The diel migrations and distributions within a mesopelagic community in the North East Atlantic. 5. Vertical migrations and feeding of fish

Prog. Oceanog. Vol. 13, pp. 389-424, 1984.

0079-6611/84 $0.00 + .50 Copyright © 1984 PergamonPress Ltd.

Printed in Great Britain. All rights reserved.

The Diel Migrations and Distributions within a Mesopelagic Community in the North East Atlantic. 5. Vertical Migrations and Feeding of Fish H. S. J. ROE and J. BADCOCK Institute of Oceanographic Sciences, (N.E.R.C.), Wormley, Godalming, Surrey, GU8 5 UB, U.K.

CONTENTS 1. 2. 3. 4.

Introduction Materialsand Methods Net Feeding Results 4.1. The total population 4.2. Individualspecies 4.2.1. Benthosemaglaciale 4.2.3. Cyclothone braueri 4.2.4. Xenoderrnichthys copei

389 390 391 394 394 394 396 401 404 409

4.2.5.

413

4.2.2.

Argyropelecus hemigymnus Stomias boa ferox, Chauliodus sloani, C danae

5. Discussionand Conclusions 6. Summary Acknowledgements References

416 420 421 421 1. INTRODUCTION

THIS PAPER describes the distributions and feeding of midwater fish taken at 44°N 13°W, and is one of a series describing the diel distributions of the mesopelagic community at that position (ROE, ANGEL, BADCOCK, DOMANSKI, JAMES, PUGH and THURSTON, 1984; ANGEL, 1984; ROE, 1984a,b; ROE, JAMES and THURSTON, 1984; DOMANSKI, 1984; and PUGH, 1984). The gross vertical distributions of the fish analysed here are generally well established (e.g. BADCOCK, 1970; BADCOCK and MERRETT, 1976, 1977) but most previous work has been based upon vertical series of hauls, (sensu ROE et al., 1984) often widely spaced in time, which can only produce fairly generalised results. The present study is based upon a series of hauls made at four depths, 100, 250, 450 and 600m, each of which was fished for a continuous period of 48 hr. The individual depths were not fished concurrently but the data have been amalgamated to form two consecutive diel periods. ROE et al. (1984) describe the sampling procedures and discuss the presentation of the results. Repeated sampling at constant depths can provide greater details of distributions and migratory behaviour than one-off vertical series, but there have been few such studies where the micronekton has been analysed and even fewer which have considered the fish (e.g. LEGAND, BOURRET, FOURMANOIR, GRANDPERRIN, GUEREDRAT, MICHEL, RANCUREL, REPELIN and ROGER, 1972; ROE, 1974). HOPKINS and BAIRD (1977) gave a comprehensive review of the feeding of mesopelagic fish. Since then there have been a number of papers describing the feeding of individual species 389 JPO 13:3/4-J

390

H . S . J . ROE and J. BADCOCK

(e.g. GJOSAETER, 1978a, b; GORELOVA, 1978, ROWEDDER, 1980; IMSAND, 1981a; SCOTTO DI CARLO, COSTANZO, FRESI, GUGLEILMO and IANORA, 1982) or miscellaneous groups of fish (e.g. APPELBAUM, 1982, CLARKE, 1978, 1980, 1982; KAWAGUCHI and MAUCHLINE, 1981; and MAUCHLINE 1982) and estimates have been made of the energy budget of Valenciennellus tripunctulatus (HOPKINS and BAIRD, 1981 ; BAIRD and HOPKINS, 1981a, b). Although some authors (e.g. CLARKE, 1980)have examined fish feeding in relation to prey taken during the same diel period, only MERRETT and ROE (1974) have analysed such feeding in relation to concurrent prey availability. MERRET and ROE's work was limited by being confined to a single depth (250 m) and a single 24 hr period; the present samples permit a more extensive analysis both in time and space. 2. MATERIALS AND METHODS The fishing methods and procedures of the 48 hr series have been described by ROE et al. (1984). The fish analysis is based solely on the RMT 8 catches which have been standardised to numbers caught per 10,000 m 3 of water filtered. A two-sample t-test has been used to assess the significance of numerical variations and differences are considered to be significant when p ~< 5% (CAMPBELL, 1974). Standard length was measured to the nearest mm. Fish have also been identified from the vertical series made prior to the 48hr hauls (ANGEL, 1977) and from a number of hauls fished between 300-600m by day and night on the same and subsequent cruises. Some of the hauls in the vertical series were made to the north and some to the south of a thermal front which may have affected the distributions of the siphonophores (PUGH, 1984). It is probable that the repeated hauls between 300-600m also spanned this front but there is no evidence from either data set that the fish distributions were influenced by this. The fish data from all three series of observations are therefore considered to be comparable. Feeding was studied in the three most abundant species, Benthosema glaciale, Argyropelecus hemigymnus and Cyclothone braueri, and for four others, Xenodermichthys copeL Stomias boa ferox, Chauliodus sloani and C. danae which were considerably scarcer but which showed distinct vertical migrations. For the three abundant species 10 specimens per haul were taken at random, or as many as were available if less than 10 were caught, whilst for the scarcer species all undamaged specimens were used. The fish were sexed, if female the stage of ovarian maturity recorded (MERRETT, 1971), and the stomach and gut (intestines) opened separately under a microscope. The amount of food in each part was assessed visually and the contents identified as far as possible. Food in the mouth or oesophagus was not included in the analyses. Individual prey could often be identified and counted, but on many occasions accurate assessment of prey numbers was impossible. For example, copepod remains were frequently fragmentary and these have been counted as being from one individual unless distinct unique structures, e.g. female genital segments, were found. Consequently the numbers of prey given in the subsequent tables should be regarded as minimum estimations of the numbers eaten. Ivlev's Electivity Indices (~'i) have been calculated where possible: Ei _ r i - - P i ri q- Pi

where r i and Pi are the percentage composition of species i in the diet and plankton respectively (IVLEV, 1961). This results in an index ranging from -- 1 to + 1 with -- l indicating complete avoidance, 0 indicating no active selection and + 1 complete selection.

5. Vertical migrations and feeding of fish

391

The fragmentary nature of much of the prey precluded direct measurements, so estimates of prey sizes are taken from unpublished I.O.S. data obtained from various Atlantic stations, and the mean body lengths of the copepods are given as a range of the means of populations occurring at these various stations. 3. NET FEEDING Before proceeding it is appropriate to consider whether these results show natural predation or feeding within the net. HOPKINS and BAIRD (1977) briefly reviewed net feeding and concluded that it "is probably not extensive for many midwater fishes". Since then there have been conflicting reports, although most work on the diet of mesopelagic fish has ignored the problem. CLARKE (1978, 1980), ROWEDDER (1980) and IMSAND (1981a) found little or no evidence for net feeding, but LANCRAFT and ROBISON (1980) introduced artificial "prey" into a net and showed that such feeding can occur. They found that contamination of stomach contents varied specifically and was high in large or robust species commonly recovered alive (e.g. Stenobrachius leucopsaurus), and low in small or fragile species which were usually dead on arrival at the surface (e.g. Cyclothone). Furthermore, the incidence of net feeding was higher by day than night, small "prey" was more readily ingested in the cod end than large, and fish from discrete depth tows were less likely to feed within the net than those from oblique hauls because they were exposed to fewer potential prey. The present tows were short (one hour) and fished between discrete depths. The planktivorous fish, Benthosema, Argyropelecus, Cyclothone and metamorphic Xenodermichthys were small, much smaller than LANCRAFT and ROBISON's (1980) most abundant net feeder, and were invariably dead on retrieval. Their prey was mainly small Crustacea (copepods and larval euphausiids) which are unlikely to be retained by the 4.5 mm mesh of the RMT 8. This combination of factors makes it very improbable that net feeding was extensive in these fish. Larger prey, e.g. euphausiids, decapods and fish, are more effectively sampled by the RMT 8 and were eaten by the large Xenodermichthys, Chauliodus and Stomias, most of which showed limited signs of life when recovered from the trawl. The feeding of Chauliodus and Stomias is probably radically different from the other fish considered here, and the incidence of food in their stomachs was so low that any possible net feeding has no effect on the conclusions discussed later. The diet of the large Xenodermichthys is perhaps the most problematic here, but it was entirely consistent with the distributions of both the fish and their prey. If cyclic feeding is apparent then dietary contamination must be small. The presence of food within a stomach can result from net feeding but clearly absence of food cannot. Similarly possible vomiting or voiding food as faeces can be disregarded in any species where cyclic feeding is indicated. Reflex gulping may account for some apparent net feeding (HOLTON, 1969; HOPKINS and BAIRD, 1975), but very few of the present fish had prey in their mouths or oesophagus and such prey has been ignored. The diets of all the fish examined here were restricted to a very small part of the potential prey biomass. Such selectivity is inconsistent with net feeding where fish may be expected to feed indiscriminately at random. In conclusion there is no evidence for net feeding here, and this, combined with previous findings, makes it almost certain that the present diets result from natural predation. A low level of contamination is probably undetectable, however, and equally probably does not matter. General trends and patterns are apparent in the present data and any low level of contamination will merely blur the overall picture.

Gonostoma elongatum G U N T H E R , 1 8 7 8 Argyropelecus hemigymnus C O C C O , 1 8 2 9 A. olfersi ( C U V I E R , 1 8 2 9 ) Maurolicus muelleri ( G M E L I N , 1 7 8 8 ) Valeneiennellus tripunctulatus E S M A R K, 1871 Chauliodus danae R E G A N a n d T R E W A V A S , 1 9 2 9 C. sloani S C H N E I D E R , 1801 Stomias boa ferox R E I N H A R D T , 1843 Leptostomias sp. Benthosema glaciale ( R E I N H A R D T , 1 8 3 7 ) Boliniehthys indicus ( N A F P A K T I T I S a n d N A F P A K T I T I S , Diaphus holti TANIN G, 1 9 1 8 D. effulgens G O O D E a n d B E A N , 1 8 9 6 D. rafinesqui ( C O C C O , 1 8 3 8 )

C sp.

