968 4.4 0

4 6 Nov. 1968 4.9 0

3 27 Dec. 1967 4.9 I

4 3 Dec. 1968 5.0 1

6 3 Dec. 1968 5.1 0

4 21 Dec. 1967 5.2 0

6 21 Dec. 1967 5.3 0

7 18 Jan. 1968 5.5 0

5 21 Dec. 1967 5.6 6

3 27 Dec. 1967 5.9 5

3 19 Dec. 1968 6.8 4

1 27 Dec. 1967 7.1 46

1 19 Dec. 1968 7.2 48

2 19 Dec. 1968 7.4 8

2 21 Nov. 1968 8.1 3

1 21 Nov. 1968 8.6 40

DISCUSSION _

The results of this work have revealed several important life history

characteristics of the northern shrimp population in the Gulf of

Maine which are affected by temperature and provide some basis

for predicting how low temperatures might possibly stimulate

population growth. Attention has focused on several factors which

affect the reproductive potential of this population, i.e., migratory

behavior, egg parasitism and mortality, spawning times, growth

rates, and the timing and/or rate of sex transition.

In further examining the effects of temperature on various life

history characteristics of Pandalus borealis, a great deal may be

inferred from studies carried out in other locations. Two of the most

fundamental characteristics which have been shown by a number

of authors to vary over the geographic range of the species are

growth and longevity. In general, growth in more northern latitudes is slower than in more southern latitudes. Totallength-at-age-2

estimates reported by Rasmussen (1953), for example, for the islands

of Jan Mayen and Spitsbergen, were 30-35 mm lower than in the

North Sea (Allen 1959) and southern Norway (Rasmussen 1953),

and 50 mm lower than in British Columbia (Butler 1971) and the

Gulf of Maine (Haynes and Wigley 1969 and this study). Maximum

age also varies with geographic range from 3 years in the North

Sea (Allen 1959) to 7 V2 years or older in Spitsbergen (Rasmussen

1953). The estimated maximum age for P. borealis in the Gulf of

Maine is 5 years (Haynes and Wigley 1969 and this study).

A comparison of estimated ages at first spawning made by various

authors (Butler 1964; Allen 1959; Rasmussen 1953; Poulsen 1946;

Squires 1965; Horsted and Smidt 1956) for P. borealis populations

exposed to different average annual bottom water temperatures at

different geographical locations (Fig. 22) revealed that slower growing, longer lived shrimp in arctic waters mature as females at older

ages than those in more temperate waters. According to the functional (logarithmic) relationship used to describe the relationship

between age at first spawning and temperature (Fig. 22), a reduction of only 2°C (from 4.5 to 2.5°C) could delay maturity from

age 3 to age 4 and thereby increase generation length by 1 year.

16

The range of annual mean fall bottom water temperatures reported

by Davis (1978) for the Gulf of Maine for the period 1963-75 was

3°C (5.7°-8.6°C): a maximum change of 1°C was reported between consecutive years during this same period. The annual range

of mean spring bottom temperatures during the period 1968-75 was

about 1.5°C with a maximum change ofO.8°C. Evidence presented

in this report does suggest that growth rates and the rate or onset

of sex transition of northern shrimp in the Gulf of Maine do vary

according to temperature, but it is not known whether the temperature changes reported by Davis are sufficient to also affect the age

at which females mature.

An inverse relation between temperature and time of spawning

has been reported by Allen (1959) and Haynes and Wigley (1969).

In the cold waters of Spitsbergen and Greenland (average annual

bottom temperatures of 1° -3°C), spawning occurs in July and

August, but in the North Sea (average 8° -9°C), it occurs in October. Butler (1964) noted that females in the warm waters of British

Columbia (average >9°C) begin to spawn in mid-November. The

inverse relation between the time of spawning and temperature in

different geographical areas throughout the range of P. borealis

and in different areas within the Gulf of Maine in the same season

both support the hypothesis that colder temperatures favor earlier

spawning. Nunes (1984), on the other hand, reported that P. borealis

held in the laboratory at ambient Gulf of Alaska temperatures (annual mean of 6.3°C) spawned almost 2 months earlier than P.

borealis held at 2°_3°C and 8°-9°C.

