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Fish Larvae, Development, Allometric Growth, and the Aquatic Environment

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Fish Larvae, Development, Allometric Growth, and the Aquatic Environment 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 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 eggs 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 teleosts (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 egg 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., herring), 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 fisheries 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 larva 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 notochord) 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.
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