Eugene K. Balon

Origin and domestication of the wild carp, Cyprinus carpio: from Roman gourmets to the swimming flowers

Abstract Paleogeographical, morphological, ecological, physiological, linguistic, archeological and historical evidence is used to explain the origin and history of the domestication of the wild carp. The wild ancestor of the common carp originated in the Black, Caspian and Aral sea drainages and dispersed east into Siberia and China and west as far as the Danube River. It is represented today by the uncertain east Asian subspecies Cyprinus carpio haematopterus and by the east European Cyprinus carpio carpio . There is evidence that the Romans were the first to culture carp collected from the Danube, and that the tradition of the “piscinae” was continued in monasteries throughout the Middle Ages. Distribution of the carp west of the Danubes piedmont zone was clearly caused by humans, as was the introduction throughout the continents. Some domestication in China may have been independent of similar activities in Europe, but most of the modern-day activities with the common carp in far east Asia are restricted to the domesticated carp imported from Europe, or at best to hybrids of local and imported strains. The xanthic (red) common carp seem to have first appeared in early cultures of Europe, China and Japan but reached their fame through recent artificial selection of multicolored aberrants in the Niigata Prefecture of Japan. The production of the colored carp — the Japanese “nishikigoi” — presently exceeds in monetary value the production of carp as human food. The nishikigoi as “swimming flowers” delight modern people as much as the taste of carp delighted the Romans at the beginning of carp domestication.

Additions and amendments to the classification of reproductive styles in fishes

SynopsisThe guild concept is explained to represent peaks in the landscape of reproductive styles, which respond to the ‘altricial ⇄ precocial principle’ caused by the processes of heterochrony and saltation. Guilds represent evolutionary trends but not units. New evidence for a specialization within the mouthbrooding external bearers is reviewed, e.g. the unique specialization of juvenile feeding inside the females buccal cavity. Ability to withstand extreme environments is revealed in some water-edge spawners and a new guild of nonguarding aerophils is distinguished. The walleye is placed into another guild and the significance of spawning inside of sponges discussed. Due to a better understanding of reproductive styles used by some external bearers, termed earlier as forehead, skin and possibly armpit and backpack brooders, a single guild of auxiliary brooders is named. The classification of internal bearers is revised into four redefined and renamed guilds — facultative internal bearers, obligate lecithotrophic livebearers, matrotrophous oophages and adephophages, and viviparous trophoderms.

Reflections on some decisive events in the early life of fishes

Abstract A scholarly life-history model, applicable to various ontogenies, requires precise definitions of the major periods and their boundaries. The theory of saltatory ontogeny enables one to construct such a model based on natural boundaries between consecutive intervals of development. This theory stipulates that development does not proceed by a continuous accumulation of inconspicuous, small changes but is a sequence of rapid changes in form and function alternating with prolonged intervals (steady states) of slower development during which complex structures are prepared for the next rapid change. These times of rapid changes from one steady state to the next are called thresholds and represent decisive events of life history. Saltation explains some of the most misunderstood events of ontogeny. For example, it explains why only activation should be accepted as the beginning of ontogeny, and why insemination, fertilization, and hatching are not the appropriate clues for timing ontogeny. Similarly,...

Alternative Ways to Become a Juvenile or a Definitive Phenotype (and on Some Persisting Linguistic Offenses)