Opisthoproctus soleatus V A I L L A N T , 1 8 8 8 Xenodermichthys copei G I L L , 1 8 8 4 Searsia Koefoedi P A R R , 1 9 3 7 Bonapartia pedaliota G O O D E a n d B E A N , 1 8 9 6 Cyclothone alba B R A U E R , 1 9 0 6 C. braueri J E S P E R S E N a n d T A N I N G , 1926 C. livida B R A U E R , 1 9 0 2 C. microdon G U N T H E R , 1 8 7 8 C. pallida B R A U E R , 1 9 0 2 C. pseudopallida M U K H A C H E V A , 1 9 6 4

Depth (m)

1969)

D

100

-

.

-

. -

-

-

-

-

-

.

8.0 0.05 0,2

0.2 0.2

0 . 1

0.05 0.1 1.0

N

.

.

.

O.4

4.5 0.03

.

0.07

.

-

0.1 . 11.8 . 0.03

-

-

-

-

-

D

.

250

.

.

.

-

-

-

-

0 . 1

0.6 . 0.05

O.02 5.9 0.02 0.1 0.4 0.02 0.02 0.1

0.02

0 . 2

0.4

N

.

-

-

-

-

-

-

1.7

0.1 0.8

0.02 0.2

0.04 0.02 0.3

0.02 62.5

-

0.04 0.7

D

0.1

1 . 1

N

-

-

-

-

-

-

-

0.02 0.05 0.02 0.1

0.1

0.2 0.05 O.O5

0.02

49.0

-

-

8

450

T A B L E 1. M E A N N U M B E R S O F F I S H / H A U L / 1 0 , 0 0 0 m 3 O F W A T E R F I L T E R E D BY T H E R M T D = D a y ; N = N i g h t ( S u n s e t to Sunrise inclusive)

-

-

-

0.03

0.I

0.03 0.03 0.09

O.O6

8.7 0.1 O.5 0.06 1.1 0.06

0.7 0.1

D

600

-

0.2

0.04 0.1

0 . 0 4

0.03 8.O 0.1 0.5 0.1 1.4 0.04

0.5 0.1

N

© g3

>

r-,

©

b,-)

0.5 0.2 0.7 0.56 0

Total Mean No. Standard Deviation No. of Spp. (exc. leptocephali + unidentified)

D

Paralepidid larvae Leptocephali Unidentified

Lobianchia gemellari (COCCO, 1838) Notolychnus valdiviae (BRAUER, 1904) Notoscopelus Kroeyeri (MALM, 1861) Protomyctophum arcticum (LOTKEN, 1892) Scopelosaurus sp.

L. sp.

Lampadena speculigera GOODE and BEAN, 1 896 Lampanyctus crocodilus (RISSO, 1810) L. intricarius TANING, 1928 L. macdonaldi (GOODE and BEAN, 1896) L. pusillus (JOHNSON, 1890)

Depth (m)

TABLE 1. CONTINUED 100

10.91 10.04 17

0.05 0.2 0.2 0.1

0.2 0.02

17.26 6.49 9

0.1

q

8.03 2.51 18

0.1

0.02

0.05

67.18 10.14 19

0.02 0.2 0.04

0.02 0.4

0.04

0.1 0.02

D 0.04 0.02

N 0.05

0.2 0.03

D

0.1 0.02

N

250

450

50.97 12.72 16

0.02

0.1

0.02

0.02

N

12.15 3.41 19

0.03

0.02 0.04

0.04 0.06 0.3

D

0.1

0.03

N

11.18 1.75 15

600

~o

O

< a

394

H.S.J. ROE and J. BADCOCK

4. RESULTS

4.1. The total population Table 1 shows the mean numbers o f each species per haul by day and night; for convenience night includes hauls spanning sunset and sunrise. Figure 1 shows the numbers of individuals and species in each haul. Thirty four species were identified, but at each depth most were very scarce and the population was dominated b y 3 species, C. brauerL B. glaciale and A. hemigymnus. Greatest numbers were caught at 450 m where fish comprised the second most abundant group sampled by the RMT 8 (ROE, 1984a, his Table 3). Significantly more fish were caught at 1 0 0 m by night than by day (p = 1%) whereas significantly more were taken during the day at 2 5 0 m (p = 0.1%) and at 4 5 0 m (p = 1%). There were no significant day-night differences in total numbers at 6 0 0 m . These numerical changes result from vertical migrations away from, into and through the various depth strata.

4.2. Individual species The vertical distributions and feeding o f seven species o f fish are described below. Some o f these species were eaten by the decapod Crustacea analysed by ROE (1984a) and appropriate instances are cross referenced here.

40

20

20

10

30

15

10.

5 Z

o° 90.

o

o-

o

0

70.

2 -a 50.

:31). Z

ill

tl

10.

,01[

5

..................... ;:i:~:!:!:!:!:i:!:~:i:~:;:i:;:~ii!~iii~; :i!;~i!i!i;

600m

9

10

!{:.ii!i::::::::i :~:iiU:i::ii i~i~:.~~i~iU/i:!i;:~i~i~

ii~i!iiii~iiii!!~iii~i!iiii~ii~i!iii~iiii~(ii~:~iii~i~i~iii~:~iii~i!ii~! I ""

"" 13

.......... 17

::'::'::::ii~ :~...................i:~!:~:~:~:~:~i :: il '" 21

""

1 5 9 Time GMT,00hr$

i!i~i~iiljii!~ii ii ..

• ....... 13

ii

" .... iiii :ii~:Z~i~::ii::::::~i::i:::::::::::::~i: 17

21

1

5

5 9

FIG. 1. The total fish population: histograms = numbers of individuals per haul per 10,000 m 3 of water filtered f = the number of species per haul; 48 hr series data.

5. Vertical migrations and feeding of fish

8o

~.

4o.

20

•Nos. o

20

4o

8o

60

395

lo

No. o

19

,

29,

E

~ 500

B. glaciale A.hemigyrnnus

I

n=256

l

n=74

n:16

100~ II 40

20

Nos. 0

20

n:34

40

]

=DAY

C. braueri = NIGHT

E .= ~50C r-,

n:206

~

n:223

1000

FIG. 2. Vertical distributions of Benthosema glaciale, Argyropelecus hemigymnus and Cyclothone braueri from the vertical series (see text). 35" 100m 25-

15.

%

5

0

~ 25

:•:•:!:•:!:•:•:i?:•:i•:i:i:i:i:i:•:•:•:i!:!:•:!:!:!:!:•:!:!:•:•:i• ;iii!iiiiiiiiiiiiiiiii!ililililili!i![il!i!ii][iiiiiiiiiiiiiiiiiiiiiiiiiiiiiiil] ~ii~i~i~i~i~i~i~i~i~i~i~i~i~;~iii~iiiii~i~i1ii~i~i~i~iiiii~ i!i!!!ii!i!iliii!i!ili!ili!ii!iii[iiiiii!iii!i!i!i!!ii!i!!!!iii! ~

n

450m

5.

1

I

600m

9

~ ~ ~ ~ i i i i i i l i!!:~:~:[!~:~:~:!:~:i:i:i:i:i:i:~:i:i:~!:i:~:~:~:~:~:~:~:~:~:i:~:~:iijii~ii

13

17

21

1 5 9 Time GMT, 0 0 hrs

13

17

21

1

5

9

FIG. 3. Benthosema glaciale: numbers of individuals/haul/10,000 m3 of water filtered; 48 hr series data.

396

H . S . J . ROE and J. BADCOCK

Vertical

G

rm

Series -

48hr Series

Io-loom -

lOOm

-

C

. • _

5C

4G =DAY 8C

m

30

=NIGHT 6G 250m

20

4C 200-300m 2C

I0

A-

0

-~o

_

450m

300-400m

I~ r'~ml r-~m

Q

400-500 m

d

Z c

G

600m

u I~_ 500-600m ~ ~

C m

600-7'00m r-I r-~

r-~ r-1

700-800m

C

800 -900 m m "18" ' ' "2:2' ' 2 6 ' " ' ~ " " ~34 ' ' ~3/3' ' ~,i Standard

''1i "" 2~'" ~6'" h6"" k / ' ' ~ ' ' Length

;,~ "

mm

FIG. 4. Benthosema glaciale: population size frequencies at each depth from the vertical and 48hr series, o = Day, • = Night. 4.2.1. Benthosema glaciale. The data from both the vertical and 48 hr series show general agreement (Figs 2, 3, 4). Most individuals lived between 200 and 3 0 0 m by day and migrated upwards at night. The population size frequency consisted of an abundant group of SL 2024ram and a scarcer ill-defined group of SL 2 9 - 4 0 m m , corresponding to age groups I and II of HALLIDAY (1970) and GJOSAETER (1973a). During the day the proportion of group II fish increased with depth (Fig. 4). Both age groups migrated at night but the data are insufficient to show whether or not size stratification was maintained at this time. The relative scarcity o f Benthoserna in the night vertical series is due to the puzzling absence of group I fish. The 48 hr series data, with large catches around sunset and sunrise at 100 m and concomittant decreases in abundance at 250 and 450 m (Fig. 3), suggest a population centered around 2 5 0 m by day which migrated up to some depth between 100m and the surface at night. Additional specimens were indeed caught at night with a non-quantitative surface net (ROE et al., 1984). The increase and decrease in numbers at 250 m during the day (Fig. 3) indicate that this movement may have been more or less continuous. 4.2.1 .I. F o o d a n d f e e d i n g - Table 2 shows the stomach analysis for each depth, giving the mean number o f each prey per fed stomach and the frequency of occurrence of prey per fed stomach; i.e. at 100m 74 stomachs contained food of which 41 (55.4%) contained euphausiid larvae. Table 3 summarises the percentage of fed stomachs which were more than half full, contained

Prey Euphausiid larvae Euphausiid adult Copepods Amphipods Ostracods Chaetognaths Fish Digested debris

Depth(m)

No. Examined No. with Food S-T (mm)

Day/Night

Depth (m)

D

1 1 31

41 1 63 1

100

86 74 29.3

Total

53

33

13

44

1

39

450

4

250

No. of fish with Prey

86 74 29.3

N

100

2

6 1

1

600

90 47 25.7

D

0.01 0.01

20.2 0.04 9.5 0.01

100

23 12 28.6

N

250

71 52 31.9

D

1.2

0.6

0.02

4.3

450

0.5

250

No.of Prey/Fish

113 59 26.2

Total

4.3 0.2

1.0

600

5 5 27.6

N

450

1.4 1.4 41.9

55.4 1.4 85.1 1.4

100

76 57 31.8

Total

7 5 30.5

N

89.8

22.0

6.8

250

77.2

2.0

57.9

68.4

450

Freq. of Occ. of Prey (%)

