fish larvae, development, allometric growth, and the

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. Fish larvae, development, allometric growth, and the aquatic environment. - ICES mar. Sei. Symp., 201: 21-34.

During metamorphosis, 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 fishes 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 carp 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 o f 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 are the smallest free-living vertebrates. In some species under favourable conditions eggs hatch within 24 h of fertilization and a tiny animal of a few millimetres in length is exposed to the hazards of free life; viz., to eat or be eaten. With the exception of a few families of livebearers (e.g., Embiotocidae, Poecilidae), teleosts are oviparous and generally produce numerous rather small eggs. Marine fishes, often with small pelagic eggs, may produce more than a million eggs during spawning, while freshwater fishes mostly have fewer, but larger, eggs. In general, fecundity is inversely related to egg size and increases linearly with body size. A carp (Cyprinus carpio) of 4.9 kg produced nearly 765000 eggs (Hoda and Tsukahara, 1971). Mortality often reaches 99% or more and there is little doubt that the high fecundity and the resulting small eggs have considerable morphological, physiological, ecological, and behavioural consequences for at least the embryonic and larval stage. The abundant and rapidly increasing literature on fish larvae, mainly due to the exhaustive practices of fisheries and the growing need for fish culture, reveals a variety of terminology on the early development of fish (e.g., Balon, 1985) and therefore we devote a short paragaph to these questions.

Fish larvae, being so small, must have problems using their limited resources for maintenance, activity, obtaining energy from external sources, and growth. There will be some common features over the wide variety of 30 orders and 424 families of living teleosts (Nelson, 1976). A search for generalities in the pattern of development and growth is by no means easy in view of the considerable variety in abiotic and biotic factors in the environment. In the present paper, we have therefore chosen to concentrate on the feature common to nearly all fish larvae, viz., living in water. Water, although varying in temperature, salinity, pH-value, and concentrations of other ions, is, with its slightly varying density and larger temperature-dependent variation in viscosity, common to all larvae and constant throughout ontogenetic and evolutionary time. The reproductive strategy of most teleosts, which is supposedly the result of strong selective forces, has led to mechanisms for synchronization of the arrival of parents at the spawning grounds by schooling (e.g., herring), and to timing of the reproductive cycle within the most productive annual periods.

Its most distinctive characteristic, the numerous mostly small eggs, results in problems common to nearly all fish larvae. How are the restricted resources to be divided between growth, maintenance, and activity to 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.

Egg diameter (mm)

Total length (mm) of larva at:

HatchingBranchial

ventilation First-feedingReaching the juvenile stage

Mugil curema 0.6-1.3 1.7 3.7 5.3Pagrus major 0.9 2.1 3.5 8

Ctenopharyngodon idella 1.2 4.1 7.5 8.0 11Tinea tinea 1.2 4.8 5.6 7.2 16Gobio gobio 1.3 4.1 7.3 21Cyprinus carpio 1.9 4.5 5.5 5.8 21

Stenodus leucichthys 3.1 11.1 11.6 14.0 35Thymallus thymallus 3.1 12.2 16.6 18 30Hucho hucho 4.5 13.7 15.6 25 39Salvelinus fontinalis 4.6 16.0 25.5 30 45Braehymystax lenok 4.9 11.3 17.4 21Salvelinus alpinus 5.2 15 23.5 25 45Salvelinus namayeush 5.4 13 25.5 28 55Salmo mykiss 5.9 10.4 29 26 30Oneorhynehus keta 7.0-7.3 20 19.5 40 40

opment? Our general hypothesis is that the pattern of development and allometric growth of structures and organs in larvae closely reflects their priorities of feeding, locomotion, and respiration in view of their size and environmental circumstances. In the following, we compare the sequence of main events in the development of eggs and larvae in order to detect similarities. Thereafter, we retrace features of allometric growth and the dynamics of morphological development and try to establish its relationship with the aquatic environment.