Inshore-offshore migrations and the separation of the life cycle

into inshore and offshore components have been reported in British

Columbia (Berkeley 1930), Norway (Wollebaek 1908; Hjort and

Ruud 1938), Korea (Kim 1966), and West Greenland (Horsted and

Smidt 1956). These authors inferred an inshore spawning migration of females into shallower water and an offshore migration of

males from size frequency data collected at different times of year.

Some of these reported movements have been associated with

temperature differences. In one case, the migration of adult shrimp

into fjords on the west coast of Greenland was confirmed directly

by tagging studies (Horsted 1969).

I

6i- • • • £.

.4

IN y ~1.90691·0 t 1875

I SPITSBERGEN

2 w. GREENLAND

3 S, GREENLAND

.. MIST FJORD, NORWAY

5 NEWFOUNDLANQ

6 GULf OF MAINE

7 DENMARK

8 OSLO FJORO,NORWAY

9 NORTHUMBERLAND

10 BRITISH COLUMBIA

4 5 6

TEMPERATURE °c

Figure 22.-The relation between average annual bottom temperature and the

approximate age of first maturity of female Panda/us borealis throughout the

geographical range of the species.
Barr (1970) reviewed published evidence that northern shrimp

leave the bottom and rise into the upper water layers at night. Both

Wollebaek (1903) and Hjort and Ruud (1938) reported the belief

among Norwegian fishermen that shrimp rise offthe bottom at night.

Horsted and Smidt (1956) noted that Greenland fishermen have

observed the same phenomenon and reported taking a few shrimp

well off the bottom at night; they concluded that shrimp probably

migrate in response to the upward movement of prey organisms.

On the basis of catches in vertically-deployed shrimp pots, Barr

and McBride (1967) and Barr (1970) have shown that in Alaska,

P. borealis and other pandalids migrate vertically about 100 m at

night. Diurnal vertical migrations have also been inferred from trawl

catches. Haynes and Wigley (1969) found P. borealis in midwater

trawls at night, but not during the day, while a number of authors

have reported reduced bottom trawl catches at night (Wollebaek

1903; Hjort and Ruud 1938; Horsted and Smidt 1956; Blacker 1957;

Bryzagin 1967). In another study, the relative abundance of eggbearing females in bottom trawl catches was reported to be much

lower during daylight hours when smaller non-ovigerous shrimp

presumably descend to the bottom (Jones and Parsons 1978). These

results and the results ofthis study suggest that the presence of eggs

impedes swimming ability. As was observed for P. borealis in this

study, the vertical migration of P. jordani off the Oregon coast was

limited by a strong thermocline (Milburn and Robinson 1968). In

contrast, Barr (1970) reported that the diurnal vertical migration

of P. borealis in Alaska was unaffected by temperature variations,

either seasonally or vertically.

Observations on the food and feeding behavior of P. borealis

reported in this study were generally confirmed by Wienberg (1981)

who confirmed earlier reports that in the North Sea this species

is omnivorous and feeds on planktonic and benthic prey organisms.

Principal prey were polychaetes, molluscs, and benthic as well as

planktonic crustaceans, although diet composition was a function

of prey availability, time of day, and developmental stage of the

shrimp. During the night, shrimp which migrated vertically fed

mainly on plankton; during the day when shrimp remained on the

bottom, benthic species were ingested. Ovigerous females did not

feed as actively as males.

The results of this study differed from results presented for the

Gulf of Maine by Haynes and Wigley (1969) in two respects. First,

length-at-age data compiled during this study showed rather slower

growth for younger shrimp than did data collected by Haynes and

Wigley. This difference might have resulted from the warmer

temperatures of inshore waters in 1963-65 (Fig. 3) when lengthsat-age for 0 and I-group shrimp collected by Haynes and Wigley

were determined. Secondly, our results did not show a levelingoff of egg numbers for shrimp larger than 160 mm TL (32 mm

CL) as was reported by Haynes and Wigley (1969)7. (Fecundities

estimated by Haynes and Wigley did, however, include a greater

percentage oflarger shrimp than in this study.) More importantly,

fecundities estimated by Haynes and Wigley were considerably

higher at all sizes: a 160 mm TL female carried an estimated 3,000

eggs in 1963-65, and only 2,000 eggs in 1968.

