II. Developmental and environmental interactions

ICES mar. Sei. Symp., 201: 21-34. 1995

Fish larvae, development, allometric growth, and the aquatic environment

J. W. M. Osse and J. G. M. van den Boogaart

Osse, J. W. M., and van den Boogaart, J. G. M. 1995. larvae, development, allometric growth, and the aquatic environment. - ICES mar. Sei. Symp., 201: 21-34.

During , fish larvae undergo rapid changes in external appearance and dimensions of body parts. The juveniles closely resemble the adult form. The focus of the present paper is the comparison of stages of development of belonging within different taxa in a search for general patterns. The hypothesis that these patterns reflect the priorities of vital functions, e.g., feeding, locomotion, and respiration, is tested taking into account the size-dependent influences of the aquatic environment on the larvae. A review of some literature on ailometries of fish larvae is given and related to the rapidly changing balance between inertial and viscous forces in relation to body length and swimming velocity. New data on the swimming of larval and juvenile are presented. It is concluded that the patterns of development and growth shows in many cases a close parallel with the successive functional requirements.

J. W. M. Osse and J. G. M. van den Boogaart: Wageningen Agricultural University, Department of Experimental Animal Morphology and Cell Biology, Marijkeweg 40, 6709 PG Wageningen, The Netherlands [tel: (+31) (0)317 483509, fax: (+31) (0)317 483962],

Introduction Fish larvae, being so small, must have problems using their limited resources for maintenance, activity, obtain­ Fish larvae are the smallest free-living vertebrates. In ing energy from external sources, and growth. There will some species under favourable conditions hatch be some common features over the wide variety of 30 within 24 h of fertilization and a tiny animal of a few orders and 424 families of living (Nelson, 1976). millimetres in length is exposed to the hazards of free A search for generalities in the pattern of development life; viz., to eat or be eaten. With the exception of a few and growth is by no means easy in view of the consider­ families of livebearers (e.g., Embiotocidae, Poecilidae), able variety in abiotic and biotic factors in the environ­ teleosts are oviparous and generally produce numerous ment. In the present paper, we have therefore chosen to rather small eggs. Marine fishes, often with small pelagic concentrate on the feature common to nearly all fish eggs, may produce more than a million eggs during larvae, viz., living in water. Water, although varying in spawning, while freshwater fishes mostly have fewer, temperature, salinity, pH-value, and concentrations of but larger, eggs. In general, fecundity is inversely other ions, is, with its slightly varying density and larger related to size and increases linearly with body size. temperature-dependent variation in viscosity, common A carp (Cyprinus carpio) of 4.9 kg produced nearly to all larvae and constant throughout ontogenetic and 765000 eggs (Hoda and Tsukahara, 1971). Mortality evolutionary time. The reproductive strategy of most often reaches 99% or more and there is little doubt that teleosts, which is supposedly the result of strong selec­ the high fecundity and the resulting small eggs have tive forces, has led to mechanisms for synchronization of considerable morphological, physiological, ecological, the arrival of parents at the spawning grounds by school­ and behavioural consequences for at least the embryonic ing (e.g., ), and to timing of the reproductive and larval stage. The abundant and rapidly increasing cycle within the most productive annual periods. literature on fish larvae, mainly due to the exhaustive Its most distinctive characteristic, the numerous practices of and the growing need for fish cul­ mostly small eggs, results in problems common to nearly ture, reveals a variety of terminology on the early devel­ all fish larvae. How are the restricted resources to be opment of fish (e.g., Balon, 1985) and therefore we divided between growth, maintenance, and activity to devote a short paragaph to these questions. survive the present and to reach the next stage of devel­ 22 J. W. M. Osse and J. G. M. van den Boogaart ICES mar. Sei. Symp., 201 (1995)

Table 1. Relations between egg diameter and (total) length of larvae at hatching, first branchial ventilation, first-feeding and reaching the juvenile stage arranged according to increasing egg diameter. From: de Sylva, 1984; Fukuhara, 1985; Antalfi and Tölg, 1971;Penaz, 1980; Penaz, 1978;Osse, 1989 and Penaz, 1983 (salmonoids). Length at becoming juvenile is our interpretation of the data of Fukuhara.

