Changes in predation by the juvenile goby deltentosteus quadrimaculatus (teleostei, gobiidae)

Netherlands aTournal of Sea Research 14 (3/4) : 362-373 (1980)

CHANGES IN PREDATION BY T H E J U V E N I L E GOBY DELTENTOSTEUS Q.UADRIMACULATUS (TELEOSTEI, GOBIIDAE) by L. V I L L I E R S Direction des Gentres d'Exp~rimentations Nucldaires ( DIRCEaV) , Service Mixte de Gontr61e Biologique, B.P. 16, 91310 Montlbdry, France

CONTE~,ITS I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . II. Locality and Techniques. . . . . . . . . . . . . . . . . . . . . a. Study area . . . . . . . . . . . . . . . . . . . . . . . . . b. Material and Methods . . . . . . . . . . . . . . . . . . . . III. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . a. Changes in food composition in relation to growth . . . . . . . . b. Changes in food composition in relation to depth . . . . . . . . . c. Size relation between predator and prey . . . . . . . . . . . . . d. Relation between the mean weight of stomach contents and the size and weight of Ddtentosteus quadrimaculatus . . . . . . . . . . . . . IV. Discussion and Conclusions . . . . . . . . . . . . . . . . . . . V. Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . VI. References. . . . . . . . . . . . . . . . . . . . . . . . . . .

362 363 363 364 364 364 365 367 369 369 371 371

I. I N T R O D U C T I O N Most studies on the dynamics of bottom faunas during recent years (BLEGVAD, 1917; L~.BOUR, 1918, 1919, 1920; SnORYIOZN, 1939; PORUMB, 1961; Muus, 1967; GII~ON, 1968, 1969; CASABIANCA ~K KmN~.R, 1969; HmTHAGEN, 1971, 1975, 1977; HEALEY, 1971, 1972; FONDS, 1973; MCGRATH, 1974; MXLLER, 1975; NEKR~SOVA& KOVTUN, 1976; GIBSON & EzzI, 1978; BERG, 1979) stress the considerable importance of small fish, particularly Gobiidae. The work by BODIOU & VXLLI~.RS(1979) and VmLmRS (1979) have shown the ecological interest of the juvenile stages of Deltentosteus quadrimaculatus which prey on the meiobenthic populations, especially on harpacticoid copepods. When their density is high, they can constitute an important link in the littoral food chains. Here an attempt is made to establish the importance of the species from a study on its stomach contents at group level. Acknowledgements.--The author is most grateful to J. Soyer, Director of the Laboratoire Arago, Banyuls-sur-Mer, who encouraged him in

363

P R E D A T I O N BY J U V E N I L E GOBY

his research and provided all the material facilities. He also thanks J. Y. Bodiou for his friendly and constructive help, W. Delahaye for the drawings and Mrs M. Delahaye for translating the text into English. II. LOCALITY AND TECHNIQUES a. STUDY AREA

Samplings were made in the bay of Banyuls-sur-Mer, Pyr6n6es Orientales, France (Fig. 1) on well-sorted fine sands (PERES & PICARD, 1964). This biotope corresponds for the macrobenthos to the community of Spisula subtruncata (GuILLE, 1970) and for the meiobenthos to the community of Halectinosoma herdmani and Harpacticus flexus (SoYER, 1970) which is identical to that of Bovlog & VILLIERS (1979). From mid-April to December 15 samplings were carried out, i.e. each week as long as the post-larvae arrive, then each fortnight and finally each month. Five transects were sampled that correspond to the isobaths of 3, 5, 10, 15 and 20 metres (Fig. 1). Trawlings lasted 10 minutes at constant speed (0.8 m.s-t). 3 °08

•

•

I

4 2 o29-

BANYULS- SUR- MER

AtlmDfl©

Oeealn

FRANCE

~ ITALY It,~

I O

I

I 5OOn~

I

Fig. 1. Geography of the area and the sampling transects at the depths of 3, 5, 10, 15 and 20 metres. Symbols indicate gravel (B), well-sorted fine sands (A) and muddy sands (O).