Material and methods

Most data were collected from the literature, others at our laboratory. Size, dimensions, and wet weight of carp larvae were determined from laboratory cultures kept at 24°C and fed with living Artemia nauplii. At a total length of 10 mm, Artemia was gradually substituted by small Trouvit pellets (Trouw and C o ., Putten, The Netherlands). From hatching, larval samples were fixed in neutral formalin, cleared, and differently stained with Alcian blue and Alizarine red (Moser et al., 1984). Swimming motion was studied from individual frames of 200 f r s -1 16 mm cine film taken with a shadowgraphic technique (Drost and van den Boogaart, 1986a).

T erm ino logy

As pointed out by Blaxter (1986,1988), terminology for early stages in the life history of fishes should be applicable to all taxonomic groups and the enormous variety

of patterns of development found therein. Balon’s (1984, 1985) choice for the term embryo to indicate the stage from fertilization to first feeding, thereby neglecting the time of hatching, seems biologically sound, since it indicates the whole period of early cleavage, determination, differentiation, and growth until a stage is reached suited to extract energy and building materials from the outside world. It has two important drawbacks, however. The first is that it suggests there is a definite 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 first to the second source, and remains of the yolk sac are present together with food organisms in the gut. Also, hatching is biologically important, not just because the animal suddenly becomes exposed, for example to abrasion forces of waves and flowing water, but also because it can now actively avoid predators. So, in our opinion, there are firm biological arguments for distinguishing the stages of egg, larva, and juvenile. These terms have morphological as well as functional significance. Until hatching, we speak of eggs containing the developing embryo. The term larva is used for the whole period after hatching and the term juvenile is set apart for the 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 larval patterns of pigmentation and the primordial finfold. The subdivisions yolk-sac larva, preflexion, flexion (of the caudal end of the notochord) and postflexion 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

0 (LuJZnZZL

dorsal view

7 -8 h .

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 inherited from the palaeoniscoid ancestors. Besides, there is the big practical advantage that this terminology from Kendall et al. (1984) closely reflects external characters and is relatively easy to use even for newcomers in the field.

Between the larval and juvenile stages there are transitional stages, abrupt or prolonged, and in many cases accompanied by a change from planktonic habits to demersal or schooling pelagic habits. The transformation from larvae into juveniles, the former rather generalized but mostly with at least distinct larval pigmentation, the latter typical for the species, will be called metamorphosis because the loss of larval characters and the appearance of the juvenile form involve important changes in size, shape, respiration, locomotion, ecology, and behaviour. In cod, Thorisson (1994) proposes a metamorphosing interval between 10 and about 12 mm length, but we do not have solid arguments for restricting metamorphosis to changes occurring in that length range. In other cases of metamorphosis, e.g., amphibians, considerable time may elapse between stages. We do not, however, consider an almost complete cessation of development as an essential criterion for the use of the term metamorphosis. In fishes, gradual metamorphosis as well as rather abrupt changes (leptocephalus larvae) are observed, so the time course of development provides only arbitrary arguments for avoiding the term metamorphosis. Stages are arbitrarily chosen moments in an essentially continuous process of development, distinguished by the appearance or disappearance of

externally discernible morphological characters. Nevertheless, every stage must perform at least two tasks: survival and change into the next. As form-function relations sometimes change abruptly, developmental constraints and periods of greater vulnerability to changes in environmental parameters can be expected. The presence of critical periods (Hjort, 1914) is most likely a reflection of such constraints.

D ev e lo p m en t

Eggs and embryology

Relations between egg size, size of hatching, start of branchial ventilation, first-feeding, and final transformation to the juvenile stage have been demonstrated in the literature for many species (Table 1). Size at hatching and the timing of the above features all increase with egg size. Such trends are not always clear; compare, for example, the start of branchial ventilation in Salvelinus and Brachymystax. Environmental conditions are important, but are often not known in enough detail to explain such deviations from a main trend. The overall relation between available resources in the egg and development of the above functions confirms the importance of the amount of yolk. It shows that in eggs that are rich in yolk the moment of hatching is progressively delayed and the hatching larvae have attained greater body lengths. Consequently, performing the above functions is also delayed. Predation pressure on fish is probably strongest in early developmental stages, like 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

Feeding

Juvenile

Pagrus majorFukuhara (1985)

Hatching

1 mmVentilation

Feeding

Juvenile

Cyprinus carpioPenaz 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 of parental care for eggs and larvae, the reader is referred to Balon (1985).