Total length (mm) of at:

Egg diameter Branchial Reaching the (mm) Hatching ventilation First-feeding juvenile stage

Mugil curema 0.6-1.3 1.7 3.7 5.3 Pagrus major 0.9 2.1 3.5 8 Ctenopharyngodon idella 1.2 4.1 7.5 8.0 11 Tinea tinea 1.2 4.8 5.6 7.2 16 Gobio gobio 1.3 4.1 7.3 21 Cyprinus carpio 1.9 4.5 5.5 5.8 21 Stenodus leucichthys 3.1 11.1 11.6 14.0 35 Thymallus thymallus 3.1 12.2 16.6 18 30 Hucho hucho 4.5 13.7 15.6 25 39 Salvelinus fontinalis 4.6 16.0 25.5 30 45 Braehymystax lenok 4.9 11.3 17.4 21 Salvelinus alpinus 5.2 15 23.5 25 45 Salvelinus namayeush 5.4 13 25.5 28 55 Salmo mykiss 5.9 10.4 29 26 30 Oneorhynehus keta 7.0-7.3 20 19.5 40 40

opment? Our general hypothesis is that the pattern of of patterns of development found therein. Balon’s development and allometric growth of structures and (1984, 1985) choice for the term embryo to indicate the organs in larvae closely reflects their priorities of feed­ stage from fertilization to first feeding, thereby neglect­ ing, locomotion, and respiration in view of their size and ing the time of hatching, seems biologically sound, since environmental circumstances. In the following, we com­ it indicates the whole period of early cleavage, determi­ pare the sequence of main events in the development of nation, differentiation, and growth until a stage is eggs and larvae in order to detect similarities. There­ reached suited to extract energy and building materials after, we retrace features of allometric growth and the from the outside world. It has two important drawbacks, dynamics of morphological development and try to however. The first is that it suggests there is a definite establish its relationship with the aquatic environment. point in time at which endogenous food is replaced by exogenous sources, which does not apply. Many species, e.g., carp (Penaz et al., 1983), gradually change from the Material and methods first to the second source, and remains of the yolk sac are Most data were collected from the literature, others at present together with food organisms in the gut. Also, our laboratory. Size, dimensions, and wet weight of carp hatching is biologically important, not just because the larvae were determined from laboratory cultures kept at animal suddenly becomes exposed, for example to abra­ 24°C and fed with living Artemia nauplii. At a total sion forces of waves and flowing water, but also because length of 10 mm, Artemia was gradually substituted by it can now actively avoid predators. So, in our opinion, small Trouvit pellets (Trouw and Co., Putten, The Neth­ there are firm biological arguments for distinguishing erlands). From hatching, larval samples were fixed in the stages of egg, larva, and juvenile. These terms have neutral formalin, cleared, and differently stained with morphological as well as functional significance. Until Alcian blue and Alizarine red (Moser et al., 1984). hatching, we speak of eggs containing the developing Swimming motion was studied from individual frames of embryo. The term larva is used for the whole period 200 frs-1 16 mm cine film taken with a shadowgraphic after hatching and the term juvenile is set apart for the technique (Drost and van den Boogaart, 1986a). subsequent stage showing completion of the fin rays, the completion (or nearly so) of ossification and the start of scale formation concomitant with the loss of the typical Terminology larval patterns of pigmentation and the primordial fin- As pointed out by Blaxter (1986,1988), terminology for fold. The subdivisions yolk-sac larva, preflexion, flexion early stages in the life history of fishes should be appli­ (of the caudal end of the ) and postflexion cable to all taxonomic groups and the enormous variety larva have the advantage that they refer to the acqui- ICES mar. Sei. Symp.. 201 (1995) Fish larvae, development, allometric growth, and the aquatic environment 23

7 -8 h .

dorsal view

0 (LuJZnZZL

Figure 1. The embryonic development of Barbus conchonius (Cyprinidae) during the first day at 25°C. Hatching occurs between 27 and 30h after fertilization, an = anus; b = blastoderm; e = eye; h = head; o = otic vesicle; s = somite; t = tail; y = yolk. Egg diameter is 1 mm (from Timmermans and Taverne, 1989)