4 1 31.5

D

600

33.3

100.0 16.7

16.7

600

11 6 31.4

Total

TABLE 2. B E N T H O S E M A G L A C I A L E : ANALYSIS OF STOMACH CONTENTS: THE UPPER PART OF THE TABLE SHOWS THE NUMBERS OF FISH EXAMINED AT EACH DEPTH BY DAY AND N I G H T AND THEIR MEAN STANDARD LENGTHS; "]HE LOWER PART SHOWS, FOR EACH DEPTH, THE NUMBERS OF FISH WHICH HAD EATEN EACH PREY TYPE, THE MEAN NUMBER OF COUNTABLE PREY PER FED FISH AND THE FREQUENCY OF OCCURRENCE OF EACH PREY PER FED FISH

¢-0 e~

5

<

0 57.7 0

100 250 450 600

-

D

Depth (m)

N

55.4 8.5 80.0 20.0

% > ~- Full

10.6 75.0 0

D

% Fresh

89.2 66.7 100.0 80.0

N

Stomach Contents

95.7 78.8 25.0

D 41.9 66.7 60.0 20.0

N

% Digested

56.7 52.2

D

0 37 23 0

(n)

26.0 41.2 66.7 33.3

N

% with Food

Gut Contents

14 7 1 1

(n)

26.0 43.4 53.2 20.0

Total

TABLE 3. BENTHO,TEMA GLACIALE: THE % OF STOMACHS OF FED FISH WHICH WERE > ~- FULL, CONTAINED FRESH (IDENTIFIABLE) FOOD AND DIGESTED (UNRECOGNISABLE) FOOD. THE % OF GUTS (INTESTINES) WHICH CONTAINED DIGESTED FOOD, n ----NO. EXAMINED

©

>

~u

0 M

s

5. Vertical migrations and feeding of fish

399

recognisable (fresh) food and unidentifiable digested debris, and the percentage of guts containing food (all of which was digested). No sex-related variations were found. Copepods and euphausiid calyptopes were the dominant recognisable prey (Table 2). The commonest copepods were Metridia lucens and Clausocalanus sp. which respectively formed 76.3% (338) and 17.1% (76) of the identifiable species in the stomachs at 100m; 80.0% (16) and 0 at 250m; 33.3% (10) and 10% (3) at 450m; and 76.5% (13) and 0 at 600m. The calyptopes were not specifically identified. At 100 m they were mainly stage I and II, a few of which were measured (total length 0.88-1.28 ram, mean 1.04 ram), whereas at 450 m they were older (and larger) but all partially digested. Some of the stage I and II calyptopes were within the size ranges reported by MAUCHLINE (1959) for Meganyciphanes norvegica, and older larvae of this species (Calyptopes III and furcilia) were common in the plankton at both 100 and 450m (ROE, JAMES and THURSTON, 1984). Using the RMT 1+8 it is possible to simultaneously compare the proportions of prey in the fish stomachs (caught by the RMT 8) with their proportions in the plankton (RMT 1). All the numerically important groups in the RMT 1 catches were counted (Table 4). Copepods were by far the most abundant planktonic group but euphausiid larvae were not completely analysed. Consequently it is unrealistic to calculate group electivity indices for Benthosema although since these larvae were relatively scarce in the plankton they were probably selectively preyed upon by Benthosema at 100 and 450m. Within the copepods it is possible to calculate Ivlev's Electivity Indices (Ei) for the various species, although the prey data for depths > 100m is scarce (Table 5). The indices are consistent however, Benthoserna positively selected M. lucens but avoided the far more numerous Clausocalanus. M. lucens is larger than Clausocalanus (mean body lengths are 92.13-2.15 mm, d 1.58 mm and ? 1.15-I .23 ram, d 1 .I 1-1.18 mm respectively, ROE, 1977, unpublished) and it may be that Benthosema was selected according to size. Feeding chronology was deduced from the proportions of fresh and digested food in specimens from various depths (Table 3). Benthosema caught at 100m at night contained a high incidence of fresh food in the stomachs coupled with a scarcity of food in the guts. Furthermore, the proportion of stomachs which were > ½ full was highest in the middle and late part of the night and the proportion of empty stomachs greatest early in the night. In contrast, at 250m, none of the stomachs from day-caught fish were half full and very few contained fresh food; digested remains however were almost universal. Data from these two shallow depths indicate that B. glac~ale fed actively at night at the shallow end of its migratory cycle and digested its food during the day. Lack of daytime feeding at 250 m was not due to the absence of suitable prey for M. lucens and Clausocalanus were both abundant at this depth by day (Table 5), as were many other similarly sized plankton. A few individuals, which may have been either non-migrants or migrants from deeper depths, apparently fed actively at 250 m by night. The data from 450 m are equivocal. The high incidence of recognisable food in the stomachs of fish caught by day (Tables 2 and 3) suggests that active feeding occurred at this time. However the recognisable prey of these fish consisted mainly of partially digested large calyptopes and their presence may reflect resistance to digestion rather than immediate feeding. These difficulties in interpretation are discussed later. B. glaciale was not specifically identified as prey for any of the other fish here, nor for the crustaceans examined previously (ROE, 1984a), although Systellaspis debilis did eat unidentifiable myctophids at both 100 and 450 m. The feeding of B. glaciale has been previously investigated by GJOSAETER (1973b, 1978c), KINZER (1977), WORNER (1979), and KAWAGUCHI and MAUCHLINE (1981), all of whom found that copepods were the principal prey and indicated some degree of size selectivity.

Other Copepods

Clausocalanus Metridia lucens

Mean No. Copepods/haul No. specifically identifiable copepods in Benthosema guts

0 0.13 0.01 99.61 0.07 0.25

D

ri

17.1 76.3 6.6

Ei

67.6 15.9 I6.5

0.6 + 0.6 - 0,4

ri 0 50.0 50.0

70.1 21.0 8.9

Pi

2

443

Pi

40,108,3

D

23,674.2

N

100m

23821.1

0 0.07 0.03 99.38 0.11 0.41

N

40265.6

0 0.02 0.002 99.61 0.07 0.30

D

250

23874.0

0 0.10 0.03 96.60 1.75 1.51

N

39603.7

0.02 0.10 0.11 96.98 2.57 0.23

D

450

35249.7

0.02 0.08 0.05 96.77 2.77 0.29

N

18637.4

0.14 0.03 0.05 93.88 5.37 0.52

D

600

24456.5

0.09 0.03 0.05 95.38 4.06 0.39

N

1.0 + 0.4 + 0.7

Ei

250

Pi 0 86.2 83.3 1.7 16.7 12.1

ri

18

23,062.4

N

1.0 + 1.0 + 0.2

Ei

Pi 0 90.1 13.6 3,1 86.4 6.8

ri

22

38,407.7

D

1.0 + 0.6 + 0.8

Ei

450

ri 27,2 63.6 9.2

90,8 3.8 5.4

Pi

l1

36,424.3

N

Ei --0.5 + 0,9 + 0.3

0 0 100

ri

76.1 13.3 10.6

Pi

1

17,947.1

D

1.0 -- 1.0 + 0.8

Ei

600

0 81.2 3.8.8

ri

Ei 82.8 -- 1.0 9,2 + 0.8 7.9 + 0.4

Pi

16

23,327.5

N

IVLEV ELECTIVITY INDICES (E i) FOR VARIOUS PREY COPEPODS: r i = % OF SPECIES i OF THE SPECIFICALLY IDENTIFIABLE COPEPODS IN THE DIET, pi = % OF SPECIES i IN THE PLANKTON

100

GLACIALE:

45353.3

TABLE 5. B E N T H O S E M A

Total No

Mysids Euphau siids Amphipods Copepods Ostracods Chaetognaths

Group

Day/Night

Depth (m)

TABLE 4. RMT 1 CATCHES; THE MEAN % NUMBERS OF EACH ANALYSED GROUP PER HAUL BY DAY AND NIGHT AT EACH DEPTH Copepods = adult calanoid8 and Euphausiids exc|udes nauplii and most calyptopes

g~ 0

t~

0

O~

"~ c~

5. Vertical migrations and feeding of fish

~

:~

401

250m

11

1'5

#

~13

~1 ' ~' 1'1 ' "/5 ' TIME (GMT, OOhrs)

f9 ......... ' ~3 " ''

. .~. . . '

~

1'1

FIG. 5. Argyropelecus hemigymnus; numbers of individuals/haul/10,000m 3 of water filtered at 250 m; 48 hr series data.