Only minor differences are observed in the appearance and sequence of early stages of development of teleost fishes until hatching. Only the time involved in processes like gastrulation and neurulation differ significantly between species and taxa, resulting in incubation periods ranging from one day to several weeks, or even months, until hatching. Temperature is an important variable parameter. Figure 1 shows the development until hatching of a cyprinid (Barbus conchonius) at 25°C, according to Timmermans and Taverne (1989). The embryonic axis arises at 9h , followed immediately by the formation of somites. The tail separates from the yolk at 18 h. The heart starts to beat at 20 h and hatching occurs between 27 and 30 h after fertilization. At 48 h the head is fully detached from the yolk and the eyes are pigmented. The yolk is gradually absorbed in the following two days, while the larva starts to feed. Development in other cyprinids, such as carp and zebrafish, is similar although at a slower rate, e .g ., carp larve hatch 48 h after fertilization at 23°C.

Detailed information on early embryology of some other species (Catastomus commersoni, Labeotropheus sp., Stizostedion vitreum) is given in Balon (1985), suggesting that the main course of development is similar in most teleosts.

Larvae

The course of development after hatching of the red sea bream (Pagrus major) shows the considerable change in proportions of the body occurring during further development (Fig. 2A). The finfold has disappeared completely at around 8 mm TL (total length). Similar pictures from the developing carp (Cyprinus carpio) (Fig. 2B), where the finfold disappears around 10mm TL, also show that in the juvenile there is a gradual transition from a typical early larval form towards the miniature adult. If we compare the sequences of events with respect to body length in both species (Fig. 3), an overall similarity in the appearance of these morphological characters becomes evident between a representative of a rather primitive group, the Ostariophysi and one of the Sparidae, a family of the Acanthopterygii, the most advanced group of the teleosts. The main difference is that in red sea bream the transformation to the juvenile stage occurs at about 8 mm SL, whereas in carp it is delayed to 15 mm SL.

Larval length of red sea bream at hatching is 2.1 mm TL and in carp 4.5 mm TL. This difference is attributable to the considerable difference in egg diameter, which in red sea bream is on average 0.92 mm (Fukuhara, 1985) and 1.86 mm in carp (Kamler, 1992). First- feeding occurs one day after yolk absorption in red sea bream (Fukuhara, 1985), i.e., at a length of about 3.5 mm, while in carp this occurs at about 5.8 mm. Active swimming movements precede feeding. At


Transformation

AStandard length in mm 10

— I—15 20

__ I_25

—I—30

___ L_35

___I

Developmental stage Larvae Juveniles

f dorsal/ anal

Segmentation J caudalof soft ray j pectoral --------- ------------------- ►

\ ventral ------►

Branching of soft ray

j dorsal I anal

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

AStandard length in mm 10 :

Developmental stage Larvae

15:- 20 __ L_

25 —I—

30 __I_

35 __L

Segmentation of soft ray

Branching of soft ray

f dorsal I anal

^ caudal I pectoral y ventral

I dorsal I anal

< caudal I pectoral y ventral

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

\ furcated

Juveniles

Scale formation

Original data from Hoda & Tsukahara (1971) CypritlUS CarpioFigure 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

B

Hatching

ICES mar. Sei. Symp.. 201 (1995)

A

Hatching

2 mm

Feeding

2 mm

Ventilation

Hatching

Ventilation

2 mm

Feeding

JuvenileJuvenileJuvenile

Hucho huchoPenaz (1981)

Salvelinus namayeushBalon (1980)

Thymallus thymallusP enaz(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

1 m m

Ventilation

Hatching

1 mmVentilation

Feeding

Feeding

Hatching

1 m m

Ventilation

Feeding

Juvenile JuvenileJuvenile

Ctenopharyngodon idellaAntalti & Tolg (1971 )

Gobio gobioPenaz (1978), Prokes and. Penäz (1979)

Tinea tineaP enaz(1982)

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).