sition of an ancient character that all teleosts have in­ externally discernible morphological characters. Never­ herited from the palaeoniscoid ancestors. Besides, there theless, every stage must perform at least two tasks: is the big practical advantage that this terminology from survival and change into the next. As form-function Kendall et al. (1984) closely reflects external characters relations sometimes change abruptly, developmental and is relatively easy to use even for newcomers in the constraints and periods of greater vulnerability to field. changes in environmental parameters can be expected. Between the larval and juvenile stages there are tran­ The presence of critical periods (Hjort, 1914) is most sitional stages, abrupt or prolonged, and in many cases likely a reflection of such constraints. accompanied by a change from planktonic habits to demersal or schooling pelagic habits. The transform­ Development ation from larvae into juveniles, the former rather gen­ eralized but mostly with at least distinct larval pigmen­ Eggs and embryology tation, the latter typical for the species, will be called Relations between egg size, size of hatching, start of metamorphosis because the loss of larval characters and branchial ventilation, first-feeding, and final transform­ the appearance of the juvenile form involve important ation to the juvenile stage have been demonstrated in changes in size, shape, respiration, locomotion, ecol­ the literature for many species (Table 1). Size at hatch­ ogy, and behaviour. In , Thorisson (1994) proposes a ing and the timing of the above features all increase with metamorphosing interval between 10 and about 12 mm egg size. Such trends are not always clear; compare, for length, but we do not have solid arguments for restrict­ example, the start of branchial ventilation in Salvelinus ing metamorphosis to changes occurring in that length and Brachymystax. Environmental conditions are im­ range. In other cases of metamorphosis, e.g., amphi­ portant, but are often not known in enough detail to bians, considerable time may elapse between stages. We explain such deviations from a main trend. The overall do not, however, consider an almost complete cessation relation between available resources in the egg and of development as an essential criterion for the use of the development of the above functions confirms the im­ term metamorphosis. In fishes, gradual metamorphosis portance of the amount of yolk. It shows that in eggs that as well as rather abrupt changes (leptocephalus larvae) are rich in yolk the moment of hatching is progressively are observed, so the time course of development delayed and the hatching larvae have attained greater provides only arbitrary arguments for avoiding the term body lengths. Consequently, performing the above metamorphosis. Stages are arbitrarily chosen moments functions is also delayed. Predation pressure on fish is in an essentially continuous process of development, probably strongest in early developmental stages, like distinguished by the appearance or disappearance of eggs and small larvae (Bailey and Houde, 1989). For 24 J. W. M. Osse and J. G. M. van den Boogaart ICES mar. Sei. Symp.. 201 (1995)

Hatching Hatching

1 mm Ventilation

Feeding Feeding

Juvenile Juvenile

Pagrus major Cyprinus carpio Fukuhara (1985) Penaz et al (1983) Figure 2. (A) Stages in the development of red sea bream (Pagrus major), redrawn from Fukuhara (1985). The first two stages are from Flussain etal. (1981). (B) Stages in the development of the common carp (Cyprinus carpio) (Penaz et al., 1983).

relations between life history strategies and the degree Larvae of for eggs and larvae, the reader is The course of development after hatching of the red sea referred to Balon (1985). bream (Pagrus major) shows the considerable change in Only minor differences are observed in the appear­ proportions of the body occurring during further devel­ ance and sequence of early stages of development of opment (Fig. 2A). The finfold has disappeared com­ fishes until hatching. Only the time involved in pletely at around 8 mm TL (total length). Similar processes like gastrulation and neurulation differ signifi­ pictures from the developing carp (Cyprinus carpio) cantly between species and taxa, resulting in incubation (Fig. 2B), where the finfold disappears around 10mm periods ranging from one day to several weeks, or even TL, also show that in the juvenile there is a gradual months, until hatching. Temperature is an important transition from a typical early larval form towards the variable parameter. Figure 1 shows the development miniature adult. If we compare the sequences of events until hatching of a cyprinid (Barbus conchonius) at 25°C, with respect to body length in both species (Fig. 3), an according to Timmermans and Taverne (1989). The overall similarity in the appearance of these morphologi­ embryonic axis arises at 9h, followed immediately by cal characters becomes evident between a representa­ the formation of somites. The tail separates from the tive of a rather primitive group, the Ostariophysi and yolk at 18 h. The heart starts to beat at 20 h and hatching one of the Sparidae, a family of the , the occurs between 27 and 30 h after fertilization. At 48 h the most advanced group of the teleosts. The main differ­ head is fully detached from the yolk and the eyes are ence is that in red sea bream the transformation to the pigmented. The yolk is gradually absorbed in the follow­ juvenile stage occurs at about 8 mm SL, whereas in carp ing two days, while the larva starts to feed. Development it is delayed to 15 mm SL. in other cyprinids, such as carp and zebrafish, is similar Larval length of red sea bream at hatching is 2.1 mm although at a slower rate, e.g., carp larve hatch 48 h after TL and in carp 4.5 mm TL. This difference is attribu­ fertilization at 23°C. table to the considerable difference in egg diameter, Detailed information on early embryology of some which in red sea bream is on average 0.92 mm (Fuku­ other species (Catastomus commersoni, Labeotropheus hara, 1985) and 1.86 mm in carp (Kamler, 1992). First- sp., Stizostedion vitreum) is given in Balon (1985), sug­ feeding occurs one day after yolk absorption in red sea gesting that the main course of development is similar in bream (Fukuhara, 1985), i.e., at a length of about most teleosts. 3.5 mm, while in carp this occurs at about 5.8 mm. Active swimming movements precede feeding. At ICES mar. Sei. Symp.. 201 (1995) Fish larvae, development, allometric growth, and the aquatic environment 25