'Figure 8 in Haynes and Wigley was corrected to account for an apparent error

in the conversion from dorsal carapace length to total length.

17

Correlation between temperature,

population size, and landings

Examination of historical Maine landings data (Figs. I, 2) reveals

a period ofincreased landings in the 1940s with an absence of landings in the mid-1950s followed by a much more substantial increase

in landings in the late 196Os. Although no fishing effort data were

collected until 1964, fishermen reported that they continued to look

for shrimp without success during 1954-57 when no landings were

recorded. This information plus the observed changes in catch-perunit-effort (CPUE) in the late 1960s and early 1970s (Fig. 3) suggested that the periods of high and low landings corresponded to

periods of high and low population size. Further evidence for a

reduction in population size since the late 1960s and early '70s was

provided by biomass estimates for the period 1969-79 and annual

trawl survey catch rates compiled since 1968 (Clark et al. 1979;

Diodati et al. 1984).

Since inshore waters in winter are well mixed and generally

isothermal, the monthly sea surface temperatures recorded at Boothbay Harbor are a fair indication of the temperatures to which the

egg-bearing females are exposed following their inshore spawning

migration in the fall. From 1906 to 1949, average monthly sea surface temperatures during January, February, and March of each

year were less than 4°C (Welch and Churchill 1985). After 1954

(with one exception), the average sea surface temperatures for those

months were less than 5°C and, generally (through 1980), less than

4°C. During 1950-53, on the other hand, the average sea surface

temperature at Boothbay Harbor during at least one of the same

3 months was above 5°C (Table 6). Four years later (1954-57),

when shrimp hatched in 1950-53 would have recruited to the commercially exploited population, no shrimp landings were recorded

in Maine. The implication is that record-high inshore winter water

temperatures in 1950-53 were associated with a reduction in the

adult population 4 years later.

There was no clear indication of a relationship between temperature and the dramatic increase and decrease in landings and CPUE

in the late 1960s and early 1970s (Fig. 3). The lack ofsuch a relationship may have been due, at least in part, to the compounding

effect of a tremendous increase in fishing effort after 1967. Anthony and Clark (1980) examined the relationship between population size, temperature, and fishing effort by comparing stock size

estimates obtained from trawl surveys during this period with lagged

annual effort and Boothbay Harbor sea surface temperatures (under

the assumption that temperature and exploitation primarily affect

recruitment 4 years later). They showed that a general decline in

stock abundance between 1969 and 1975 was associated with

Table 6.-Average monthly winter surface-water temperature (OC) at Boothbay Harbor, Maine, and shrimp landings (metric tons) 4 years later. (Temperatures >soC are

underlined).

Shrimp landings

Year January February March 4 years later

1949 3.6 2.2 2.8 17.6

1950 5.7 3.4 3.3 0

1951 6.1 4.1 4.7 0

1952 5.2 4.2 4.2 0

1953 4.7 5.5 6.1 0

1954 4.2 3.5 5.0 2.3

Source: Welch and Churchill (1985).
declining temperatures during 1964-67, increasing temperatures during 1967-69, and relatively stable temperatures in 1969-71. Fishing

effort increased from 500 to 8,000 standard fishing days between

1964 and 1970. The general trend in annual sea surface temperatures

during 1967-75 was upwards from 7.3°-9.4°C (Fig. 3) and was

associated with consistently low estimates ofstock abundance during 1971-79. Fishing effort declined dramatically after 1972 and

remained below 500 standard days during 1977-808.

Offshore habitat preferences

A number ofsurveys (Bigelow and Schroeder 1939; Walford 1948;

Wigley 1960; Haynes and Wigley 1969) concur in showing that

P. borealis occurs in heaviest densities in the summer in the deeper

waters of the western Gulf of Maine, particularly in the vicinity

of Jeffreys Ledge. Bottom trawl surveys conducted by the U.S.