Cat

ost

om

us

com

mer

son

i C

oues

ius

plum

beus

O

smer

us

mor

dax

Per

cina

ca

pro

des

ICES mar. Sei. Symp., 201 (1995) Fish larvae, development, allometric growth, and the aquatic environment 27

jueioiyeoo tftMOJølueioiyøoo mjmojø


Relative volume during growth

■ = brain □ = muscle B = skeleton

60-

40-

2 0 -

weight (mg)

Cyprinus carpio100 1000 10,000

I100

\1000 io,ooo“^ weight(mg)

Cichlasoma octofasciatumredrawn from Yapo (1990)

Figure 7. Change of relative volume of brain, muscle, and skeleton during growth in weight classes of 0-10, 10-100 mg, etc., in Cyprinus carpio and Cichlasoma octofasciatum (redrawn from Yapo, 1990).

lengths of 3.5 mm, carp larvae are still inside the egg; so red sea bream completes its metamorphosis at a considerably smaller size. Is this relation between egg size and the completion of metamorphosis exceptional or are there similar cases? Within the Salmonidae, Hucho hucho (Penaz, 1981a, b), Salvelinus namaycush (Balon,1980), and Thymallus thymallus (Penaz, 1975), yolk-sac larvae of 12-15 mm (Fig. 4) are found and the primordial finfold is apparent even later. First-feeding occurs at lengths of about 18 mm, 28 mm, and 19 mm, respectively. Within the Cyprinidae, body length (Fig. 5) at first-feeding is at about 7 mm in Ctenopharyngodon idella (Antalfi and Tölg, 1971), Gobio gobio (Penaz,1981), and Tinea tinea (Penaz, 1982). In Mugil curema (de Sylva, 1984), as in red sea bream, first-feeding occurs at less than 4 mm (Table 1). Although the survey is very limited, we always see a similar sequence of events occurring at different body lengths. The finfold seems to be present in all fish larvae (Moser, 1984; Moser et al.,1984), its function is unknown. Some possibilities are mentioned in the discussion.

A llo m e try

Allometry is a common feature during development. Since evolution ensures the initial investment of enough effort in developing the most essential organs for primary functions, to be followed at a later stage by development of organs with lower priority for survival, are

there sequential patterns of development and do they show certain general trends in the development of teleosts? Fuiman (1983) determined the growth coefficients (in fact the exponent k of a simple power function: y = bxk) in a catostomid, a cyprinid, a salmonoid, and a percid (Fig. 6). He found that the anterior and posterior parts of the body in all these fishes grew faster than the middle section, although at a somewhat greater length range in Osmerus mordax. Percina caprodes showed the phenomenon only weakly in the head but clearly in the tail region. The U-shaped growth profile in early larvae is also recognizable in Clupea 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 intestine, appears to be given priority. This is probably not surprising in view of the easily digested planktonic food, sometimes with powerful digestive enzymes (e.g., in herring, Pedersen, 1987). In early life many fish appear to rely on zooplanktonic prey as an exogenous source of digestive enzymes (Wieser, 1991).

Is this positive allometry of head and tail, with its 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 comparative studies of allometry in fish larvae are not very numerous. Yapo (1990) measured the relative volumes of the brain, muscles, and skeleton of Cyprinus carpio and Cichlasoma octofasciatum from serial sections (Fig. 7). Also here a similarity is observed between the groups, early priority of growth of the brain is followed by the skeleton (cartilage and bone) and muscle tissue. Oikawa and Itazawa (1985) attribute the decrease of the weight exponent in the formula of the metabolic rate of carp during development to the positive allometric growth of the low metabolic activity white muscle after the juvenile stage. The weight-length graph of the carp (Osse, 1990) (Fig. 8) shows a weight increase with length prior to the juvenile stage with a growth coefficient of 4.48; thereafter it is reduced to 3.12, i.e. close to isometry. O ther allometries of length of intestine, body depth, and pectoral fin length with body length are shown in Fig. 9 (Hoda and Tsukahara, 1971). Note that the change of growth coefficient is found at about the same body length, except in the case of gut length. A striking case of sequential growth is seen in the number of primordial germ cells in Barbus conchonius (Timmermans and Taverne, 1989). Their number is constant from about 15 h after fertilization to an age of 21 days. At that time they rapidly increase in number, together with the growth of gonadal primordia, while the animal as a whole grows from 4 to 10 mm TL and from about 2 to 20 mg in wet weight. Another clear allometry in the carp is found in the growth of the gill