Transformation A Standard length in mm 10 15 20 25 30 35 — I— __ I_ —I— ___ L_ ___I Developmental stage Larvae Juveniles

f dorsal / anal Segmentation J caudal of soft ray j pectoral ------► \ ventral ------► j dorsal Branching of I anal soft ray caudal pectoral y ventral

/ rounded — Hind margin of J truncated the caudal fin j emarginated \ furcated

Scale formation

Band formation

Pyloric caeca development

Redrawn from Fukuhara (1985) Pagrus major

T ransformation A Standard length in mm 10 : 15:- 20 25 30 35 __ L_ —I— __I_ __L Developmental stage Larvae Juveniles

f dorsal I anal Segmentation ^ caudal of soft ray I pectoral y ventral I dorsal I anal Branching of < caudal soft ray I pectoral y ventral

/ rounded Hind margin of J truncated the caudal fin ( emarginated \ furcated

Scale formation

Original data from Hoda & Tsukahara (1971) CypritlUS Carpio Figure 3. A comparison of developmental events at (standard) body lengths in the red sea bream (Pagrus major), and the common carp (Cyprinus carpio). Data from Fukuhara (1985) and Hoda and Tsukuhara ( 1971 ). Note the overall similarity in the sequence of events. See text for further explanation. 26 J. W. M. Osse and J. G. M. van den Boogaart ICES mar. Sei. Symp.. 201 (1995)

A B

Hatching Hatching Hatching

2 mm 2 mm 2 mm

Ventilation

Feeding Feeding Ventilation

Juvenile Juvenile Juvenile

Hucho hucho Salvelinus namayeush Thymallus thymallus Penaz (1981) Balon (1980) Penaz(1975) Figure 4. (A-C) Stages in the development of three species of Salmonidae with lengths at hatching and at the starts of ventilation and feeding. Redrawn from Penaz (1975, 1981) and Balon (1985).

Hatching Hatching Hatching

1 m m 1 m m Ventilation 1 mm Ventilation

Ventilation Feeding Feeding

Feeding

Juvenile Juvenile Juvenile

Ctenopharyngodon idella Gobio gobio Tinea tinea Penaz(1982) Antalti & Tolg (1971 ) Penaz (1978), Prokes and. Penäz (1979) Figure 5. (A-C) Stages in the development of three species of Cyprinidae with length at hatching and at the starts of ventilation and feeding. Redrawn from Antalfi and Tölg (1971), Prokes and Penaz (1979) and Penaz (1978, 1982). CSmr Si yp,21 (1995) 201 Symp., Sei. mar. ICES Catostomus commersoni Couesius plumbeus Osmerus mordax Percina caprodes Fish larvae, development, allometric growth, and the aquatic environment aquatic the and growth, allometric development, larvae, Fish lueioiyøoo lueioiyøoo mjmojø jueioiyeoo tftMOJø jueioiyeoo

27 28 J. W. M. Osse and J. G. M. van den Boogaart ICES mar. Sei. Symp., 201 (1995)