364

L. VILLIERS b.

MATERIAL

AND METHODS

The young gobies are caught with a small iron-framed bottom trawl with a rectangular entrance (86 × 33 cm) (designed and made by technicians of the Laboratoire Arago; LABAT, 1976), netting with 4 m m mesh size, at the codend 0.5 ram. Catches are fixed at once in a 5% formol solution. Digestion stops immediately by blocking of the enzymatic activities. The ichthyological material is sorted in the laboratory and the total length of each fish is measured to the nearest mm. Subsamples of 30 gobies per transect are selected at random for stomach analysis. The stomach is extracted by cutting the oesophagus above the heart and at the first fold of the digestive tract. The stomach contents of 1128 gobies are analysed, using a binocular microscope. The various preys are measured with an ocular micrometer and isolated according to taxonomic group. The dry weight of the preys is determined after oven drying at 70 ° C for 48 hours. To assess the difference in nutrition of the zoological groups a food index I.A. (indexe alimentaire; LAUZANNE, 1975) is used which takes the frequency (0) and weight (W) percentages of the preys into account: I.A. = OW/IO0 in which O is the percentage of stomachs in which a prey occurs in relation to the total number of stomachs containing food, and W the weight percentage of a (group of) prey occurring in one whole sample in relation to the total weight of the preys consumed. LAUZANNE (1976) distinguishes secondary (0 < I.A. < 10), important (10 < I.A. < 25), essential (25 < I.A. < 50) and dominant (50 < I.A. < 100) preys. Food diets have been determined for fish of 10 to 60 ram, classes differing by 5 mm. IlI. a. CHANGES

IN FOOD

RESULTS

COMPOSITION

IN RELATION

TO GROWTH

The 3388 preys counted belong to 11 zoological groups, of which 7 are crustacean orders. The results (Fig. 2) confirm our former observations (BoDiou & VILLXERS, 1979). The juvenile stages of Deltentosteus quadrimaculatus feed exclusively on secondary producers of which crustaceans largely predominate in frequency (75% to 98%) and in weight (85%). The food indices of the prey groups vary with the size of the gobies; 3 categories can be seen: (1) when the gobies are less than 20 m m in length, they are almost exclusive zooplankton eaters (71.4% I.A.); (2) when 20 to 25 mm, they adopt a mixed diet (Fig. 2a and b) in which amphipods (16.5% I,A.) and harpacticoid copepods (9.5%

PREDATION

BY JUVENILE

365

GOBY

T.A.

I,A.

SO-

80. a.

b. AMPHIPODS

COPEPODS 60-

60-

40-

20-

20-

/

0

0

Goby (ramI

Goby (mm)

10

I.A.

¢.

Z.A.

POLYCHAETES

10

I

d.

MYSIDS

Goby (mm)

10-

.

Goby (ram)

10

0

f.

DEC A P O D S

0 Goby (ram)

Goby (ram)

Fig. 2. Food indices (I.A., %) for the main prey groups in relation to the size of Deltentosteus quadrimaculatus (ram) : a. pelagic copepods (e) and harpacticoid copepods (©); b. amphipods; c. polychaetes; d. mysids; e. cumaceans; f. decapods. I.A.) predominate; the latter group is quantitatively less important but is nevertheless favoured as seen by th'e high frequency percentage of up to 68.6% (Fig. 3a and b) ; (3) when over 30 mm, the gobies feed on benthic macrofauna exclusively (Fig. 2b to f), particularly on amphipods (34% ~ I.A. ~ 59%) ; the part played by harpacticoid copepods becoming insignificant to non-existent (Fig. 3a). When the total length of the goby surpasses 20 mm, the weight of the amphipods is higher than that of all other preys (Fig. 4). b.