Bureau of Commercial Fisheries in 1967 and 1968 consistently produced large quantities of shrimp in Jeffreys Basin (U.S. Dep. Interior 1967, 1968). Catches made during the course of this study

confirmed these observations: the largest catches were consistently made in Jeffreys Basin. In this study, catch rates during June

and July 1968 were inversely proportional to bottom water temperatures and reached a maximum at 3°C (Fig. 13). A high concentration of shrimp in the Jeffreys Ledge area, particularly west of

the Ledge and in Scantum Basin, was also indicated by bottom trawl

surveys conducted by the Maine Department of Marine Resources

during the period of low shrimp abundance in 1975-78 (Schick et

al. 1980). The fact that this distribution pattern persisted even when

population size was low suggests that it is characteristic ofthe population and persists regardless of changes in population abundance.

The southwestern region of the Gulf provides suitable temperature conditions to support the offshore life stages of P. borealis.

Bottom temperatures are colder in the western sector of the Gulf,

due largely to the persistence of vertical stratification during the

warmer months which limits solar heating to the water mass lying

above the thermocline. Further eastward along the coast, increased

tidal turbulence produces greater vertical instability and more thorough mixing ofsurface and bottom waters throughout the year. Bottom temperatures in the eastern Gulf are therefore slightly warmer

throughout the year than in the western Gulf. In addition, submarine

basins which retain cold bottom waters are much more widespread

in the western sector of the Gulf. Jeffreys Basin is one such area;

bottom temperatures there were considerably colder during the

course of this study than at other offshore sampling locations. Jeffreys Basin and other similar areas in the western Gulf can therefore

be characterized as "refuges" for this boreal species, where conditions for sex transition, reproduction, and perhaps feeding are

superior to other locations in the Gulf. The correlation of shrimp

abundance and the high organic content of sediments reported by

Bigelow and Schroeder (1939), Wigley (1960), and Haynes and

Wigley (1969) may be coincidental rather than causal since partially enclosed submarine basins probably trap both sediments and

cold, dense water.

'Estimates of total fishing effort for the period 1960-74 are from Anthony and Clark

1980; estimates after 1974 were derived from total landings and CPUE data in Diodati

et al. 1984.

18

Reproductive strategy

Several biological characteristics of the northern shrimp population in the Gulf of Maine may be interpreted as mechanisms selected

for maximum egg production. Most importantly, pandalid shrimp

are protandric hermaphrodites; each individual has reproductive

potential which enables the population to exploit favorable environmental circumstances to the maximum limit. In a theoretical treatment of the selective advantages of hermaphroditism, Smith (1967)

noted that synchronous hermaphroditism appears to be more advantageous for short-lived animals. With a somewhat longer life span,

protandric hermaphroditism conveys reproductive advantage over

synchronous hermaphroditism and bisexuality. Thus, northern

shrimp, living from 3 to over 8 years in various locations in the

Atlantic, have evolved the form ofsexual reproduction that results

in the maximum rate of population growth under favorable

conditions.

Warner (1975) developed a model which accounted for agespecific differences in survival and fecundity and examined the adaptive significance ofsequential hermaphroditism in terms of increased

reproductive potential of individuals in the population. He concluded

that the degree ofselection pressure depends primarily on the fecundity schedule of the females: when fecundity increases with age

and individuals mate at random (presumably true for P. borealis),

protandry may confer a selective advantage. Furthermore, when

female fecundity increases rapidly with age and/or when more age

classes are represented in the population, the age of sex transition

is delayed. Warner used survival and fecundity data from Haynes

and Wigley (1969) to correctly predict the age of sexual transition

for the Gulf of Maine P. borealis population9 •

A second feature ofthe reproductive strategy of northern shrimp

in the Gulf of Maine is their migratory behavior. We have demonstrated that the distributions and migratory behavior of northern

shrimp in the Gulf of Maine change with age, i.e., O-group shrimp,

for the most part, remain inshore, I-group shrimp migrate offshore,

2-group shrimp undergo sex transition in offshore waters, eggbearing 3-group females migrate inshore in the fall and winter where

larvae hatch in the early spring, after which some return offshore

to make a second (and possibly a third) inshore spawning migration. Inshore-offshore migrations and the separation of the life cycle

into inshore and offshore components have been reported in British

Columbia (Berkeley 1930), Norway (Wollebaek 1908; Hjort and

Ruud 1938), and West Greenland (Horsted and Smidt 1956).