10000 -

o>E

f 1000 -

§

100 -

1 0 -

6 8 10 12 14 16 18 20 30 40 60Standard 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,1985). Until about 7 mm TL the surface area of the gills grows with body mass to the power 7.066(1), then reduces to a power function with an exponent 1.222 and to 0.794 at a body weight of less than 1 g net weight. Such allometries are not restricted to carp. The Pacific mackerel (Scomber japonicus (Kramer, I960)) also shows allometric growth (Fig. 11) with a sudden change in growth coefficient of body depth with body length occurring at 8.5 mm SL. Our conclusion is not just that allometries are of general occurrence, but also that there is a similarity in particular allometries at an equal size range of fish larvae in distantly related taxa. Two questions are raised. What causes these events and why do they happen at some specific moment during development from a functional point of view? How do they serve the animal in coping with the environment? We will discuss only the second question.

T h e aqua tic en v iro n m en t

Two types of forces can be distinguished acting on moving objects in fluids: pressure forces and viscous forces. Pressure forces act normally (perpendicular), viscous forces tangentially on a hypothetical element of fluid. Viscous forces correspond with shear stresses.

The forces acting on a moving fish differ with the

hydrodynamic regime. The Re (Reynolds) number can be considered to be the quotient of the inertial and viscous forces (Re = u*l/v), where u and 1 are velocity and length respectively and v is the kinematic viscosity of the water. Viscous forces in the flow around a moving object, e.g., a fish or fish larva, are all important when Re is less than 1. Inertial forces dominate the flow when Re is greater than 200 (inertial regime). When Re is between 1 and 30 the regime is still viscous, because these forces dominate the flow. At 30 < Re < 2 0 0 an intermediate zone is recognized, where the balance between the two forces gradually shifts from a viscous to an inertial regime (Fuiman and Webb, 1988).

Sw im m ing o f fish larvae

Fish larvae can perform two types of swimming, cruising 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 BL s“ 1 (BL = body length). Fuiman and Webb (1988) found that larvae spend 98% of the time in the viscous and intermediate hydrodynamic regimes, of which 23% is in the viscous regime. Figure 12 shows that gliding is very ineffective, the kinetic energy being rapidly lost to friction. Gliding distance is 10% of the total distance covered in 55% of the time of the whole action. During

30 J. W. M. Osse and J. G. M. van den Boogaart ICES m ar. Sei. Symp., 201 (1995)

S.L. 22.5 mm

<d 100 -ctoB” 1 0 -

o

S.L. 9.5 mm

O)c0

50 100 200 40010 205

£

1 100- T3 O JD

° 1 0 -

S.L. 22 mm

_co.0-o

50 100 200 4005 10 20

S.L. 21 mmO)

c 1 0 -

20Standard length (mm)

R edraw n from H oda & Tsukahara (1971)

Figure 9. The relations between body length and length of intestine, body depth, and pectoral fin length in Cyprinus carpio (redrawn from Hoda and Tsukahara, 1971)

100000 -

S.L. ± 20 mm

10000 -

1000 - S.L. ± 7 mm

100 -

1 0 -

0 . 1 -

0.01 -

0.0010.001 0.01 0.1 10 100 1000 100001

Wet body weight (g)Oikawa & Itazawa (1985)

Figure 10. The relation between gill area and body weight in Cyprinus carpio (from Oikawa and Itazawa, 1985). Note that, initially, gill surface grows at the 7th power of body weight.

y=0.715X-0 305- 0 6 -

ye1.147X-0.713

S’ 0 2

S.L. = 8.5 mm

-0 20 6 0.9 10 11

Log standard length (mm)07

Figure 11. Allometry in the Pacific mackerel (Scomber japonicus). Body depth is shown in relation to body length (drawn from data of Kramer, 1960).

escape responses (at burst speeds) Batty (1981) found speeds of 20 BL s_l in plaice larvae of 7 mm. In these latter cases they rapidly leave the intermediate regime to move into a regime with Re values above 200, but even then the first part of this burst swimming is in the viscous and later in the intermediate regime. Another effect of being very small while swimming is a considerable yaw of the head. These effects decrease with increasing fish size (Table 2). Here as well as in plaice larvae (Batty,1981) maximal velocities exceed 30 BL s-1, velocities which are hardly ever achieved in adult fish. This is another demonstration of the importance of scale effects

in growing fish. So the hydrodynamic environment changes significantly during growth and the morphology of fish larvae reflects the influence of the changing balance of forces.