CHANGES

IN FOOD

COMPOSITION

IN RELATION

TO DEPTH

There is a change in the composition of the food consumed by fish of the same size class (20 to 25 mm) caught at different depths, particu-

366

L. V I L L I E R S %

%

_~Polagic coO~pod$

v/o

lb

2'o

I*

4'o

5+

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6~

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4'o

~

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%

Ooby (mini

%

'

i

%

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CUMACIEANS

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DICAPODS

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,~

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ib

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Fig. 3. Frequency (%, upwards) and weight (%, downwards) distributions of preys found in the stomachs of Deltentosteus quadrimaculatus of different length (turn).

larly for h a r p a c t i c o i d copepods and a m p h i p o d s , the two most imp o r t a n t categories of prey. T h e n u m b e r of harpacticoids in the stomachs drops from 76% at 5 m to 5 8 % at 20 m (Fig. 5a), the f r e q u e n c y of o c c u r r e n c e from 77% at 5 m to 5 2 % at 20 m d e p t h (Fig. 5b). O n the other h a n d , the f r e q u e n c y of a m p h i p o d s in the stomachs increases from 2 3 % at 3 m to 5 9 % at 20 m.

PREDATION

BY JUVENILE

367

GOBY

Melluscs Ostracods

~ic

cop~od~

Harpacticold copepods Cylwis larvae

Mysids Cumaceans i Amphipods

I Decapods I Fish lar,,~e IO

Fig. 4. Dry weights (rag) of different prey groups found in the stomachs of Deltentosteus quadrimaculatus of different length (mm).

C. S I Z E R E L A T I O N

BETWEEN

PREDATOR

AND PREY

A relationship between the size of the prey and that of the predator is evident for young gobies of 7 to 48 m m (Fig. 6), a well-known phenomenon for carnivores. The mean relative size of prey is about 5% for the smallest gobies and increases progressively with the size of the gobies, reaching 1S % for fish of 45 to 48 m m in length (Fig. 6). The range in prey length widens with the size of the goby (Fig. 6), demonstrating a less selective aspect of predation in the larger individuals. After log transformation a strong linear correlation appears between the size of the preys and that of the gobies (Fig. 6; y = 0.017xl.496; R = 0.996; P < 0.01).

368

L. V I L L I E R S moT

In

"--'"~ *-''

~

........

n

"-'-'-

Fig. 5. Frequency (%, left) and weight (%, right) distributions of preys found in the

stomachs of Ddtentosteus quadrimaculatusfrom hauls at different water depth (m).

Prey ( r a m )

prey

(%)

prod

..... 2 / / " 4"

-10 / C ~ . . . . . . -o-- . . . . . .

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-6

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o

,~,

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Fig. 6. Absolute length (mm, O) and length relative to predator length (%, ©) of preys found in the stomachs ofDdtentosteus quadrimaeulatusof different length (mm). Indicated are 95% confidence intervals of the mean lengths of the preys (vertical bars) and numbers of preys counted in each size class of the gobies.

PREDATION

BY J U V E N I L E

369

GOBY

d. R E L A T I O N B E T W E E N T H E M E A N W E I G H T OF S T O M A C H C O N T E N T S A N D T H E S I Z E A N D W E I G H T OF D E L T E N T O S T E U S QUADRIMACULATUS The mean weight of the stomach contents, empty stomachs included, has been calculated in relation to the weight of the gobies. After log transformation, a linear type of regression is deduced (Fig. 7a; y = 1.27 10-2x0.747; R-----0.99). The same holds for the relation between weight of the stomach contents and length of the gobies (Fig. 7b;y = 1.41 10 -5 xZ-766; R = 0.99).

0.7.~

0.?~

0.50 *

0.50 -

0.25 -

0.25

0

i

0

,b

2'0

30

40

-

0

5~mmSO

46o

Fig. 7. Relations between m e a n weight of stomach contents, empty stomachs included, (rag), and size (ram, left) and weight (mg, right) of Deltentosteus quadri-

maculatus. IV. DISCUSSION

AND CONCLUSIONS

With their high densities Gobiidae probably constitute important links in the food chains of littoral areas. Many studies on this theme indicate the existence of a large variety of feeding types among the gobies (St-IORYIGIN, 1939; BOGACHVK, 1959; ABEL, 1962). Three main types are apparent: carnivores, omnivores and herbivores (GIBSON, 1969; WHEELER, 1969), the carnivores predominating (GIBSON, 1969; HESTHAGEN, 1971; MCGRATH, 1974; BODIOU & VILLIERS, 1979; BERG, 1979). The juveniles of Deltentosteus quadrimaculatus belong to this last group. The small predators lie in wait for their prey and feed mainly on benthic organisms which they swallow alive according the observations of PORUMB (1961). The principal characteristics of the diet are evident from the first stages onwards. The changes in predation with age can be circumscribed clearly. The part played by the diverse elements in the diet of