35" 30 25 20' -~15 Z 10

10

15 20 25 30 Stondard Length mm

35

FIG. 6. Argyropelecus hemigymnus; population size frequency at 250 m, day and night samples combined; 48 hr series data. GJOSAETER (1973b) and KINZER (1977) observed more feeding by night than by day and the former found seasonal variation in feeding intensity and referred to a few isolated observations made by earlier workers. As far as is known the food and feeding activity of the four other species of Benthosema is similar to that of B. glaciale (KINZER, 1969; LEGAND and RIVATON, 1969; BAIRD, THOMPSON, HOPKINS and WEISS, 1975;HOPKINS and BAIRD, 1977; CLARKE, 1978; and GJOSAETER, 1978d). 4.2.2. Argyropelecus hemigymnus. In the 48hr series A. hemigymnus was virtually confined to a depth of 250m (Table 1, Fig. 5) with a bimodal size distribution by day and night (Fig. 6). More specimens were caught by night than by day but the difference in numbers was not significant. The sparse data from the vertical series (Fig. 2) generally agree with those from the 48 hr work. Distinct vertical migration, no migration at all, and migration of only a part of the population have all been reported in this species (BADCOCK, 1970; GIBBS and ROPER, 1970; BADCOCK and MERRETT, 1976, 1977), and in the temperate eastern north Atlantic migration is apparently confined to animals larger than 18ram SL. (BADCOCK and MERRETT, in

402

H . S . J . ROE and J. BADCOCK

TABLE 6. ARGYROPELECUS HEMIGYMNUS: ANALYSIS OF STOMACH CONTENTS AT 250m; SEE LEGEND TO TABLE 2 Day]Nigh t

D

N

Total

No. examined No. with rood S-~ (ram)

59 36 20.1

96 68 22.6

155 104 21.5

Prey

No. of fish with Prey

No. of Prey/Fish

Freq. of Occ. of Prey %

Euphausiid larvae Copepods Amphipods Ostracods

7 69 2 1

0.07 2.0 0.02 0.01

6.7 66.3 1.9 1.0

Chaetognaths Digested debris

51 63

0.5

49.0 60.6

prep.). The absence of clear migratory patterns does not preclude partial and acyclic migrations and the problems of detecting these have been discussed previously (ROE, 1974; PEARRE, 1979;ROE, 1984a; ROE etal., 1984). 4.2.2.1. Food and feeding- Most of the recognisable prey were copepods and chaetognaths (Tables 6 and 7). A. hemigymnus was effectively a non-migrant but much of its prey was migratory and consequently there were some temporal changes in its diet. Clausocalanus and Aetideus arrnalus were abundant at 250 m throughout the diel period (ROE, 1984b) and of the total Clausocalanus and Aetideus eaten, 46 and 45% respectively were eaten by day and 54 and 55% by night. Extensive migrants such as P. robusta, E. acuta and Undeuchaeta occurred at 250m almost entirely at night and were consequently eaten only at this time. Apart from M. lucens, which was eaten mainly at night but was more abundant at 250m by day, the occurrence of copepods in the diet is consistent with the observed vertical distributions of predator and prey. A. hemigymnus fed u p o n virtually all the available abundant copepod species, the notable exception being Ctenoealanus vanus which comprised 6.3 and 7.8% of the copepod population at 250m by day and night respectively but was absent from the fish stomachs. Chaetognaths were much more abundant at 250m during the night than by day (Table 4) and were more frequently eaten at night (Table 7). Their remains consisted of heads (15 stomachs - in four of which they could be identified as Sagitta maxima) and gelatinous muscular tissue. This gelantinous tissue was attached to two of the heads and was clearly the chaetoghath body wall. Consequently in 42 stomachs where no heads were found, similar remains (totally lacking nematocysts) have been identified as chaetognaths. Both size groups of A. hemigymnus selectively ate chaetognaths, although this selection was more positive by the larger fish (Table 7). As a group, copeopods were eaten in much the same proportion as in the total plankton, but the different species were selectively eaten or avoided. Clausoealanus was avoided by the large Argyropeleeus but not by the small fish; conversely small Argyropelecus avoided the large copepods which were selectively eaten by the large fish (Table 7). As with Benthosema this selection is probably based upon prey size. The missing copepod in the diet, C. vanus, is smaller than any of the species in Table 7, (9 mean body lengths 1.07-1.1 mm, ROE, 1972, unpublished) and it may have been too small for even the smallest fish to eat.

7.

0.02 0.002 0.07 0.30 99.61

92.0

? < 0.1 21.0 < 0.1 < 0.1 < 0.1 < 0.I < 0.1 < 0.1 < 0.1

70.1 0.2 0.6

99.8

61.5 19.2 11.5 3.8 3. 8 0 0 0 0 0 0 0 0

26

t young calyptopes not analysed in R M T 1 c a t c h .

~:%

Clausoealanus Aetideusarmatus Scolecithricella minor Oncaea sp. Euchirella spp. Metridia lucens Undeuchaeta spp. Euchaeta acuta Pleuromamma robusta P. gracilis Augaptilus megalurus Heterorhabdus ?abyssalis Candacia sp.

No.

3.3t 0 0 3.3 93.3

ri

11-20mm, n = 42

Pi

ROE,

-- 0.06 + 0.98 + 0.90 ? + 0.95 --1.0 - - 1.0 -- 1.0 -- 1.0 - - 1.0 - - 1.0 - - 1.0 - - 1.0

- - 1.0 - - 1.0 + 0.83 0.03

El

Day

FROM

99.9

25.0 8.3 0 0 8.3 41.7 8.3 0 0 8.3 0 0 0

21

0 0 0 33.3 66.7

ri

-+ -? + + + --+ ---0.98 0.33 0.98 1.0 1.0 0.98 1.0 1.0 1.0

0.47 0.95 1.0

- - 1.0 1.0 - - 1.0 + 0.98 -- 0.20

Ei

2 1 - 3 5 m m , n = 17

0.1 1.7 0.6 0.1 1.0 0.9 0.1 0.1 0.1 91.5

< < <

<

?

86.2 0.3 0.3

0.10 0.03 1.75 1.51 96.6

Pi

99.9

80.9 9.5 0 9.5 0 0 0 0 0 0 0 0 0

21

0 0 0 6.5 93.5

ri

-+ -? ----------

---+ --

n = 36

1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0 1.0

0.03 0.94 1.0

1.0 1.0 1.0 0.62 0.02

Ei

N ig h t

MEAN

BODY

99.8

8.2 4.9 1.6 3.3 8.2 39.3 13.1 11.5 4.9 0 1.6 1.6 1.6

61

0 0.7 0.01 27.9 66.2

ri

1.0 0.4 1.0 0.9 0.19

-- 0.83 + 0.88 + 0.68 ? + 0.96 + 0.92 + 0.91 + 0.98 + 0.66 - - 1.0 + 0.88 + 0.88 + 0.88

-+ -+ --

Ei

21-35 mm, n = 60

INDICES

1.58-2.15 3.34-5.13 3.57-3.83 2.98-3.26 1.70-1.82 4.46-5.01 2.40-2.75* > 2.0

1.67-1.80 1.08-1.46"* ca 1 . 0 " 2.5-4.16

1.1-1.23

Mean L e n g t h ( m m )

OF COPEPODS

AT 250m.

LENGTHS

BY DAY AND NIGHT

1980). n = NO. OF FISH

OF COPEPODS.

1933; **PARK,

ll-20mm,

*ROSE,

SPECIES

(El) F O R B O T H S I Z E G R O U P S

INDIVIDUAL

INDICES FOR

1972, UNPUBLISHED;

4) AND

ELECTIVITY

(SEE TABLE

(SIZE DATA

OF PREY

Specifically identificable C o p e p o d s in S t o m a c h s

Euphausiids Amphipods Ostracods Chaetognaths Copepods

Pre...yy

GROUPS

ARE SHOWN,

FOR

ARGYROPELECUS HEMIGYMNUS: IVLEV

CALCULATED

Argyropelecus size & n u m b e r

ARE

TABLE

4~

::r

¢-D

e.+

<

tan

404

H . S . J . ROE and J. BADCOCK

No. of Specimens 10

100

5

3 6 10

6

5 5

10 10 10

3

9

10 10 9 9 10

10 g~l:Full

80 [-I:Little • : Empty

g 20,

fl

'

I~,

'

I~

' 2'3

. . . . . 7. .

11

I~

'

;~

' 2.3

'

~

'

~

'

1'i

Time GMT, 00 hrs

FIG. 7.

Argyropelecus hemigymnus; percentage

of stomachs in each haul which were e m p t y m, contained little food D, were half full rn or full e.

The changing proportions of food in the stomachs indicate cyclic feeding during both diel periods (Fig. 7). The incidence of stomachs which were less than half full was high throughout the 48 hr, but that of full and half-full stomachs was greatest in the afternoons and early part of the nights and, conversely, that of empty and little filled stomachs was highest in the mornings. The data therefore suggest that A. hemigymnus fed most actively in the afternoon and evening but less so during the rest of the diel period. This conclusion agrees with that of MERRETT and ROE (1974) but the reasons for this cycle remain obscure. Suitable size prey was available at 250m at all times; perhaps feeding is stimulated by the changing light levels in the afternoon and evening, or by the arrival of migrant species providing a greater diversity of potential prey. A. hemigyrnnus was not found in the stomachs of any of the decapods examined previously (ROE, 1974a), nor in any othe other fish here. MERRETT and ROE's (1974) work is the only previous account of feeding chronology in this species but there are additional records of its prey (JESPERSEN, 1915; HOPKINS and BAIRD, 1977). The latter authors listed dietary data from various areas and found that copepods and ostracods predominated but that chateognatbs were an important food in the subarctic Pacific. There are no other reports of prey selection in this species although similar behaviour does occur in A. aculeatus (MERRET and ROE, 1974). 4.2.3. Cyclothone braueri. C. braueri occurred mainly between 400 and 600m in the vertical series (Fig. 2) and at 450 and 600m in the 48 hr series (Fig. 8). The population size frequency was bimodal (Fig. 9) and the sexual determination of individuals used for stomach analysis identify the smaller size group as mostly males and the larger as females. Shallow living females tended to be smaller (SL < 29 mm) and less mature than deeper living ones, and, at least in the vertical series, males occurred only between 300 and 100m whereas females were more broadly distributed. Both size stratification and sexual segregation have been previously observed in C. braueri by BADCOCK and MERRETT (1976, 1977, in prep.). Evidence for diel migration is equivocal. The different day-night catch rates for small (SL 18-23 mm) individuals taken between 300 and 500 m in the vertical series (Fig. 9) and the significantly higher numbers (p = 1%) caught by day than by night at 450m in the 48hr series both suggest a limited migration at night. However neither the total population data from the vertical series (Fig. 2) nor the size data from the 48 hr series (Fig. 9) support such

5. Vertical migrations and feeding of fish

405

90. 450 m

iiiiiiii!iliiii~iiiiiiiii!ii!iiiiiiiiiiiii~

70-

~i~iiiii!iiiiilililiiiiiiiiiiliiii!iiiii!iiiiiiii!!iiiiiliiiiiiililiiiiiiiil

50E

g

-

II II

-

o.30. O

~IOZ

,

::

....

ii!il

20.

9

FIG. 8.

13

17

21 1 5 Time GMT, 00hrs

9

13

17

21

1

5

9

Cyclothone braueri; n u m b e r s of individuals/haul/10,000m 3 of water filtered; 4 8 h r series data.

5ool

48hr Series

300 - 400 m 300l

450m

400-500 m

,~r

500-600 m

[]

=DAY

'° f

600 m

5O

.>_.

