Environmental Factors and Rates of

5 Environmental Factors and Rates of

Development and Growth MALCOLM JOBLING

98 Chapter 5

and particularly so for the earliest part of the life history. A good terminology should be simple and linked to form and function. Difficulties arise in producing a terminology that meets the needs of workers representing different disciplines (e.g. de- velopmental biology, taxonomy, physiology, fish- eries biology and management) and encompasses the myriad patterns of development seen in fish. For example, some species of fish hatch in a well- developed state, especially where there is vivi- parity, ovoviviparity or a protracted incubation period within the egg; other species have short egg incubation times and the fish hatch at a much earlier state of development (Blaxter 1988; Balon 1990; Jobling 1995; Hutchings, Chapter 7, this volume).

Balon (1975, 1984, 1990) proposed a saltatory model of development in which the entire life his- tory, from the fertilization of the egg until death, can be divided into five periods: embryonic, larval, juvenile, adult and senescent. The model is termed ‘saltatory’ because the periods are separated by major thresholds involving a rapid transition to a new ‘stabilized’ state. Each period may be divided into phases, as a convenient means of identifying different levels of morphological or physiological development. Steps, which are the shortest inter- vals of ontogeny, are separated by less dramatic thresholds, and are found within a phase. Meta- morphosis is a major threshold separating the lar- val period from the juvenile or adult period. Early in the life of the fish developmental events are re- flected in rapid morphological and physiological changes, but in each successive period the develop- mental rate decreases until senescence and death.

The embryonic period, starting with fertiliza- tion of the egg, is characterized by endogenous nu- trition. This may be from the yolk or, in the case of viviparous species, nutrition via special absorp- tive organs (Balon 1990). The embryonic period includes a cleavage phase, covering the time between fertilization and the commencement of organogenesis, and an embryonic phase within which there is intense organogenesis within the egg membrane. The embryonic phase continues until hatching, when the embryo enters the eleutheroembryonic phase (Greek eleutheros,

free)(Fig. 5.1) and this continues until most of the yolk has been utilized and the fish begins to take exogenous food.

The larval period starts when the transition to exogenous feeding has taken place. This period lasts until ossification of the axial skeleton. Some embryonic organs persist, and there may be devel- opment of organs which are later lost or replaced by others performing the same function. Examples are surface blood vessels on fins and filamentous appendages used in gas exchange. The larval period may be divided into two phases: the protopterygio- larval and the pterygiolarval phases. The first spans the interval between the first exogenous feeding and the start of fin differentiation. The pterygiolarval phase terminates when the median fin-fold is no longer visible. The larval period may

be long, as in some species of eel (e.g. Anguilla spp.), whereas in salmonids it is difficult to distin- guish a distinct larval period.

The juvenile period begins once the fins are

Fig. 5.1 Recently hatched, free embryos (eleutheroembryos) of two fish species that differ in developmental pattern. (a) The Atlantic cod, Gadus morhua , has small (1.1–1.9 mm diameter) pelagic eggs with a relatively short incubation time (9–25 days) and the fish are small (3.5–4.5 mm) at hatch. (b) Atlantic salmon, Salmo salar, produce large (5–6 mm diameter) demersal eggs which hatch to give large (15–25 mm) offspring after protracted incubation (50–160 days). (Source: from Jobling 1995.) Fig. 5.1 Recently hatched, free embryos (eleutheroembryos) of two fish species that differ in developmental pattern. (a) The Atlantic cod, Gadus morhua , has small (1.1–1.9 mm diameter) pelagic eggs with a relatively short incubation time (9–25 days) and the fish are small (3.5–4.5 mm) at hatch. (b) Atlantic salmon, Salmo salar, produce large (5–6 mm diameter) demersal eggs which hatch to give large (15–25 mm) offspring after protracted incubation (50–160 days). (Source: from Jobling 1995.)

The adult period starts with gonad maturation, culminating in the production of the first gametes. The adult period usually incorporates spawning runs or migrations (see Metcalfe et al., Chapter 8, this volume), specialized reproductive behaviour (see Forsgren et al., Chapter 10, this volume), and changes in external morphology and colour. Spawning may be repeated for a number of years or seasons, as in iteroparous species, or may be per- formed only once, as is the case with the semel- parous species, such as some eels and salmonids (see Hutchings, Chapter 7, this volume). During the adult period, available resources may be directed more towards the development of the go- nads than towards somatic growth. Consequently, rates of growth are generally lower during this period than during the juvenile period.

The senescent period covers a period of extre- mely slow growth during which reproductive activity may also be reduced. The period of senes- cence can last for several years, during which there is a gradual decline in the numbers of fertile ga- metes produced (e.g. sturgeon, Acipenser sturio). Alternatively, the senescent period may last for no more than a few days or weeks, during which time the body undergoes rapid degenerative changes (e.g. Pacific salmon, Oncorhynchus spp.).

Balon’s (1975, 1984) saltatory model and termi- nology of ontogeny are holistic, and there are compelling arguments for their adoption (Balon 1990, 1999). However, they have not been univer- sally accepted due to a failure to highlight some transitional events that many workers consider important. For example, according to Balon’s ter- minology, the larval period is defined as starting when the fish undergoes the transition from en- dogenous to exogenous feeding. Hatching is not

deemed to be sufficiently significant to merit use as a criterion for demarcation of the transition between developmental periods. Many workers, however, consider the larval period to commence at the point at which the fish hatch, and will refer to the newly hatched fish as a yolk-sac larva. Blaxter (1988) recommends that the terms ‘em- bryo’ be used to cover the period from fertilization to the point of hatching, ‘larva’ to cover develop- ment from hatching to metamorphosis, and ‘juve- nile’ for the period from metamorphosis to first spawning. As a supplement to this, Kamler (1992) provided a series of developmental divisions based upon the general sequence of growth patterns dis- played during the early life of fish. An embryo grows slowly from fertilization to hatching, and growth accelerates following the transition to a yolk-sac larva. Larvae grow to reach the maximum size that their yolk reserves will support and then growth rate decreases, usually coincident with the start of exogenous feeding. Between the start of ex- ogenous feeding and final yolk resorption there is often an energy deficit, involving negative growth; after final yolk absorption non-feeding larvae con- tinue to show weight loss and die from starvation, whereas feeding larvae show rapid growth.