370

L. VILLIERS

the juveniles is due to complex interactions between the nutritional potentialities of the environment and the behaviour of the predator by which the food composition evolves throughout growth. The postlarvae eat zooplankton, almost exclusively small crustaceans, and they may be said to belong to the predatory type described by BOOACHVK(1959) for Pomatoschistus microps. The juveniles are zoobenthos eaters. They pass through two stages concerning the size of the prey consumed; being at first meiobenthos eaters, they become progressively macrobenthophagous. This development, already suspected by LEBOUR (1920) and SuYEmRO (1942) appears to be a common phenomenon. As the fish grows, the number of prey species increases. When the young fish turn from predominantly pelagic food to benthos, at a length of 20 mm, their behaviour changes. At lengths less than 15 mm they are not completely dependent on the sea bottom; in fact, they remain several centimetres above it. The bottom is gradually more often occupied as during growth the juveniles switch from planktonic to benthic preys; finally, the gobies behave by lying in wait on the bottom for their prey. These observations corroborate those made on the nutritional behaviour of the larval stages of several Pleuronectidae (PETERSEN,1893 ; LEBOUR, 1918; SHELBOURNE, 1953, 1962; LAST, 1978) and Gobiidae (LEBOUR, 1918, 1919, 1920). Food composition appears to depend on water depth. For young gobies between 20 and 25 ram, the frequency ofharpacticoid copepods in the stomach contents is seen to diminish with depth, whereas that of amphipods increases. This corresponds to the nutritional potentialities of the sublittoral sands between the isobaths of 3 and 20 m. Whereas the density of the meiofauna, and particularly that of the harpacticoid copepods, seems fairly unaffected by depth (BODIOU, 1975), the macrofauna (amphipods) density increases with depth (GuILLE, 1970; AMOUROUX, 1974). Size relations between predator, especially benthic fish, and prey are often cited (PETERSEN,1893; LEBOUR, 1920; SUYEHIRO,1942 ; ABEL, 1962; GIBSON, 1968; YUROCHKO, 1976; LAST, 1978). We have shown earlier (BoDmu & VILLIERS, 1979) that the predation on certain meiobenthos species, especially harpacticoid copepods, by juvenile Deltentosteus quadrimaculatus, corresponds to size criteria which is confirmed by the present study. The increase in prey weight, as well as that in the stomach contents, progresses exponentially with growth. Although the absolute weight of the ingested preys increases with the size of the gobies, the relative weight of the preys and their numbers decrease. This study attempts to add to our understanding of the trophic relations in the benthic ecosystem. The essential position of young

P R E D A T I O N BY J U V E N I L E GOBY

371

Deltentosteus quadrimaculatus as an exclusive carnivore feeding on all groups present at the bottom, was demonstrated. Its marked preference for small crustaceans may be a "choice" but it must be noticed that amphipods are the most a b u n d a n t group found on the littoral sands of this area (GuILLE, 1970). It seems logical therefore to suppose that the Gobiidae show a selective diet based essentially on the species and size composition of the prey populations present. V. SUMMARY Juveniles of the goby Deltentosteus quadrimaculatus hunt at sight lying in wait for their prey. They feed mainly on benthic organisms which are swallowed alive. The stomachs were analysed. The preys counted belong to 11 zoological groups of which seven are crustacean orders. The crustaceans comprise on average 92% of the total number of preys or 85% of the weight of preys. The species composition of the food changes during early growth, The postlarvae feed on zooplankton. Once the gobies reach 15 m m total length, the contribution of zoobenthos to their diet increases, to become the almost exclusive food source above 20 m m length. They then pass through two stages according to the size of their prey, feeding firstly on meiobenthos and passing over progressively on macrobenthos. This development in the choice of food is related to the goby's behaviour. Food composition also appeared to depend on water depth. For youngs the frequency ofharpacticoid copepods in the stomach contents decreased with depth whereas the occurrence of amphipods increased. The selective character of predation was also evident from the fact that the mean size of preys increased regularly with that of the gobies. This increase, even as that of the total weight of the stomach contents, followed exponential trends. VI. R E F E R E N C E S ABEL, E. F., 1962. Freiwasserbeobachtungen an Fischen in Golf von Neapel als