In previous work, Drost et al. (1988a, b) demonstrated effects of the hydrodynamic regime on the feeding and swimming of carp larvae. With a quantitative hydrodynamic model of suction feeding they showed the importance of viscosity effects of the flow inside the mouth of a 6 mm TL carp larva. The conclusion was that 60% of the energy spent in the expansion of the head during feeding (the suction feeding act was completed in


o- - 100«E 10 - - 1 1 0Œ>E 2 0 - -1 2 0i -

3 0 - -1 3 0

4 0 - - 140

5 0 - -1 5 0

6 0 - -1 6 0

- 1 /0

8 0 - -2 0 0

-4 5 09 0 -

10 15 10 205 150Distance (mm)

Figure 12. Burst swimming of 5.45 mm TL carp larvae. Note that gliding is ineffective. From time point 170 msec a distance of less than one-third of body length is covered in 280 ms (from 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, 1986b).

We present here new data of burst swimming of carp larvae and juveniles at four length classes (5.5, 6.6, 10.3, and 20.3 mm TL) filmed at 200 f rs -1 . The analysis revealed (Fig. 13) that the smallest larvae show about equal angles of curvature (anguilliform motion) over the whole body during the acceleration phase. As soon as they have attained velocities of about 5 0 m m s~ \ body curvatures become more restricted to the posterior portion of their body (Fig. 13B). Characteristic Re values have then reached 250. Initially, resistive forces dominate, and then, with increasing speed, inertial forces become more important. Webb and Weihs (1986) propose a resistive model describing the friction forces that counteract movements of the body of the larvae. At low Re values, swimming movements fitting

Table 2. Burst swimming of larval and juvenile carp. Note decrease of frequency of beating and maximal velocity with size and increase in gliding distance.

Total body length (B/L) fish (mm) 5.5 10.4 23.6

Max. tail beat freq. (Hz) 50 20 20Max. velocity (BL s_1) 33 33 11Max. head yaw (%BL) 11 6 5Gliding length (BL) 0.7 1.4 3.4

Cyprinus carpio larvaeAverage maximal angles between successive body segments of 1/12th body length

5 0 1 5 50 mm T.L. 6.60 mm T.L. 10.30 mm T.L. 20.30 mm T.L.40 -

30 -CO£DOo» 20 - a) c <

10 -

0 20 40 8060 100% of total body length

Figure 13. (A) The maximal angles of body curvature, measured over the body divided into 12 segments in larvae and juveniles of Cyprinus carpio during burst swimming. Note the change from resistive swimming, with about equal angles of curvature over the whole body length in small larval, to reactive swimming, with increasing angles of curvature restricted to the tail in bigger larvae and juveniles. (B) Angles of body curvature during burst swimming in a 5.5 mm carp larva. The main curvature rapidly becomes more restricted to the tail region.

this model can be described as anguilliform. This is what we observe initially in Fig. 13A. These authors also mention a reactive model describing the forces 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 movements fit most closely (Webb and Weihs, 1986). This type of movement is seen in the last 40 ms of Figure 13B. So, in the case of Figure 13, a change from resistive to reactive swimming is seen during one swimming bout as a subcarangiform swimming movement is gradually adopted. In larvae longer than 6.6mm, the initial acceleration is higher and body curvature is restricted mainly to the tail (Fig. 13A). The morphological differentiation of the caudal fin (Fig. 14) closely parallels the change in the swimming mode. Ossifica-

0 20 40 60 80 100 ► % of total body length

Cyprinus carpio, larva 5.5 mm T.L. body curvature in successive beats


Cyprinus carpio

length (mm)6.44

0.5 mm

1— > 208.96

7.65

9 13.46

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.


tion of the caudal fin rays and the caudal part of the notochord strengthens the construction to transfer the momentum of the moving water to the larva, thereby making it suitable for reactive swimming (Fig. 14). This is observed at lengths between 7 and 10 mm.