"6

0

Z

'12 600-700m

-

1~ r

10 30

700-800m 50

~ r-, - - ~

16

20

24

28

~ 32

800-900m 900-1000m 36

40

44

Standard

17

Length

FIG. 9.

25

29

33

37

Cyclothone braueri; population size frequencies at each depth from the vertical and 4 8 h r series, u = Day, • = Night.

JPO 13:3/4-K

21 mm

406

H.S.J. ROEandJ. BADCOCK

TABLE8. CYCLOTHONEBRAUERI:ANALYSISOFSTOMACH CONTENTS;SEELEGEND TO TABLE 2 Depth (m) Day/Night No. Examined No. with Food SL (mm)

Depth(m) Prey Decapod? Euphausiid larvae Copepods Ostracods Eggs? Polychaete spicules Digested debris

450 D

600 N

140 70 31.1

Total

119 52 30.8

259 122 31.0

D 116 57 30.4

N

Total

99 50 30.6

215 107 30.4

No. of Fish with Prey

No. of Prey/Fish

Freq. of Occ. of Prey %

450

450

450

600

1 100 3 2 21

600

0.01 1 85 2 1 25

1.3 0.02

600

0.8 0.01 1.1 0.02

82.0 2.5 1.6 17.2

0.9 79.4 1.9 0.9 23.4

a conclusion. Previous work has shown that C. braueri is caught more often by day than by night (BADCOCK, 1970; BOND, 1974; BADCOCK and MERRETT, 1976, 1977) and diel variations in catch rate could result from behavioural features such as activity cycles, clumping or dispersal rather than from migration. Cyclic respiratory activity has been demonstrated in C. acclinidens (SMITH and LAVER, 1981) and whilst it is difficult to imagine Cyclothone actively avoiding 8 m 2 nets during the night, the possibility cannot be excluded. Similarly neither can vertical migration, although if this is regular it must be limited in extent and perhaps confined to only a small part o f the population. 4.2.3.1. Food and feeding - Results o f the stomach analysis are shown in Table 8; no guts were analysed. Only 14 males were examined but apart from possible size selection there was no evidence for a sexual difference in feeding behaviour. Copepods were the dominant prey but were nearly always present in small numbers, as one or two copepods per stomach. As a group they were eaten in much the same proportion as in the plankton, (at 4 5 0 m E i = + 0.001 (day), - - 0 . 0 1 (night) and at 6 0 0 m E i = 4- 0.007 (day) and + 0.02 (night)), and most o f the prey species were at least generically identifiable (67.3% at 4 5 0 m , 79.4% at 6 0 0 m ) . C. braueri generally ate the abundant planktonic copepods in accordance with their vertical distributions (Table 9, ROE, 1984b), but was selective. Relatively scarce species were selected for, but Clausocalanus was avoided and several copepod species which comprised more than 1% o f the planktonic populations were totally absent from the fish stomachs (Spinocalanus brevicaudatus at 450 and 6 0 0 m , S. abyssalis and Metridia venusta at 6 0 0 m ) . This selection is probably based upon size. Clausoealanus and most o f the "missing" species are small, their mean b o d y lengths being < 1.5 mm, although M. venusta is considerably larger. In contrast, among the other prey species, only M. lucens has a mean b o d y length o f < 2.5 mm (ROE, 1972, unpublished; T A N A K A and OMORI, 1969). However, there is no evidence that small female

No. of specimens Overall Mean Size (ram)

Clausocalanus M. lucens P. robusta E. rostrata

600m

No. of specimens Overall Mean Size (mm)

Clausocalanus Metridia lucens Euchirella rostrata Undeuchaeta plumosa Pleuromamma robusm

450m

3.26

t .58 2.5 3.34 3.09

d

9

1.21 2.13 3.19 3.69

(mm)

Mean Body Length

13.0 26.1 28.3 21.7 89.1% 29 2.06

89.5%

92.4% 59 2.53

95.9%

76.1 13.3 0.7 0.3

11.9 3.0 52.2 14.9 10.4

ri

90.1 3.1 0.9 0.9 0.2

Pi

Day

-+ + +

0.70 0.26 0.94 0.97

-- 0.77 - - 0.10 + 0.96 + 0.89 + 0.94

Ei

91.9%

82.8 9.3 0.5 0.2

95.6%

90.8 3.8 0.7 0.1 0.1

Pi

92.4% 37 1.81

13.2 37.7 34.0 7.5

94.8% 27 2.50

5.3 5.3 50.0 5.3 28.9

ri

Night

-+ + +

0.72 0.56 0.96 0.95

--0.89 + 0.16 + 0.97 + 0.96 + 0.99

Ei

TABLE 9. CYCLOTHONE BRA UERI: THE MOST ABUNDANT IDENTIFIABLE COPEPODS EATEN AT 450 AND 600 m IVLEV'S ELECTIVITY INDICES (El) ARE CALCULATED. MEAN BODY LENGTHS ARE TAKEN FROM THE LITERATURE

c)

t'~

ca_

O

.<

408

H . S . J . ROE and J. BADCOCK

100 80

F'/,I= Full D=Y2Full

60

I"-I: Little gg= Empty

40 20

o,,¢ c

~ioo

g

u_

8C 6C 4C

2C

Time, GMT 00hrs

FIG. 10. Cyclothone braueri: percentage of stomachs in each haul which were e m p t y . , tained little food ~, where half full ~3, or lull ®.

con-

C. braueri (SL 26-36 mm) ate smaller prey than large fish, although the only identifiable prey in the few males (SL 19-21 mm) were small ostracods (2 stomachs), Clausocalanus (3 stomachs) and a single male M. lucens. There was little diel difference in the occurrence of food in Cyclothone stomachs (Fig. 10), nor in the incidence of fresh or digested food. The overall incidence of full stomachs was higher by day than by night at both depths, although there were no regular variations in the degree of fullness at either depth, and it was higher at 450 than at 600 m (% stomachs > ½ full at 450 m = 34.3 day, 17,3 night; 600m = 7.0 day, 4.0 night). The greater incidence of full stomachs at 450m was not due to an increase in the numbers of prey eaten at this depth (Table 8), but the overall size of the prey may have been larger. Actual prey specimens were not measured, but by taking the mean body lengths of the principal copepod prey (Table 9) with the numbers found in the stomachs, the overall mean size of the copepod prey was significantly larger at 450 than at 600m by day and night (p = 1% and 0.1% respectively). Regardless of whether C. braueri ate larger copepods at 450m, there is little evidence here for a diel feeding cycle; C. braueri consumed small amounts of food at any time of the day or night. Cyclothone were an important prey for decapod Crustacea (ROE, 1984a), and C. braueri was identified from the guts of Acanthephyra purpurea, A. pelagica, S. debilis and Sergia ?bisculcatus. Despite its abundance in the Atlantic and Mediterranean there is very little information on the diet of C. braueri and none on its feeding chronology. NUSBAUM-HILAROWlCZ ( 1 9 2 0 cited by MARSHALL, 1960) recorded fish scales and lenses from its gut but most of the data

5. Vertical migrations and feeding of fish

409

on Cyclothone feeding comes from studies on other species (e.g. MARSHALL, 1960; COLLARD, 1970; DEWlTT and CAILLET, 1972; LEGAND etal., 1972; GORELOVA and TSEITLIN, 1979; and GORELOVA, 1980). Small copepods and ostracods are the predominant prey although larger animals are sometimes eaten. Some authors (DEWITT and CAILLET, 1972; LEGAND et al., 1972) concluded that various Cyclothone spp. fed more by night than by day, which, in the case of C. acclinidens seems consistent with SMITH and LAVER's (1981) in situ measurements of increased respiration rate at night. On the other hand DEWlTT and CAILLET (1972) and GORELOVA (1980) found no diel differences in the feeding of several spp. and concluded that shallow living individuals fed more intensively than deep ones. GORELOVA (1980) also showed that smaller Cyclothone ate smaller prey than large ones and GORELOVA and TSEITLIN (1979) calculated digestion rates for four spp. and found that each species ate very little at any one time. The present results seem to be in accord with most of these observations. 4.2.4. Xenodermichthys copei. BADCOCK and LARCOMBE (1980) summarised the vertical distribution of X. copei from the area. They divided the population into 3 size-groups: metamorphic individuals (SL 9-32mm), juveniles/sub-adults (SL 33-99 ram) and adults (SL > 99 ram). By day the total population occurred between 400 and 800 m with metamorphic fish and juveniles throughout the depth range and adults below 500 m. At night the depth range was 200-800 m; some individuals of all groups moved upwards but adults migrated furthest. Specimens in the 48 hr series were divided into two groups - sexually indeterminate (SL 9-37 ram) and sexually determinate (SL 36-170 ram) (Table 10), which correspond to BADCOCK and LARCOMBE's (1980) metamorphic group and to their juvenile and adult groups respectively. During metamorphosis Xenodermichthys changes from a structurally feeble fish to one which is relatively robust and presumably more capable of making extensive migrations. The sexually indeterminate group were more numerous than the larger fish and were most abundant at 450 m (Table 10, Fig. 11). There is no evidence for vertical migration in this group at either depth, the mean number per haul by day and night at 450 and 600m being 0.6:0.7 and 0.5:0.5 respectively.

250 m

E0 3 0 0

m

ra

mn

m

z:

m

i

. . . . . . . . . . .

1

)})

'

i 9

FIG. l 1.

[] 13

...........'niiiliit 17

21

Xenodermiehthys copei:

1 5 9 13 Time G M T , 0 0 hrs

17

21

1

5

9

numbers of i n d i v i d u a l s / h a u l / 1 0 , 0 0 0 m3 of water filtered; 48 hr series data. cJ = sexually indeterminate, • = sexually determinate.

9-37 11-20

9-37

0 55 35

90

250 450 600

Range

No.

15.1

15.7 14.1

Mean

17

7 7 3

No.

36-163

47-161 36-51 142-163

Range

Size

Size (mm)

Depth (m)

Males

Sexually Indet.

87.0

102.3 43.6 152.7

Mean

3

0 3 0

No.

39-49

39-49

Range

44.0

44.0

Mean

Ovarian Stage I Size

6

2 3 1

No.

42-93

89-93 42-53 64

Range

Stage II Size

Females

64.3

91.0 48.3 64.0

Mean

13

8 2 3

No.