We conclude that the migratory behavior of P. borealis in the

Gulf of Maine is related to seasonal and inshore-offshore temperature differences. We have suggested that the offshore migration

of maturing male shrimp from inshore waters may be stimulated

by a reduced tolerance for warmer temperatures as shrimp approach

maturity in their second summer. Being a boreal species, P. borealis

in the Gulf of Maine can be expected to avoid bottom water temperatures which exceed those encountered in more northern latitudes, i.e., temperatures >5-6°C. Furthermore, accelerated growth

in warmer offshore waters apparently stimulates earlier (or quicker)

sex transition. Stevenson and Pierce (1985) have shown that fastergrowing PandaIus montagui change sex a year sooner than slower

growing individuals in the same age group. Finally, completion of

egg development during the winter in the coldest prevailing temper-

"It must be realized that both Smith's and Warner's approaches to modeling hermaphroditism deal with genetic reactions to long-term natural selection pressures. Changes

in the timing ofsexual transition maj be under the influence of much more immediate

short-term exogenous factors (e.g., temperature) so that differences are related to

geographic distribution.
Figure 23.-Predicted mean fecundity per 25-mm dorsal carapace length female

P. borealis for selected years during 1964-82; 60 minus mean April-July bottom

water temperatures for offshore stations 3-7 (see Table 2 and Figure 4) for selected

years 1968-82; annual 1967-82 Gulf of Maine landings; and annual 1967-77 catchper-unit~ffort data. Landings and CPUE data were lagged backwards 4 years

to account for the time delay between larval hatching and recruitment. Curves

were drawn by eye. Legend: X = May-July temperatures; (X) = April, June

temperatures. Sources: Fecundity data are from Stickney and Perkins (1981).

Temperature data for 1968-79 from Welch and Churchill (1985), and for 1979

and 1982 from Charles Parker, Bigelow Laboratory for Ocean Sciences. Landings and CPUE data are from Diodati et al. (1984).

place after the number of eggs in the ovaries is determined (i.e.,

factors which might affect the survival rate of oocytes). A field study

clearly cannot be expected to answer all of these questions.

Evidence for a relationship between fecundity and temperature

is provided by comparing previously reported changes in the mean

annual fecundity of 25 mm CL P. borealis in the Gulf of Maine

between 1962 and 1982 with average annual April-July bottom water

temperatures from various locations in the southwestern Gulf of

Maine (Fig. 23). Fecundities were high in the mid-1960s, low in

the late 1960s and early 1970s, and high again in the late 1970s

(Table 7). As a working hypothesis, we propose that the mechanism

controlling long-term variations in fecundity and, perhaps, changes

in population size, is water temperature, or, more specifically, the

magnitude of the temperature difference encountered by maturing

female shrimp during diurnal vertical migration. High fecundities

in the rnid-1960s and late 1970s corresponded with periods of low

April-July offshore bottom water temperatures in the southwest Gulf

of Maine; low fecundities in the late 1960s and early 1970s corresponded with high offshore bottom water temperatures recorded

in the same locations and time of year (Fig. 24). Since vertical

migration is apparently impeded by temperatures >6°C (Fig. 12),

we suggest that high fecundity is associated with a greater positive

differential between 6°C and the observed bottom water temperature, a condition which existed in the late 1960s and late I970s (Fig.

23). A linear regression of fecundity vs. April-July bottom water

temperatures (Fig. 24) showed that a 26% reduction in fecundity

was associated with an increase from 4 ° to 6.25°C in temperature

during the period 1973-82. A similar rate of decline in fecundity

was observed between 1968 and 1969 when May-July bottom water

temperatures were 3.5° and 5°C, respectively (Table 7), although

the data shown in Figure 24 suggested that fecundities were lower

in 1968 and 1969 than in 1973-82 for other reasons.