Discussion

Of the many factors influencing growth and development of fish larvae, temperature is the most prominent, as it not only exerts direct influence on the biological objects (Blaxter, 1992) but also the kinematic viscosity of water is reduced by nearly 50% between 0 and 20°C (Daniel and Webb, 1987). Temperature influences body size, growth, differentiation of muscle and meristic characters. In the present overview of development, allometric growth, and the hydrodynamic environment, such temperature effects are not considered in detail. We concentrate on the dynamics of form-function relationships in view of the tight energy budget of fish larvae (Wieser, 1991) and the changing influence of the environment.

Comparison of the sequences of events in smaller and larger eggs (primarily an increase in yolk, cf. Table 1) shows that the larvae from large eggs attain a bigger size prior to hatching, the development of branchial ventilation and first-feeding. Increased size reduces the cost of transport per unit weight and is also significant in reducing predation (Bailey and Houde, 1989). The similarity in the timing of appearance of larval characters in Pagrus major and Cyprinus carpio, although occurring at different body lengths, shows that such sequences are widespread between distantly related groups of teleosts, strongly suggesting their functional importance but also reflecting the different egg size. One wonders whether length is the proper dimension for comparing stages? As explained below, length is important from the aspect of hydrodynamics, but it is also a better measure of morphological development than age. From studies of muscle development (Akster, pers. comm.), it appears that body lengths at which developmental effects occur remain constant despite changes in growth rate due to food conditions or temperature (cf. Fuiman and Webb, 1988). It would be worthwhile extending the comparison between Ostariophysi and Percoidei to establish the consistency of the difference in development between these groups.

The positive allometry of the anterior and posterior parts of the body (Fuiman, 1983) closely parallels the desirability to escape as soon as possible from the viscous and intermediate regime of Re-numbers and so to reduce the drag forces on the body. Beamish (1978) showed that the costs of transport are up to five times higher in larvae, decreasing rapidly with growth (Kauf

mann, 1990). The “preference” for positive allometry of head and tail (also seen in the carp, Van Snik, pers. comm.) can thus be explained as an adaptation to reduce the costs of transport. The intraspecific positive allometries 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 movements of the tail (Batty, 1981). This function of the pectoral fin appeared to be particularly important in small larvae during the approach of a food item, where the pectorals assist in aiming by correcting the yaw of the head. The increased growth of the intestine in 9.5 mm long carp larvae, causing the development of the intestinal fold, occurs synchronously with the restriction of the undulation of the body to the tail region, i.e. with the sub-carangiform swimming mode. The increasing gut length seems appropriate prior to the switch of the larvae from planktonic to more benthic feeding habits. Concomitantly, the ossification of the fin rays of the tail and the caudal segment of the skeleton of the body axis provides the animal with structures suitable for reactive, carangiform swimming (cf. Fig. 14).

The primordial finfold is absent in red sea bream of 8 mm TL (unpaired fins instead), whereas it is still found in carp larvae of about 10 mm TL. In the salmonids shown, it is even found in 24 mm larvae of Salvelinus. The function of the finfold in swimming, respiration, or providing flow-free space for the developing unpaired fins has not been verified. One of the effects of its presence, the great surface of the larva, increases drag and thereby the cost of locomotion. It also reduces the sinking speed of a larva. Jordan (1992), studying undulation of the chaetognath Sagitta elegans, found that in the first 80 ms of the motion inertial forces were unexpectedly high. Is this an effect of its increased body depth due to its finfold and are similar effects present in fish larvae? The early loss of the finfold in the red sea bream and its much longer persistence in salmonid larvae does not suggest an important respiratory function. Wieser (1991), however, notes that the smallest cyprinid larvae may consume as much as 80 mol 0 2g_1 h~’, one of the highest values ever recorded in fish. Is the extra surface area of the finfold an adaptation to achieve this?

Our starting hypothesis, that the patterns of development and growth are reflections of successive functional priorities at different sizes, is confirmed in many cases, but not all. Explanations for such deviations may be found in the considerable differences in habitat of the multitude of fish species.

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