TABLE 10. XENODERMICHTHYS COPEI: THE NUMBERS AND SIZES OF EACH STAGE AND SEX CAUGHT

101-170

110-170 101-155 116-143

Range

Stage III-V Size

136.6

140.5 128.0 132.0

Mean

4~

O

O

O

5. Vertical migrations and feeding of fish

411

TABLE 11. XENODERMICHTHYS COPEI: ANALYSIS OF STOMACH CONTENTS OF SEXUALLY INDETERMINATE FISH; SEE LEGEND TO TABLE 2 450

Depth (m) Day/Night

D

No. Examined No. with Food gE (mm)

26 18 15.4

600

N

Total

D

N

Total

28 12 16.0

54 30 15.7

18

17

8 13.5

9 14.3

35 17 13.9

No. of Fish with Prey

No. of Prey/Fish

Freq. of Occ. of Prey %

Depth (m)

450

600

450

600

450

Prey Euphausiid larvae Copepods Ostracods Coelenterates Radiolaria Chaetognaths Digested debris

5 8 3 6 5

3

0.2 0.3 0.1

0.2

15

5 6 1 12

16.7 26.7 10.0 20.0 16.7

0.06 50.0

600

17.6 29.4 35.3 5.9 70.6

In the sexually determinate group there was a gradation in size with depth and an extensive vertical migration. At 6 0 0 m they were present only by day (Fig. 11) and 6 of the 7 specimens were adults > 99 mm SL (Table 10). At 450 m they occurred mainly around sunset and sunrise and only 2 o f the 15 specimens were adult, and at 2 5 0 m they occurred only at night and 12 of the 17 individuals were adult. The data suggest that the largest fish were deepest by day and consequently had a more extensive vertical migration than the intermediate (sub-adult) forms. 4.2.4.1. Food and feeding - The food and feeding of the two groups has been examined separately because of their different distributions and behaviour. (a) Sexually indeterminate: The results of the stomach content analyses are shown in Table 11. At both depths the stomachs usually contained only single, small, prey items; copepods, coelenterates and radiolarians predominated. Seven copepods were identifiable in stomachs from 450 m, six Oncaea sp. and one small Pleuromamma sp., and a single Oncaea at 600 m; Coelenterates and Radiolaria were recognised from nematocysts and spicules respectively. The incidence of full stomachs was higher during the day at both depths, but the data are sparse. (b) Sexually determinate: The results of the stomach analysis are shown in Table 12. As far as can be determined, the diets of subadults (< 99 mm SL) and adults ( > 99 m SL) were the same, but the sample size is rather small. Prey was very varied, ranging from micronektonic decapods and euphausiids (e.g. Systellaspis debilis, Meganyctiphanes norvegica, Nematoscelis megalops) to planktonic copepods (e.g. Oncaea, M. lucens, U. plumosa) and Radiolaria. The latter had branching spicules embedded in a greenish debris, typical of the phaeodarians eaten by decapods (ROE, 1984a). Because some of the prey is sampled by the RMT 1 and some by the RMT 8 it is not possible to calculate electivity indices for Xenodermichthys. The consumed prey was typical of the plankton and micronekton occurring at each depth by day and/or night and indicates that feeding occurred at 2 5 0 m by night and also at 6 0 0 m during the day. The incidence of stomachs > ~ full was highest at 2 5 0 m (46.7%) but the data are very few.

250

Depth (m)

3 1 5

3

2

3 8

0

No. Examined No. with Food SL (mm)

Prey Decapods Euphausiids Mysids Amphipods Ostracods Copepods Chaetognaths Coelenterates Gelatinous Debris Radiolaria Digested Debris

N

D

Day/Night

6 7

4 3 1 2

1

450

No. of Fish with Prey

16 15 118.6

250

Depth (m)

1 2 3 3

I 1 1 3

1

600

16 15 118.6

Total

0.2

0.3

0.2 0.9

250

3 2 38.7

D

0.4 0.4 0.1

0.1

450

No. o f Prey/Fish

11 8 66.2

N

450

1.3

0.2 0.2 0.2 2.0

0.2

600

14 10 55.9

Total

20.0 6.7 33.3

20.0

13.3

20.0 53.3

250

7 6 131.1

D

7 6 131.1

Total

60.0 70.0

40.0 30.0 10.0 20.0

10.0

450

16.7 33.3 50.0 50.0

16.7 16.7 16.7 50.0

16.7

600

Freq. of Occ. o f Prey %

0

N

600

T A B L E 12. X E N O D E R M I C H T H Y S COPEI: ANALYSIS O F S T O M A C H C O N T E N T S OF S E X U A L L Y D E T E R M I N A T E FISH; SEE LEGEND TO T A B L E 2

0

e~

g

0

5. Vertical migrations and feeding of fish

413

The diet of both groups of Xenodermichthys was distinct from the other fish spp. examined in containing a high proportion of coelenterates and Radiolaria. In these respects it was similar to that of the mysid Eucopia and to some decapods (ROE, 1984a). By day, large X. copei may be relatively inactive (BADCOCK and LARCOMBE, 1980) and both the feeble metamorphic fish and sluggish large individuals may browse upon inactive prey or debris - which may account for the presence of surprisingly small copepods (e.g. Oncaea) in the stomachs of large fish. Metamorphic X. copei were themselves eaten by the decapod S. debilis (ROE, 1984a). As far as we are aware there are no other systematic accounts of feeding in this species; BEEBE (1933) recorded that the stomach of one individual was full of "a finely digested shrimp" and MAUCHLINE (1981) found that one fish had eaten a mysid, Boreornysis rnicrops. 4.2.4.2. Parasites - Sporozoa occurred in the hind guts of every individual larger than 37 mm SL, their numbers ranging from "a few" to "several thousands". Cestodes were found in the pyloric caecae of 41% of the 36-170 mm group and in one 37 mm metamorphic fish. Up to six tapeworms per fish were recorded. Single nematodes occurred on the stomach wall and pyloric caecae of two individuals. This infestation by parasites is unique in this series. MARKLE and WENNER (1979) recorded trematodes in X. eopei but found neither sporozoa nor cestodes. 4.2.5. Stomias boa ferox, Chauliodus sloani, C. danae. These three species are considered together because their migratory and feeding behaviours were very similar. 4.2.5.1. Vertical distribution - S. boaferox and C sloani are large temperate species which are relatively poorly sampled by the RMT 8. C danae is a smaller and more subtropical species which was very scarce at 44°N 13°W. On a few specimens ofS. boaferox were caught in the vertical series, from between 500 and 700 m by day and between 10 and 900 m by night. Subsequent sampling at this position showed that by day most individuals lived between 400 and 600 m and that by night some of them remained at depth and did not migrate. In the 48 hr series S. boaferox occurred mainly at 450 m by day and had a distinct migration up to at least 100 m depth at night (Table 1, Fig. 12). Virtually the entire population migrated, leaving 450 m in the afternoon and arriving at 100 m after sunset, and subsequently leaving 100 m before sunrise and returning to 450 m later in the morning. Most specimens were juveniles; one female was mature (SL 312ram), and only four large males were caught (SL 146-243 mm) (Table 13). There is limited evidence of depth stratification

100m

% O

250 m

[i!iii!iiiiiiiiiiii!i!iiiilililiiii!iiiii!!iiiiiiili

o.

r7

O

z

17 17

n [7 ~

!iii!iiiiiiiiiiiiiiiiiiiii~!iiiiiiiiiiiiiiiiii!iiii!iiI-1 [1 m M

600m 9

filiiiiiili!i!ii!!iii!ilil)iiii!i!i!i!iiiili!i!ilili!)ili!i!ilili!iiiil

iiiiiiiiii!~iiiiiiiiiiliiiiiiiiiiiiiiiiii!ii!iiiiii| r~

r7

,

...... iiiii~i~iiiiiiiiiiiiiii~i!iiii!iii!iiiii~i~i~iiiiiiiiiiiiiiiiiiiiiiiiiiiiiJ7

!i!i i i i i i i~i i i~i iiiiiiiiiii~''~iii~i; iii r7

ii:iiiiiiiilili!i!iiiii

N 13

" 17

21

~:~,~:~,~:i:iii 1 5

I-7 9 13 Time G M T , 0 0 h r s

17

'iiiiiiiliiiiiii!i!ili!~i~:.................. 21 1 5

9

FIG. 12. Stomias boa ferox: n u m b e r s o f individuals/haul/lO,OOOm 3 ot water filtered; 48 hr series data.

No.

6 5 27 2

Depth (m)

100 250 450 600

80-122 65-113 64-243 146-232

Size Range ( m m )

Males

96.1 90.0 97.9 189.0

Mean Size

2 4 1

No.

II I+II III/V

Stage

72-100 74-89(I)89(II) 312

Size Range ( m m )

Females

86 79.7(I)89(II) 312

Mean Size

T A B L E 13. S T O M I A S BOA F E R O X : N U M B E R S O F EACH SEX C A U G H T AT EACH DEPTH; T H E I R SIZE RANGE, MEAN SIZE AND STAGE O F O V A R I A N D E V E L O P M E N T (4 s p e c i m e n s were not sexed)

t~ ©

e~

0

4~

4~

5. Vertical migrations and feeding of fish

415

TABLE 14. CHAULIODUS SLOANI: NUMBERS CAUGHT, SIZE AND OVARIAN STAGE Males Depth (m)

No.

100

Size Range (ram)

10

25O 450 600

113-165

E

4 1 15

12t-200 197 113-200

Females No.