12

2

4

Q;

+3 "

w

- "~iZ +2

o +1

o oU

-I "'

3.0~

g , ...--CPUE ;::

/\ (-4yrs) "

...11.'\ " \ 2.0 g

, 'o/ \~~•• , '.0

A .~.

• "FECUNDITY • •

,

,

1963 65 67 69 71 73 75 n 79 1981

YEARS

w

"2400

E 2200

~~~~ 1600 ) 1400

1200

1000 ::J

u..

atures in the Gulf may reduce the incidence of egg parasitism and

ensures that the larvae will hatch in more productive inshore waters

during the period of spring plankton blooms.

Effects of temperature

on egg production

A possible effect of temperature stratification on egg production

is explained in a hypothesis proposed by McLaren (1963, 1974)

who argued that an energy bonus accrues to an animal which

migrates upward into warmer water to feed-usually at night-and

then returns to deeper, colder water during the day to assimilate

its food. The mechanism proposed by McLaren to explain the results

of a growth model which predicted higher rates of population increase for copepods (Pseudocalanus minutus) and chaetognaths

(Sagitta elegans) which are exposed to larger temperature differentials (warmer surface water and cooler subsurface water) during

vertical migration is that food is ingested more efficiently in warmer

water and assimilated more efficiently in colder water. The proposed energy bonus acquired through migration and feeding in a

thermally stratified water colurrm would increase reproductive potential by reducing generation length and increasing fecundity. According to McLaren's hypothesis, diurnally migrating animals would

therefore have lower fecundities if the minimum temperature occurs at intermediate depths and high fecundities if thermal stratification is stable (with the minimum temperature at the bottom). Thus,

as noted by McLaren (1974), small-scale vertical temperature

changes and the depth of minimum temperature may be more important than the absolute difference between surface and subsurface water temperatures.

Applying the energy bonus hypothesis to P. borealis in the Gulf

of Maine, it is possible that shrimp which migrate vertically from

colder bottom water into warmer intermediate or surface water to

feed at night and return to the bottom and assimilate their food during

the day have greater energy reserves to devote to growth and/or

egg production. Egg production, expressed as the number of eggs

which are deposited at spawning (fecundity), is in turn a consequence of the number of oocytes which are produced in the ovary

and the percentage which actually survive to spawning, both of

which could be affected by temperature changes encountered during vertical migration.

If the degree of thermal stratification does affect the fecundity

of northern shrimp in the Gulf of Maine, one would expect to find

more fecund females in the southwestern region of the Gulf, particularly west of Jeffreys Ledge, where thermal stratification

develops in the spring and prevails through the summer. There was

some evidence that intermediate-sized (but not large or small) shrimp

collected east and west of Jeffreys Ledge were more fecund than

shrimp from two other locations in the southwest Gulf of Maine

in August 1968, but the September results did not show higher fecundities for shrimp collected west of Jeffreys Ledge. If there is, in

fact, an effect of temperature change on fecundity, it would have

been difficult, if not impossible, to detect in a field study like this

one where water temperatures were measured at discrete locations

and points in time. Oogenesis has been reported to last from January

until May in the Gulf of Alaska (Nunes 1984). If egg numbers are

also determined during the fall and/or winter in the Gulf of Maine,

vertical differences in temperature could not be invoked as a factor affecting fecundity (since vertical temperature profiles are

isothermal or nearly so during that time of year in the Gulf of

Maine), unless fecundity is also a function of events which take

19
3 4 5 6 7 8

BOTTOM TEMPERATURE(oC)

Table 7.-April-July bottom temperature data for the southwestern Gulf of

Maine (stations 3-7) expressed as mean bottom temperatures and 6° minus

mean bottom temperature, predicted mean fecundities (linear model), total