Beitrag zur Kenntnis ihrer Okologie und ihres Verhaltens.--Int. Revue ges. Hydrobiol. Hydrogr. 47: 219-290. AMOUROUX,J.-M., 1974. l~tude des peuplements infralittoraux de la c6te du Roussillon.--Vie Milieu 24 (2b) : 321-354. BExo, J., 1979. Discussion of methods of investigating the food of fishes, with reference to a preliminary study of the prey of Gobiosculusflavescens (Gobiidae).-Mar. Biol. 50: 263-273. BLEGVAD,H., 1917. On the food of fishes in the Danish waters within the Skaw.-Rep. Dan. biol. Stn 24-" 17-22.

372

L. V I L L I E R S

Bonxou, J.-Y., 1975. Cop~podes Harpacticoides des sables fins infralittoraux de Banyuls-sur-Mer.--Vie Milieu 25 (2b) : 313-330. Bomou, J.-Y. & L. VmLmRS, 1978-79, La pr6dation de ta m~iofaune par les formes juv6niles de Deltentosteus quadrimaculatus (Teleostei, Gobiidae).--Vie Milieu 28.-29 (1): 143-156. BOGACHYK, T. A., 1959. Formative effect of various diet on the mandibulary and pharyngeal apparatus of Gobiidae.--Dopov. Akad. Nauk. ukr. RSR 1959 (5) : 546-549. CASABXANCA,M. L. DE & A. KroNER, 1969. G o b i i d ~ des fitangs corses, systdmatique, ~cologie, rfigime alimentaire et position dans les cha/nes trophiques.---Vie Milieu 20 (3a): 611-633. FONDS, M., 1973. Sand gobies in the Dutch Wadden Sea (Pomatoschistus, Gobiidae, Pisces).--Neth. J. Sea Res. 6 (4): 417-478. GmsoN, R. N., 1968. The food and feeding relationships of littoral fish in the Banyuls region.--Vie Milieu 19 (2a): 447-455. , 1969. The biology and behaviour of littoral fish.--Oceanogr, mar. Biol. Ann. Rev. 7: 367-410. GmsoN, R. N. & I. A. EzzI, 1978. The biology of a Scottish population of Fries' goby, Lesueurigobiusfriesii.--J. Fish. Biol. 12 (4): 371-389. GmLL~., A., 1970. Bionomie benthique du plateau continental de la cSte catalane.-Vie Milieu 21 (Ib) : 149-280. H~ALEY, M. C., 1971. The distribution and abundance of sand gobies, Gobius minutus in the Ythan estuary.--Jnl Zool. 163 (2): 177-229. - - - - , 1972. On the population ecology of the common goby in the Ythan estuary.-J. nat. Hist. 6: 133-145. HESTHAOEN, I. H., 1971. The winter food of the gobies from one of the deeper channels of the Belt Sea, with particular reference to the sand goby, Pomatoschistus minutus (Pallas).--Kieler Meeresforsch. 27: 28-35. , 1975. Seasonal occurrence and length variation in the sand goby, Pomatoschistus minutus (Pallas) in the shore zone of the inner Oslofjord.--Norw. J. Zool. 23: 242. , 1977. Migrations, breeding, and growth in Pomatosehistus minutus (Pallas) (Pisces, Gobiidae) in Oslo0orden, Norway.--Sarsia 63 (1): 17-26. L~mAT, J.-P., 1976. ]~cologie de Crangon erangon d a m le complexe lagunaire de Bages-Sigean. Univ. Paris V I : 1-105 (thesis). LAST, J. M., 1978. The food of four species of pleuroneetiform larvae in the eastern English Channel and southern North Sea.--Mar. Biol. 45: 359-368. LAUZANNE, L., 1975. R~gimes alimentaires d'Hydrocyonforskalii (Pisces, Characidae) dans le lae Tehad et ses tributaires.--Cah. O.R,S.T.O.M. (Hydrobiol.) 9 (2): 105-121. - - - - , 1976. Rdgimes alimentaires et relations trophiques des poissons du lac Tchad. - - C a h . O.R.S.T.O.M. (Hydrobiol.) 10 (4) : 267-310. LEBOUR, M. V., 1918. The food of post-larval fish.--J, mar. biol. Ass. U.K. 11 (4): 433-469. , 1919. The young of the Gobiidae from the neighbourhood of Plymouth.-J. mar. biol. Ass. U.K. 12: 48-80. , 1920. The eggs of Gobius minutus, pictus and microps.--J, mar. biol. Ass. U.K. 12: 253-260. McGRATH, D., 1974. Preliminary studies on the feeding of Gobius niger (L.) and Gobiusflavescens (Fabricius) (Pisces, Gobiidae) in the northern Baltic p r o p e r . Contr. Ask6 Laboratory 4: 1-25.