Stage

Size Range

1

II

155

1 2

II I

184 78-175

4

I-II

78-184

with size. By day the size range at 450 m was 64-109 m SL (mean 84.3 mm) whereas at 600 m it was 146-312 mm SL (mean 230 mm), and no individuals larger than 134 mm SL were caught above 450m depth by night. Catches from bigger nets elsewhere in the N.E Atlantic (BADCOCK and MERRETT, in prep.) suggest that large individuals may live deeper than small ones, but the data are too few to ascertain whether this effect is real or due to net avoidance. Nineteen specimens of C. sloani were caught (Table 14) and the limited data indicate a distribution and migration similar to that of Stomias (Table 1). C danae was even scarcer; only six fish (SL 122-165mm) were taken (Table 1) that merely confirmed an extensive nocturnal migration as found elsewhere (e.g. BADCOCK and MERRETT, 1976). 4.2.5.2. Food and feeding - The most conspicuous feature of the stomach and gut analyses was the general absence of food. In Stomias the stomachs of 48 fish were examined and the guts of 46 of these. Only two stomachs contained food (a single copepod, Pleuromamma robusta, from a 9 fish, SL 101 mm, taken at 250m, and an ostracod in a d SL 81 mm from 450 m). Three of the seven guts at 100 m and 10 out of 30 at 450 m contained digested fish and crustacean remains. The stomachs of all 19 C sloani and the guts of 17 fish were opened. The stomachs of two at 100 m contained fish remains (in one there were five eye lenses), and the guts of three at 100 m and one at 450 m contained unidentifiable digested fragments. None of the C. danae stomachs or guts contained any food. There have been relatively few observations on the food and feeding of these or related species. Fish are the most frequently recorded prey but decapod Crustacea, euphausiids and copepods have also been found (LEGAND and RIVATON, 1969; COLLARD, 1970; BORODULINA, 1972; MERRETT and ROE, 1974;APPELBAUM, 1982; CLARKE, 1982). A change in diet with increasing size has been found in C. sloani (CLARKE, 1982); Chauliodus larger than 120 mm SL were exclusively piscivorous whereas smaller Chauliodus ate euphausiids as well. A stomiatoid has been observed feeding upon krill in the Antarctic (CLARKE, 1950). The ability of C. sloani and C. danae to swallow relatively enormous prey has been commented on by, for example, ZUGMAYER (1911), LEGAND and RIVATON (1969) and MERRETT and ROE (1974). CLARKE (1982) found that the size of fish eaten by C. sloani was up to 63% of the standard length of the Chauliodus. TCHERNAVIN (1953) analysed the feeding mechanics of C. sloani and described two feeding methods, one using the modifications of the skull, anterior vertebrae and branchial apparatus to swallow large prey, and the other a more passive feeding on smaller prey (ca. 5 mm), involving the retention of prey within its mouth by the teeth on its branchial arches. The three species discussed here probably all feed in the same way (MORROW, 1964), perhaps feeding sporadically whenever the opportunity arises.

416

H.S.J. ROE and J. BADCOCK

In addition to their modified jaw mechanisms they have distendible stomachs, and it has been suggested that they may also have rapid digestion rates (BEEBE and CRANE, 1939; MARSHALL, 1954; LEGAND and RIVATON, 1969; MERRETT and ROE, 1974; CLARKE, 1982). LEGAND and RIVATON (1969) placed these predators into atrophic level B as opposed to the planktivorous fish in trophic level A. The percentage of empty stomachs in these fish is usually much higher than in those of trophic level A (LEGAND and RIVATON, 1969; BORODULINA, 1972 ; MERRETT and ROE, 1974; CLARKE, 1982), and the present results in which only 4% of Stomias and 10% of C. sloani had food in their stomachs are in keeping with previous observations. Prey was more frequent in the guts than in the stomachs here but there are no comparable data in the literature. The virtual absence of food in the stomachs of these 3 species is difficult to explain. It is unlikely that they vomited freshly eaten large prey since they all have backward pointing teeth not only on their jaws but also on the palate, and, in Stomias, on the vomer. In addition, at least in Chauliodus, the head contortions necessary to swallow such prey are probably not reversible. Digested food could presumably be vomited or voided as faeces and BORODULINA (1972) observed that "digested remains of the stomach contents were often found in the oral cavity". Nevertheless, freshly eaten food is unlikely to be digested within the fishing time. It seems more likely that these fish eat large prey rather rarely, a conclusion also reached by TCHERNAVIN (1953) from a consideration of their blood circulation and respiration. Small prey could be eaten more frequently and their scarcity in the stomach could be due to vomiting because they would not necessarily be retained by the large teeth. Indeed TCHERNAVIN (1953) suggested that such prey entered the mouth of Chauliodus with the respiratory current. In at least one large mouthed, large fanged fish (Alepisaurus) the stomach contents can be removed by merely holding the fish up by its tail and shaking it. (MATTHEWS, DAMKAER, KNAPP and COLLETTE, 1977), and perhaps in the stress of the trawl small prey simply fall out of the stomachs and mouths of these fish. 5. DISCUSSION AND CONCLUSIONS As discussed previously (ROE, 1974; PEARRE, 1979; and the present series of papers)only regular, coherent, diel vertical migrations can be shown from data sets such as those presented here. Distinction between non-migrants and irregular migrants cannot be made, nor can migrations occurring over a longer time-scale be identified. Indeed, both net catches (e.g. CLARKE, 1973; BADCOCK and MERRETT, 1976; FROST and MCCRONE, 1979) and submersible observations (e.g. BARHAM, 1970; CLARKE, 1970) have shown that some individuals can remain at depth during the night whilst the bulk of their population migrates upwards. Most species examined here were represented too sporadically in the samples to analyse fully (Table 1), but for the more abundant species the data are extremely consistent. Fourteen days elapsed between the 450 and 100m samples and 10 days between those at 450 and 250m, but despite these intervals the migration patterns were remarkably repetitious. Such repeatibility is a feature found in the data for other taxa of this series (ROE, 1984a, b; ROE, JAMES and THURSTON, 1984) and inspires considerable confidence in the validity of each individual sample set. Mean depth profiles have shown that many invertebrate taxa of this series spent much of their time undergoing diel vertical migrations (ROE, 1984a, b; ROE, JAMES and THURSTON, 1984). Fast swimming periods over sunrise and sunset alternated with periods of much slower vertical movement and, thus, only for short periods of the diel cycle can migrant animals be

5. Vertical migrations and feeding of fish

417

regarded as inhabiting a "typical" day or night depth. The application of mean depth profiles to the fish is inappropriate since the sampled depth range did not encompass the entire migratory ranges of the more abundant migrant species. Nevertheless, the data suggest that B. glaciale and perhaps S. boa ferox and large X. copei may behave in a similar way. Similar, almost continuous migratory movements has been suggested for other fish by LEGAND et al. (1972)and ROE (1974). Such behaviour does not necessarily conflict with submersible observations of lethargic fish. BARHAM (1970) pointed out that since a submersible was a moving platform it was difficult to verify that lethargic individuals were remaining at a constant depth. Any vertical movement around midday or midnight will probably be slow and possibly overlooked in short periods of observation from a mobile submersible. Light has been discussed in connection with the distributions of many species in this series (e.g. ROE, 1984a, b) and it has often been implicated in the migratory behaviour of fish (see WOODHEAD, 1966; BLAXTER, 1970, 1975 for reviews). ROE (1983) has recently concluded that specific isolumes cannot closely control the depth distributions and/or migrations of the populations of several species of fish, including B. glaciale, A. hemigymnus and C. braueri. The present data support this conclusion - any vertical movement made by A. hemigymnus or C. braueri is far less than that required to compensate for the diel changes of light, and the populations of X. copei, B. glaciale and S. boa ferox were distributed over relatively broad depth horizons by day and/or night. There are clearly considerable inter- and intraspecific differences in the migratory behaviour of the present fish, and there are similar differences in their feeding. At least two species (B. glaciale, A. hemigymnus), fed cyclically, although the interpretation of cyclic feeding from the presence or absence of fresh and/or digested food is difficult. The digestion rates of mesopelagic fish are unknown (HOPKINS and BAIRD, 1977), but Crustacea will presumably be digested more slowly than soft bodied prey and their presence in a stomach may reflect a slow digestion rate rather than active feeding (TYLER and PEARCY, 1975; CLARKE, 1978; PEARCY, LORZ and PETERSON, 1979). Different resistance to digestion could not only bias prey identification towards resistant animals (CLARKE, 1978, 1980), but could also affect the interpretation of cyclic feeding (JENKINS and GREEN, 1976). It is possible, for instance, that the partially digested large calyptopes larvae found in the Benthosema caught at 450 m by day could have been eaten at some shallower depth during the night. Similar blurring of definite on/off feeding patterns could also result from dietary contamination. Net feeding is apparently unimportant here, but a low level of net feeding may have been interpreted as natural predation, and the presence of fresh food in stomachs could have been considered to be active feeding at a time when the fish was naturally only digesting previously eaten prey. The low level of feeding ofB. glaciale at 250 m during the day could, for example, be an artifact. In view of the above it is impossible to draw firm conclusions on feeding periodicity from limited data sets such as the 450 m (by day) population of B. glaciale and the two groups of X. copei. Nevertheless it seems clear that all size groups of Benthosema fed during the night, and that at least the smaller individuals living at 250 m by day ate very little (if anything) during the day. The other cyclic feeder here was A. hemigymnus, the whole population of which fed mainly during the afternoon and early part of the night. The reasons for cyclic feeding are obscure. For a long time it has been supposed that vertical migrations are closely associated with feeding (e.g. MARSHALL, 1954, 1960). HOPKINS and BAIRD (1977) found distinct feeding cycles in many migrants which rose to depths shallower than 200m at night but more varied feeding patterns in species which remained at greater depths. This and subsequent work (e.g. OZAWA, FUJII and KAWAGUCHI, 1977; GJOSAETER,

418

H . S . J . ROE and J. BADCOCK

TABLE 15. MEAN NUMBERS/1000m 3 OF METRIDIA LUCENS 1N HAULS SPANNING SUNSET AND SUNRISE AT 100m AND PRESUNSET AND POST SUNRISE AT 250 m, DAYS 1 AND 2 COMBINED. THE "CONCENTRATION FACTOR" IS THE INCREASE IN NUMBERS BETWEEN 100 AND 2 5 0 m ; THE ARROWS INDICATE THE DIRECTION OF MIGRATION

100 m 250m

Sunset Conc.

Sunrise Conc.