Gulf of Maine landings, and catch-per-unit-effort estimates, 1964-82.

Bottom temp. (OC) No. eggs/ Landings CPUE

Year Mean' 6°-mean 24-mm femaleb (103 MT) (MT/st day)'

1964 2,000

1966 1,645

1968 3.5 (16) 2.5 1,471 6.61 2.99

1969 5.0 (4) 1.0 1,150 12.82 2.77

1970 6.4 (I) -0.4 10.67 1.67

1971 II. 13 1.60

1972 11.10 1.53

1973 6.4 (2) -0.4 1,270 9.40 1.83

1,293

1974 6.5 (3) -0.5 1,431 7.94 1.77

1975 6.2 (8) -0.2 5.29 1.93

1976 6.5 (5) -0.5 10.22 1.46

1977 5.2 (4) 0.8 0.39 1.08

1978 1,901

1979 3.8 (10) 2.2 1,933 0.49 2.43

1,772

1980 1,720 0.33 1.20

1,491

1981 1,750 1.07 1.44

1,396

1982 4.2 (3) 1.8 1,680 1.53 1.48

aNumbers in parentheses are numbers of observations.

bFecundity expressed per 25 mm dorsal CL (= 28.5 lateral CL) during the

same year when eggs were spawned (i.e., the same year temperature measurements were made). In some years, fecundities wcre estimated for more than one

sample.

'CPUE expressed per 12 hour day for commercial 34-50 GT vessels, using trip

data for Gloucester and Portland, for which 50 % or more of the total catch consisted of shrimp.

Sources: Temperature data from Maine Dep. Marine Resources (1968-77) and

Charles Parker, Bigelow Laboratory for Ocean Sciences (1979 and 1982). Fecundity data for 1964-81 from Stickney and Perkins (1981). Landings and CPUE

data from Diodati el al. (1984).

15

I- 14

::!: 13 o

o 12 o II

10

z 9

a 8

::i 7 -' 6

w 2.2 Y=2.55-0.19X -'

<l:

r 2 ::!: =0.90 w

"- 2.0

E .'79

E

If) 1.8 N '79· "-

U)

<.:J 1.6 '82

0 1.4 0'68 .'74 0

_0

>- 1.2

1

73:

I0 0'69 z

::)

u 1.0 w

"-

Figure 24.-Fecundity per 25 nun dorsal carapace length

female vs. April-July bottom temperatures in the

southwestern Gulf of Maine for the period 1973-82 (1968

and 1969 data not included in linear regression).

Y= 1.07+5.9IX

r 2 =0.98

__e

'701'74

1.1 1.2 1.3 1.4 1.5 1.6 1.7 1.8 1.9

FECUNDITY ('000 EGGS/25mm FEMALE)

2.0

Support for the hypothesis that water temperature and fecundity

are inversely related is provided by a laboratory study by Nunes

(1984) of P. borealis held at low (2°-3°C), high (8°-9°C), and

ambient (annual range of 4°_10°C and mean of 6.3°C) water

temperatures for two entire reproductive cycles. Fecundities at low

and ambient temperatures were greater than fecundities at the high

temperature. After evaluating the effects of temperature on a number

of reproductive characteristics (i.e., egg production, embryonic

development, egg loss, size of larvae, larval hatching success, and

larval viability), Nunes concluded that the optimum temperature

range for reproductive success was 3° -6°C and that population

fecundity in the Gulf of Alaska could vary with temperature by as

much as 20%,

Temperature-induced changes in fecundity could partially explain

how population oscillations such as those observed in the Gulf of

Maine during the last 30 years were produced. The dramatic decline

in landings and CPUE in the early and mid-1970s was preceded

by a period of declining fecundity (Fig. 23). In fact, landings during 1969-74 were directly related to fecundities in 1965-70 (Fig.

25), suggesting that diminished egg production per female during

1965-70 reduced the recruitment of 4-year-old shrimp into the ex20

Figure 25.-Total Gulf of Maine shrimp landings vs. fecundity per 25 mm dorsal

carapace length female 4 years earlier for the period 1969-74.

ploitable population during 1969-74, thus leading to reduced

catches'o. The fact that such a relationship could be demonstrated

is remarkable since: (1) egg production would also depend on the

numbers of female shrimp bearing eggs in any given year; (2)

recruitment must also be affected by survival rates of eggs, larvae,

and I to 3-year-old shrimp; and (3) landings are directly proportional to fishing effort which increased by about 1/3 between 1969

and 1974 (Anthony and Clark 1980). Regression analysis offecundity vs. CPUE and fecundity vs. catch rate data from bottom trawl

surveys (Table 7) failed to reveal any relation between fecundity

and these two estimates of population size. The increased incidence

oflethal egg parasites observed in shrimp exposed to temperatures

>5.5°C during the fall inshore spawning migration (Table 5) could