Relative volume during growth there sequential patterns of development and do they show certain general trends in the development of ■ = brain □ = muscle teleosts? Fuiman (1983) determined the growth coef­ B = skeleton ficients (in fact the exponent k of a simple power func­ tion: y = bxk) in a catostomid, a cyprinid, a salmonoid, 6 0- and a percid (Fig. 6). He found that the anterior and 4 0- posterior parts of the body in all these fishes grew faster than the middle section, although at a somewhat greater 20 - length range in Osmerus mordax. Percina caprodes showed the phenomenon only weakly in the head but weight (mg) 100 1000 10,000 clearly in the tail region. The U-shaped growth profile in Cyprinus carpio early larvae is also recognizable in harengus, Sardinops ocellata, Sprattus sprattus, and Esox lucius (Fuiman, 1983). The completion of the head for feeding and respiratory functions, and the tail for cruising and escape reactions prior to full development of the intes­ tine, appears to be given priority. This is probably not I \ surprising in view of the easily digested planktonic food, 100 1000 io,ooo“^ weight(mg) sometimes with powerful digestive enzymes (e.g., in Cichlasoma octofasciatum herring, Pedersen, 1987). In early life many fish appear redrawn from Yapo (1990) to rely on zooplanktonic prey as an exogenous source of Figure 7. Change of relative volume of brain, muscle, and digestive enzymes (Wieser, 1991). skeleton during growth in weight classes of 0-10, 10-100 mg, etc., in Cyprinus carpio and Cichlasoma octofasciatum (re­ Is this positive allometry of head and tail, with its drawn from Yapo, 1990). concomitant increase in body length, related to the fact that the cost of transport is up to five times higher in fish larvae than in adult fish (Beamish, 1978)? Such broad lengths of 3.5 mm, carp larvae are still inside the egg; so comparative studies of allometry in fish larvae are not red sea bream completes its metamorphosis at a con­ very numerous. Yapo (1990) measured the relative siderably smaller size. Is this relation between egg size volumes of the brain, muscles, and skeleton of Cyprinus and the completion of metamorphosis exceptional or are carpio and Cichlasoma octofasciatum from serial there similar cases? Within the Salmonidae, Hucho sections (Fig. 7). Also here a similarity is observed hucho (Penaz, 1981a, b), Salvelinus namaycush (Balon, between the groups, early priority of growth of the brain 1980), and Thymallus thymallus (Penaz, 1975), yolk-sac is followed by the skeleton (cartilage and bone) and larvae of 12-15 mm (Fig. 4) are found and the primor­ muscle tissue. Oikawa and Itazawa (1985) attribute the dial finfold is apparent even later. First-feeding occurs at decrease of the weight exponent in the formula of the lengths of about 18 mm, 28 mm, and 19 mm, respect­ metabolic rate of carp during development to the posi­ ively. Within the Cyprinidae, body length (Fig. 5) at tive allometric growth of the low metabolic activity first-feeding is at about 7 mm in Ctenopharyngodon white muscle after the juvenile stage. The weight-length idella (Antalfi and Tölg, 1971), Gobio gobio (Penaz, graph of the carp (Osse, 1990) (Fig. 8) shows a weight 1981), and Tinea tinea (Penaz, 1982). In Mugil curema increase with length prior to the juvenile stage with a (de Sylva, 1984), as in red sea bream, first-feeding occurs growth coefficient of 4.48; thereafter it is reduced to at less than 4 mm (Table 1). Although the survey is very 3.12, i.e. close to isometry. Other allometries of length limited, we always see a similar sequence of events of intestine, body depth, and pectoral fin length with occurring at different body lengths. The finfold seems to body length are shown in Fig. 9 (Hoda and Tsukahara, be present in all fish larvae (Moser, 1984; Moser et al., 1971). Note that the change of growth coefficient is 1984), its function is unknown. Some possibilities are found at about the same body length, except in the case mentioned in the discussion. of gut length. A striking case of sequential growth is seen in the number of primordial germ cells in Barbus con- chonius (Timmermans and Taverne, 1989). Their A llom etry number is constant from about 15 h after fertilization to Allometry is a common feature during development. an age of 21 days. At that time they rapidly increase in Since evolution ensures the initial investment of enough number, together with the growth of gonadal primordia, effort in developing the most essential organs for pri­ while the animal as a whole grows from 4 to 10 mm TL mary functions, to be followed at a later stage by devel­ and from about 2 to 20 mg in wet weight. Another clear opment of organs with lower priority for survival, are allometry in the carp is found in the growth of the gill ICES mar. Sei. Symp.. 201 (1995) Fish larvae, development, allometric growth, and the aquatic environment 29

10000- o> E

f 1000- §

100-

1 0 -

6 8 10 12 14 16 18 20 30 40 60 Standard length (mm) Figure 8. Length-weight graph of Cyprinus carpio. Note change of growth coefficient from initially 4.48 to 3.12 at a length of about 20mm (from Osse, 1990).