10280.35

12711.14

6982.62

~ + 1.5 I

12113.37

| + 1.05

1978b, d; TSEITLIN and GORELOVA, 1978; CLARKE, 1978; WORNER, 1979; IMSAND, 1981a; HOPKINS and BAIRD, 1981; BAIRD and HOPKINS, 1981a, b) has shown that generally fish migrate from depths of low prey density to depths of high prey density (or to a preferred prey species), in which case they feed mainly at night; or the fish and prey cohabit by day and the prey migrates away at night, in which case the fish feeds mainly by day. Benthosema migrated to some depth between 100m and the surface at night, when it fed mainly upon euphausiid larvae, M. lucens and Clausocalanus. Euphausiid larvae were not routinely analysed from the RMT1 catches but copepods were. M. lucens was abundant at 250m by day and migrated to the surface at night (ROE, 1984b). The mean numbers of M. lucens per 1,000m 3 of water filtered were:- at 450m 1,211 (day), 1,298 (night); at 250m 8,436 (day), 396 (night) and at 100 m, 255 (day) and 3,765 (night). The night figure at 100 m is probably an underestimate of the numbers available between 100m and the surface at this time, because an unsampled population of Metridia which lived between 250 and 100 m by day, migrated into the upper 100 m at night (ROE, 1984b). Some estimate of the numbers involved can be obtained by comparing the numbers caught in the presunset and postsunrise hauls at 250m with those taken in the sunset and sunrise hauls at 100m (Table 15). On average the numbers arriving at or leaving from 100 m were 1.2 times larger than those at 250 m, indicating that the M. lucens living between 100-250m numbered at least one fifth of those living at 250 m. The migrant population of M. lucens was therefore concentrated from a daytime depth range of 150m into one of 100m or less, and presumably the nearer the surface it got the more concentrated it will have become. Similar estimates could be given for Clausocalanus. Thus Benthosema's principal prey concentrated near the surface at night and the fish migrated with it and fed upon it at this time. Prey concentration provides an answer for night-time feeding but does not account for daytime fasting, especially at 250 m. Why should B. glaciale migrate 200 m at night to feed upon prey which it could eat during the day without migrating at all? The density of M. lucens at 250m by day (8.3 m -3) is far higher than any prey density calculated by CLARKE (1980), whose feeding study included the related Benthosema suborbitale. Even the daytime density at 450 m (1.2 m -3) is relatively high, and it is therefore unlikely that the daytime abundance ofM. lucens was below any critical threshold value of prey density. Whether the metabolic cost of migration is high (TORRES, BELMAN and CHILDRESS, 1979) or low (MARSHALL, 1971), the feeding strategy of B. glaciale seems energetically wasteful. The temperature difference between the surface and 250m was very small (ROE et al., 1984) and there is no obvious metabolic advantage, sensu MCLAREN (1963, 1974), ENRIGHT (1977) to the migrations of Benthosema. Perhaps the nocturnal concentration of

5. Vertical migrations and feeding of fish

419

high prey density to even higher values is biologically significant and it may simply be easier to feed amongst more concentrated prey (ROE, 1984a). A similar noctural prey concentration was encountered by migrant X. copei, which moved from a euphausiid concentration of around 30 per 10,000m 3 to a night-time density of at least 150 per 10,000m 3 (ROE, 1984a, his Table 3). The period of most active feeding in A. hemigymnus also coincided with a diel prey difference, although in this case it was achieved solely by the prey (copepods and chaetognaths) migrating whilst the fish remained stationary. Of the present acyclic feeders most data are available for C braueri, which ate a little at a time by both day and night. Feeding was more intensive at 450 m than at 600 m in terms of stomach fullness, though not in terms of numbers of prey taken. It has been suggested that C. signata migrates erratically and feeds whilst at shallow depths (DEWITT and CAILLET, 1972). Such behaviour could occur in C braueri but the present data are inadequate to resolve this problem. The diets of all the abundant fish here showed evidence of selection either from what they ate or from what they did not eat. The interpretation of selectivity is fraught with potential pitfalls (e.g. HYATT, 1979) and the use of Ivlev's Electivity Index has been criticised by several authors e.g. O'BRIEN and VINYARD (1974), GRAS and SAINT-JEAN (1982). PEARRE (1982) has recently reviewed various indices of prey preference and concluded that no single index is completely satisfactory. The changing distributions of predator and prey have been examined concurrently and repeatedly here, thereby providing a detailed picture of prey availability at each depth throughout the diel cycle. However, various groups of potential prey are either inadequately sampled by the RMT 1, or were not analysed (e.g. cyclopoid copepods, Radiolaria and larvae of most groups) and consequently the apparent proportional availability of the analysed groups in the plankton (Table 4) will be overestimated. Conversely, because of the fragmentary nature of much of the prey, the numbers of individual prey species in the stomachs may be underestimated. The calculated electivity indices will therefore be inaccurate, but their use does provide some sort of comparative yardstick. Planktivorous fish rely upon visual predation (O'BRIEN, 1979; HYATT, 1979) and size selection is common in inshore and freshwater fish. Data for mesopelagic species are scarcer (HOPKINS and BAIRD, 1977), but recent results (e.g. CLARKE, 1980; BAIRD and HOPKINS, 1981) suggest that it also occurs frequently in these fish. The present A. hemigymnus, B. glaciale and C braueri probably all selected their prey according to size. Ontogenetic changes, or increasing the size and sometimes type, of prey with increasing size of predator have often been reported in midwater fish (HOPKINS and BAIRD, 1977, 1981 ; GORELOVA, 1975, 1978, 1980; WORNER, 1979; ROWEDDER, 1980; CLARKE, 1980, 1982; KAWAGUCHI and MAUCHLINE, 1981) although it is difficult or impossible to distinguish such changes flora size selection. X. copei had a distinct change in diet with age, but whether this is simply a matter of size is impossible to say. Apparent taxonomic selection may also be size related. The increasing importance of chaetognaths in the diet of larger A. hemigymnus may be due to size rather than increasing preference for chaetognaths, but where the disproportionately eaten prey is smaller than, or the same size as the available prey then taxonomic selection seems to be operating. Such may be the case for B. glaciale and euphausiid larvae here, and previous examples have been given by MERRETT and ROE (1974), CLARKE (1980), BAIRD and HOPKINS (1981a) and IMSAND (1981b). None of the present fish ate a complete spectrum of potentially available prey, even to group level. Ostracods for example, were very poorly utilised despite being relatively abundant at

420

H.S.J. ROE and J. BADCOCK

450 and 600 m by day and night and at 250 m during the night (Table 4). Within the different groups very few of the available species were eaten, e.g. 41 species of copepod were recorded at 100 m during the night (ROE, 1984b) but B. glaciale ate only 10 of these; C. braueri ate 5 and 7 species of copepod at 450 and 600 m out of a potential total of over 70. Unsampled, smaller plankton were not eaten at all, and these restricted diets mean that a considerable part of the available planktonic biomass was bypassed by these fish. Although there is some overlap between the diets of the three main planktivorous species, their feeding preferences and time and place of feeding were different. B. glaciale fed by night at 100m on M. lucens and euphausiid calytopes, A. hemigymnus fed in the evening at 250m on chaetognaths and assorted copepods, and C. braueri ate mainly different copepods at all times at 450 and 600m. Similar resource partitioning has been reported before (see, for example, HOPKINS and BAIRD, 1977; CLARKE, 1980, 1982), and no doubt different distributions, migrations and feeding behaviour all interact to reduce competition between species. 6. SUMMARY (i) Vertical distributions, diel migrations and feeding of fish caught at 44°N13°W are described. Seven species are considered in detail - Benthosema glaciale, Argyropelecus

hemigymnus, Cyclothone braueri, Xenodermichthys copei, Stomias boa ferox, Chauliodus sloani and C. danae. (ii) The analysis is based mainly on samples taken at four depths, 100,250,450 and 600 m, each of which was fished repeatedly for a continuous period of 48 hr. Supplementary data from other series fished in the same position is also considered. (iii) Up to 14 days elapsed between the samples at the various depths of the 48hr series, but despite this delay the data are extremely repetitious. This great repeatability gives considerable support to the validity of each individual sample set. (iv) Net feeding is discussed and considered to be unimportant here. (v) B. glaciale was the most abundant distinct migrant. By day young, small individuals predominated at 250m and older, larger fish at 450m; at night all size groups migrated up towards the surface. (vi) Small, shallow living Benthosema fed cyclically, taking prey at night and digesting it by day. Larger deeper living fish also fed during the night and there is slight evidence for additional daytime feeding in this group. (vii) A. hemigymnus showed little evidence for vertical migration; feeding was cyclic, occurring mainly in the afternoon and early night. (viii) C. braueri was the most abundant fish caught but evidence for a limited vertical migration for part of the population at 450 m is equivocal. (ix) Feeding in C. braueri was acyclic; a small amount of food was eaten by both day and night. Feeding was more intensive at 450 m than at 600 m. (x) Different size and/or age classes of X. copei showed a gradation in vertical distribution and migratory behaviour. (xi) Small, sexually indeterminate individuals of)(. copei occurred at 450 and 600m and did not migrate. Larger, sexually determinate fish migrated between at least 600 and 250m. The different classes had different diets. (xii) Crustacea formed the basic diet of most of these fish but Xenodermichthys was unique in eating Radiolaria and in being heavily parasitised by cestodes and sporozoa.

5. Vertical migrations and feeding of fish

421

(xiii) Stom&s, C sloani and C. danae are presumed to feed erratically and rarely upon large prey but may take small prey more often. (xiv) Vertical migration may have been continuous for much of the diel cycles of the 3 most abundant migrants, Benthosema, Stomias and large Xenodermichthys. (xv) The influence of light upon vertical migrations is discussed. Absolute light levels cannot closely control the distributions and migrations of any of the fish populations described here. (xvi) All cyclic feeding here coincides in both time and space with maximum prey density, achieved either by the fish migrating to the prey or by the fish remaining static whilst the prey migrates to it. (xvii) Selectivity is apparent in the feeding of all the planktivorous fish here. Selection may have been based upon size (B. glaciale, A. hemigymnus, C braueri) and/or taxonomy (B. glaciale,

A. hernigyrnnus). (xviii) A considerable part of the available plankton was not utilized by these fish. Acknowledgements-We would like to thank our colleagues at the Institute of Oceanographic Sciences for identifying the various prey items; Dr. M. V. Angel (ostracods), Miss K. Chidgey (chaetognaths), Mr. P. T. James (euphausiids), Miss P. A. Kirkpatrick (siphonophores), and Mr. M. H. Thurston (amphipods).

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