be expected to increase egg mortality and also reduce recruitment

at age 4.

lOAn additional data poin! for 1979 landings-1975 fecundity was omitted from the

linear regression analysis since 1979 landings were limited by a short season (February I-March 31) and low fishing effort. High catch-per-unit-effort in 1979 further

indIcated that landings in that year bore no relation to population size.
Population fluctuations

and management implications

Large, cyclical variations in landings and catch-per-unit-effort over

the past 30 years (Figs. 1-3) suggest that the northern shrimp population in the Gulf of Maine undergoes fairly extreme, non-random

fluctuations in abundance which we contend are related primarily

to temporal changes in seawater temperature. The northern shrimp

population in the Gulf of Maine exhibits several biological

characteristics of an immature or unstable population as described

by Margalef (1963). Among the characteristics he described are

the following:

I) "Animals tend to spend their adult lives in the more mature

system but to reproduce in the less mature ones and send larvae

into them;

2) ...A unispecific population that expands over a wide range has

local differences in demographic structure, even when internal flow

of individuals is important;

3) Less mature systems species tend to be opportunistic ... and ...

are subjected to a dynamic type ofselection, often for prolificness;

4) Large fluctuations are to be expected; a rapid increase of numbers is possible only in a system that works with low efficiency;

5) Fluctuations of abundance are heavily influenced by external

inputs; i.e., by changes in the physical or abiotic environment. "

The following aspects ofthe life history of P. borealis in the Gulf

of Maine correspond to the five characteristics of an unstable population listed above:

1) The migratory behavior of this species in the Gulf results in the

partitioning of juvenile and adult life stages, with juvenile stages

restricted to inshore waters where a more variable annual temperature regime prevails and adult life stages found in thermally more

stable offshore waters, a pattern which is modified by the inshore

spawning migrations of female shrimp;

2) Despite an inshore-offshore migration, local differences in length

frequency distributions are evident;

3) Natural selection for maximum reproductive output in a species

which does not produce many eggs per female has resulted in the

evolution of sequential hermaphroditism, a process by which the

capacity of larger individuals in the population to function as eggbearers (females) is capitalized;

4) Large fluctuations in catch and stock abundance have been experienced in the fishery, a small one in the 1940s and a much larger

one between 1965 and 1975;

5) These fluctuations in abundance correlate fairly well with longterm periodic changes in mean annual sea surface temperature.

Both catch data and biological information therefore suggest that

the northern shrimp population in the Gulf of Maine is unstable.

The strong correspondence of life history characteristics and

migratory behavior with spatial and temporal temperature changes

in the Gulf of Maine underscores the importance of Margalefs fifth

characteristic: abundance is strongly influenced by the physical environment. We conclude, therefore, that in the Gulf of Maine, at

the southernmost extension of its range, the abundance of this boreal

species is strongly influenced by environmental factors, and that,

by means of its migratory behavior, it has adopted an opportunistic

life history strategy that permits it to exploit a favorable condition

(cooler water temperature) to the maximum extent. The opposite

situation exists along the coast of West Greenland near the northernmost extension of this species range, where periods of warmer

bottom water temperatures (above zero as opposed to subzero) have

been associated with stable yields (Smidt 1965, 1967). Populations

such as this one which undergo large-scale fluctuations in abun21

dance which are influenced primarily by physical features of the

environment do not respond well to attempts to control exploitation.

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