area with body mass (Fig. 10) (Oikawa and Itazawa, hydrodynamic regime. The Re (Reynolds) number can 1985). Until about 7 mm TL the surface area of the gills be considered to be the quotient of the inertial and grows with body mass to the power 7.066(1), then viscous forces (Re = u*l/v), where u and 1 are velocity reduces to a power function with an exponent 1.222 and and length respectively and v is the kinematic viscosity of to 0.794 at a body weight of less than 1 g net weight. Such the water. Viscous forces in the flow around a moving allometries are not restricted to carp. The Pacific mack­ object, e.g., a fish or fish larva, are all important when erel (Scomber japonicus (Kramer, I960)) also shows Re is less than 1. Inertial forces dominate the flow when allometric growth (Fig. 11) with a sudden change in Re is greater than 200 (inertial regime). When Re is growth coefficient of body depth with body length occur­ between 1 and 30 the regime is still viscous, because ring at 8.5 mm SL. Our conclusion is not just that allo­ these forces dominate the flow. At 30 < Re <200 an metries are of general occurrence, but also that there is a intermediate zone is recognized, where the balance be­ similarity in particular allometries at an equal size range tween the two forces gradually shifts from a viscous to an of fish larvae in distantly related taxa. Two questions are inertial regime (Fuiman and Webb, 1988). raised. What causes these events and why do they hap­ pen at some specific moment during development from a functional point of view? How do they serve the animal Swimming of fish larvae in coping with the environment? We will discuss only the Fish larvae can perform two types of swimming, cruising second question. and burst swimming. Cruising or routine swimming is seen in most species between 3 and 7 mm total length (TL) with a varying velocity, but mostly between 1 and 3 The aquatic environment BL s“ 1 (BL = body length). Fuiman and Webb (1988) Two types of forces can be distinguished acting on mov­ found that larvae spend 98% of the time in the viscous ing objects in fluids: pressure forces and viscous forces. and intermediate hydrodynamic regimes, of which 23% Pressure forces act normally (perpendicular), viscous is in the viscous regime. Figure 12 shows that gliding is forces tangentially on a hypothetical element of fluid. very ineffective, the kinetic energy being rapidly lost to Viscous forces correspond with shear stresses. friction. Gliding distance is 10% of the total distance The forces acting on a moving fish differ with the covered in 55% of the time of the whole action. During 30 J. W. M. Osse and J. G. M. van den Boogaart ICES mar. Sei. Symp., 201 (1995)

S.L. 22.5 mm 100000 - S.L. ± 20 mm

5 10 20 50 100 200 400 0 . 1 -

£ 0.01 - 1 100- S.L. 22 mm 0.001 T3 0.001 0.01 0.1 1 10 100 1000 10000 JDO Wet body weight (g) _c° 10- Oikawa & Itazawa (1985) 0o. Figure 10. The relation between gill area and body weight in -o Cyprinus carpio (from Oikawa and Itazawa, 1985). Note that, initially, gill surface grows at the 7th power of body weight.

5 10 20 50 100 200 400

y=0.715X-0 305 O) S.L. 21 mm - 0 6 -

c 1 0 -

ye1.147X-0.713

S’ 0 2

20 S.L. = 8.5 mm Standard length (mm) -0 2 0 6 07 0.9 10 11 Redrawn from Hoda & Tsukahara (1971) Log standard length (mm) Figure 9. The relations between body length and length of Figure 11. Allometry in the Pacific (Scomber japoni- intestine, body depth, and pectoral fin length in Cyprinus car­ cus). Body depth is shown in relation to body length (drawn pio (redrawn from Hoda and Tsukahara, 1971) from data of Kramer, 1960).

escape responses (at burst speeds) Batty (1981) found in growing fish. So the hydrodynamic environment speeds of 20 BL s_l in plaice larvae of 7 mm. In these changes significantly during growth and the morphology latter cases they rapidly leave the intermediate regime to of fish larvae reflects the influence of the changing move into a regime with Re values above 200, but even balance of forces. then the first part of this burst swimming is in the viscous In previous work, Drost et al. (1988a, b) demon­ and later in the intermediate regime. Another effect of strated effects of the hydrodynamic regime on the feed­ being very small while swimming is a considerable yaw ing and swimming of carp larvae. With a quantitative of the head. These effects decrease with increasing fish hydrodynamic model of suction feeding they showed the size (Table 2). Here as well as in plaice larvae (Batty, importance of viscosity effects of the flow inside the 1981) maximal velocities exceed 30 BL s-1, velocities mouth of a 6 mm TL carp larva. The conclusion was that which are hardly ever achieved in adult fish. This is 60% of the energy spent in the expansion of the head another demonstration of the importance of scale effects during feeding (the suction feeding act was completed in ICES mar. Sei. Symp., 201 (1995) Fish larvae, development, allometric growth, and the aquatic environment 31