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373

MILLER, P . J . , 1975. Predation of meiofauna by the goby (Pomatoschistusmicrops).-Bull. est. br. War. Sei. Ass 12: 1-10. Muus, B. J., 1967. The fauna of Danish estuaries and lagoons. Distribution and ecology of dominating species in the shallow reaches of the mesohaline zone.-Meddr Danm. Fisk.-og Havunders. 5 (1): 3-316. NEKRASOVA, M. Y. & I. F. KOVTUN, 1976. Annual fluctuations in the abundance of the round goby, Gobius melanostomus, in relation to natural variations in its food supply in the Azov sea.--J. Ichthyol. 16 (2): 331-336. PEpa~s,J. M. & J. PIeARD, 1964. Nouveau manuel de bionomie benthique de la Mer M6diterran6e.--Rec. Tray. Stn mar. Endoume 31 (47): 5-137. PETERSEN, C. G . J . , 1893. On the biology of our flat-fishes and the decrease of our flat-fish fisheries.--Rep. Dan. biol. Stn 4: 1-146. PORUME, I. I., 1961. Contributii la cunoasterea biologiei guvizilor (Gobius batrachocephalus, Gobius cephalargessi Gobius melanostomus) din dreptus litoralului rominesc al Marii Negre.--Hidrobiologia 3: 271-282. SHELBOORNE, J. E., 1953. The feeding habits of plaice post-larvae in the Southern Bight.--J. mar. biol. Ass. U.K. 32: 149-159. , 1962. A predator-prey relationship for plaice larvae feeding on Oikopleura.-J. mar. biol. Ass. U.K. 42: 243-252. SHORYIGXN,A. A., 1939. Food and food preference of some Gobiidae of the Caspian Sea.--Zool. Zh. 18 (1): 27-53. SOYER, J., 1970. Bionomie benthique du plateau continental de la c6te catalane franqaise. I I I . Les peuplements de Cop6podes Harpaeticoides (Crustacea).-Vie Milieu 21 (2b): 337-511. SUYEHIRO, Y., 1942. A study on the digestive system and feeding habits of fishes.-J a p . J. Zool. 10 (I): 1-303. VILLIEgS, L., 1979. Contribution/~ l'6tude de la nutrition et des aspects 6nerg6tiques chez des formes juv6niles de Deltentosteus quadrimaculatus (Valenciennes) (Pisces: Gobiidae). Univ. Paris V I : 1-175 (thesis). WHEELER, A., 1969. The fishes of the British Isles and North-West Europe. MacMillan, London: 1~13. YUROCHKO, S. Y., 1976. A quantitative evaluation of the comparative selection of food organisms by fish.--J. Ichthyol. 16 (5): 814--821.