Cyprinus carpio larvae Average maximal angles between successive o- - 100 « body segments of 1/12th body length 5 0 1 E 10- -1 1 0 5 50 mm T.L. Œ> 6.60 mm T.L. E 2 0 - -120 i- 10.30 mm T.L. 40 - 20.30 mm T.L. 3 0 - -1 3 0

4 0 - - 140 CO 30 - D£ 5 0 - -1 5 0 O o 6 0 - -1 6 0 » 20 - ca) - 1/0 < 10 - 8 0 - -2 0 0

9 0 - -4 5 0

0 5 10 15 10 15 20 0 20 40 8060 100 Distance (mm) % of total body length Figure 12. Burst swimming of 5.45 mm TL carp larvae. Note that gliding is ineffective. From time point 170 msec a distance Cyprinus carpio, larva 5.5 mm T.L. of less than one-third of body length is covered in 280 ms (from body curvature in successive beats Osse and Drost, 1989).

8 ms) was lost to the effects of friction. With optimum sized prey the energy spent in a successful act of suction feeding was less than 1% of the energy contained in the food. Initially, capture efforts are only successful in 66% of cases. The main energy expenditure for feeding is spent in search swimming (Drost and van den Boogaart, 0 20 40 60 80 100 1986b). ► % of total body length We present here new data of burst swimming of carp Figure 13. (A) The maximal angles of body curvature, larvae and juveniles at four length classes (5.5, 6.6, measured over the body divided into 12 segments in larvae and 10.3, and 20.3 mm TL) filmed at 200 frs-1. The analysis juveniles of Cyprinus carpio during burst swimming. Note the revealed (Fig. 13) that the smallest larvae show about change from resistive swimming, with about equal angles of equal angles of curvature (anguilliform motion) over curvature over the whole body length in small larval, to reactive swimming, with increasing angles of curvature restricted to the the whole body during the acceleration phase. As soon tail in bigger larvae and juveniles. (B) Angles of body curvature as they have attained velocities of about 50m m s~\ during burst swimming in a 5.5 mm carp larva. The main curva­ body curvatures become more restricted to the pos­ ture rapidly becomes more restricted to the tail region. terior portion of their body (Fig. 13B). Characteristic Re values have then reached 250. Initially, resistive forces dominate, and then, with increasing speed, iner­ tial forces become more important. Webb and Weihs this model can be described as anguilliform. This is (1986) propose a resistive model describing the friction what we observe initially in Fig. 13A. These authors forces that counteract movements of the body of the also mention a reactive model describing the forces larvae. At low Re values, swimming movements fitting acting on the body due to the acceleration of water by body movements. This model is most appropriate at higher Re numbers and subcarangiform swimming Table 2. Burst swimming of larval and juvenile carp. Note movements fit most closely (Webb and Weihs, 1986). decrease of frequency of beating and maximal velocity with size This type of movement is seen in the last 40 ms of and increase in gliding distance. Figure 13B. So, in the case of Figure 13, a change from resistive to reactive swimming is seen during one swim­ Total body length ming bout as a subcarangiform swimming movement is (B/L) fish (mm) 5.5 10.4 23.6 gradually adopted. In larvae longer than 6.6mm, the Max. tail beat freq. (Hz) 50 20 20 initial acceleration is higher and body curvature is re­ Max. velocity (BL s_1) 33 33 11 stricted mainly to the tail (Fig. 13A). The morphologi­ Max. head yaw (%BL) 11 6 5 cal differentiation of the caudal fin (Fig. 14) closely Gliding length (BL) 0.7 1.4 3.4 parallels the change in the swimming mode. Ossifica- 32 J. W. M. Osse and J. G. M. van den Boogaart ICES mar. Sei. Symp., 201 (1995)

Cyprinus carpio

length (mm) 0.5 mm 6.44

7.65

8.96 9 13.46 1— > 20 Figure 14. Chondrification and ossification of the tail region of carp larvae. Total length and age in days at (23°C) are given to the left and right sides of the successive photographs. Until 8.7 mm TL tail structures only show blue colouration (Alcian blue) in the original colour photographs. The caudal fin rays are partly ossified at length of 9.75 mm. In a 13.46 mm larva the hypural plates and the vertebrae are also ossified. ICES mar. Sei. Symp., 201 (1995) Fish larvae, development, allometric growth, and the aquatic environment 33

tion of the caudal fin rays and the caudal part of the mann, 1990). The “preference” for positive allometry of notochord strengthens the construction to transfer the head and tail (also seen in the carp, Van Snik, pers. momentum of the moving water to the larva, thereby comm.) can thus be explained as an adaptation to reduce making it suitable for reactive swimming (Fig. 14). This the costs of transport. The intraspecific positive allome­ is observed at lengths between 7 and 10 mm. tries in carp larvae, e.g. of the pectoral fin, reflect the need to provide additional thrust and to reduce the angular recoil forces generated by the lateral move­ Discussion ments of the tail (Batty, 1981). This function of the pectoral fin appeared to be particularly important in Of the many factors influencing growth and develop­ small larvae during the approach of a food item, where ment of fish larvae, temperature is the most prominent, the pectorals assist in aiming by correcting the yaw of the as it not only exerts direct influence on the biological head. The increased growth of the intestine in 9.5 mm objects (Blaxter, 1992) but also the kinematic viscosity long carp larvae, causing the development of the intesti­ of water is reduced by nearly 50% between 0 and 20°C nal fold, occurs synchronously with the restriction of the (Daniel and Webb, 1987). Temperature influences body undulation of the body to the tail region, i.e. with the size, growth, differentiation of muscle and meristic sub-carangiform swimming mode. The increasing gut characters. In the present overview of development, length seems appropriate prior to the switch of the allometric growth, and the hydrodynamic environment, larvae from planktonic to more benthic feeding habits. such temperature effects are not considered in detail. Concomitantly, the ossification of the fin rays of the tail We concentrate on the dynamics of form-function re­ and the caudal segment of the skeleton of the body axis lationships in view of the tight energy budget of fish provides the animal with structures suitable for reactive, larvae (Wieser, 1991) and the changing influence of the carangiform swimming (cf. Fig. 14). environment. The primordial finfold is absent in red sea bream of Comparison of the sequences of events in smaller and 8 mm TL (unpaired fins instead), whereas it is still found larger eggs (primarily an increase in yolk, cf. Table 1) in carp larvae of about 10 mm TL. In the salmonids shows that the larvae from large eggs attain a bigger size shown, it is even found in 24 mm larvae of Salvelinus. prior to hatching, the development of branchial venti­ The function of the finfold in swimming, respiration, or lation and first-feeding. Increased size reduces the cost providing flow-free space for the developing unpaired of transport per unit weight and is also significant in fins has not been verified. One of the effects of its reducing predation (Bailey and Houde, 1989). The simi­ presence, the great surface of the larva, increases drag larity in the timing of appearance of larval characters in and thereby the cost of locomotion. It also reduces the Pagrus major and Cyprinus carpio, although occurring sinking speed of a larva. Jordan (1992), studying undula­ at different body lengths, shows that such sequences are tion of the chaetognath Sagitta elegans, found that in the widespread between distantly related groups of teleosts, first 80 ms of the motion inertial forces were unexpec­ strongly suggesting their functional importance but also tedly high. Is this an effect of its increased body depth reflecting the different egg size. One wonders whether due to its finfold and are similar effects present in fish length is the proper dimension for comparing stages? As larvae? The early loss of the finfold in the red sea bream explained below, length is important from the aspect of and its much longer persistence in salmonid larvae does hydrodynamics, but it is also a better measure of mor­ not suggest an important respiratory function. Wieser phological development than age. From studies of (1991), however, notes that the smallest cyprinid larvae muscle development (Akster, pers. comm.), it appears may consume as much as 80 mol 0 2g_1 h~’, one of the that body lengths at which developmental effects occur highest values ever recorded in fish. Is the extra surface remain constant despite changes in growth rate due to area of the finfold an adaptation to achieve this? food conditions or temperature (cf. Fuiman and Webb, Our starting hypothesis, that the patterns of develop­ 1988). It would be worthwhile extending the comparison ment and growth are reflections of successive functional between Ostariophysi and Percoidei to establish the priorities at different sizes, is confirmed in many cases, consistency of the difference in development between but not all. Explanations for such deviations may be these groups. found in the considerable differences in habitat of the The positive allometry of the anterior and posterior multitude of fish species. parts of the body (Fuiman, 1983) closely parallels the desirability to escape as soon as possible from the vis­ cous and intermediate regime of Re-numbers and so to reduce the drag forces on the body. Beamish (1978) References showed that the costs of transport are up to five times Antalfi, A., and Tölg, I. 1971. Graskarpfen - Pflanzenfres­ higher in larvae, decreasing rapidly with growth (Kauf­ sende Fische. Donau Verlag, Günzburg. 207 pp. 34 J. W. M. Osse and J. G. M. van den Boogaart ICES mar. Sei. Symp., 201 (1995)

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