Lack of knowledge of early and juvenile development often makes it difficult to decide when a fish becomes a juvenile or, for that matter, a definitive phenotype. According to the established life-history model, a fish develops naturally in a saltatory manner, its entire life consisting of a sequence of stabilized self-organizing steps, separated by distinct less stabilized thresholds. Changes are usually introduced during thresholds. In principle, there are two ways to reach the juvenile period: by indirect or by direct development. Indirectly developing fishes have a distinct larva period that ends in a cataclysmic or mild remodeling process, called metamorphosis, from which the fishes emerge as juveniles. During metamorphosis, most temporary organs and structures of the embryos and larvae are replaced by definitive organs and structures that are also possessed by the adults. In contrast, directly developing fishes have no larvae. Their embryos develop directly into juveniles and do not need major remodeling. Consequently, the beginning of their juvenile period is morphologically and functionally less distinct than in indirect development. The life-history model helps to find criteria that identify the natural boundaries between the different periods in the life of a fish, among them, the beginning of the juvenile period. Looking at it from a different angle, when ontogeny progresses from small eggs with little yolk, larvae are required as the necessary providers of additional nutrients (‘feeding entities’ similar to amphibian tadpoles or butterfly caterpillars) in order to accumulate materials for the metamorphosis into the definitive phenotypes. Directly developing fishes start with large demersal eggs provided with an adequate volume of high density yolk and so require no or little external nutrients to develop into the definitive phenotype. These large eggs are released and develop in concentrated clutches. It therefore becomes possible and highly effective to guard them in nests or bear them in external pouches, gill chambers or the buccal cavity. Viviparity is the next natural step. Now the maternal investment into large yolks can be supplemented or replaced by direct food supply to the developing embryos like, for example, the secretion of uterine histotrophe or nutrient transfer via placental analogues. When the young of guarders and bearers start exogenous feeding, they are much larger or better developed than larvae of nonguarders and the larva period in the former is reduced to a vestige or eliminated entirely. In the latter case, the juvenile period begins with the first exogenous feeding. Such precocial fishes are more specialized and able to survive better in competitive environments. In contrast, altricial forms retain or revert to a life-history style with indirect development and high fecundity when dispersal is advantageous or essential. Fishes become juveniles when the definitive phenotype is formed in most structures, either indirectly from a larva via metamorphosis or directly from the embryo.

Types of feeding in the ontogeny of fishes and the life-history model

SynopsisDifferent types of ontogenies in fishes-indirect and direct- are correlated with different nutrient availability and feeding during early life history. A comprehensive life-history model, developed earlier, facilitates the understanding of decisive events in the life of an organism. Embryos with insufficient endogenous food supply (yolk) to build a definitive phenotype directly need the transient form of a nutrient-gathering larva. They represent an indirect development. In contrast, a large endogenous supply of nutrients enables the definitive adult phenotype to develop directly, avoiding an intervening larva and the cost of metamorphosis. The larger and more advanced an individual at the onset of exogenous feeding, the better are its chances to survive. This can be achieved by heterochronies related to feeding. Different types of feeding during the early ontogeny of fishes — endogenous, exogenous, absorptive, and a combination of all (mixed) — are demonstrated and integrated into the life-history model.

Early ontogeny of Labeotropbeus Ahl, 1927 (Mbuna, Cichlidae, Lake Malawi), with a discussion on advanced protective styles in fish reproduction and development

SynopsisWith yolk as a food source, development of Labeotropheus takes place in the buccal pouch of the female until such time as juveniles are formed. Hatching from the vitelline membrane occurs early, after 6 days of incubation, and the eleutheroembryo develops without metamorphic stages directly into a juvenile, forming advanced structures like fins, skeleton and pigments, at a time when a large yolksac is still present. A strong circulatory network on the yolk and anal fin fold, and a yellow carotenoid pigment provide the oxygen supply within the closely packed buccal pouch. A relatively large self-sufficient juvenile, 14% of the adult fish size, is released from the mothers mouth 31 days after fertilization. The evolution of advanced hiding styles in reproductive guilds of fishes is discussed and ends with a speculation that the Latimeria, having had more geological time to refine its hiding style, releases fully developed young, 25 to 30% the size of the adult fish. The advanced style of hiding eggs is accompanied not only with fewer, larger eggs, but also by a successive increase in yolk density in terms of nutrients and respiratory pigments; these in effect determine the size of the released juvenile.

Early ontogeny of walleye,Stizostedion vitreum, with steps of saltatory development

SynopsisFrequent in vivo observations of arbitrary stages revealed a saltatory pattern of development in the early ontogeny of fluvial spawning walleye. The requirement for an environment rich in dissolved oxygen was indicated by i) spawning site characteristics, ii) the lack of carotenoid pigments, iii) swim-up at hatching, iv) a planktonic (pelagic) existence by means of immobile surface suspension and subsequent surface swimming, and v) a poorly developed temporary embryonic respiratory system, including a subintestinal-vitelline vein, hepatic-vitelline vein and duct of Cuvier. Between the start of hatching and development of the ability to remain planktonic, the temporary embryonic respiratory system was enhanced by an increase in the proportion of the total blood volume passing through the subintestinal-vitelline vein — the largest respiratory surface. Immobile surface suspension was possible due to both the buoyancy of the large oil globule and the forces of surface tension. Also, immobile surface suspension would provide low energy transport from the fluvial spawning grounds to the lacustrine environment where zooplanktonic prey would be relatively more abundant. An intimate relationship between oil globule size (shape) and a dynamic behavioral transition (including the consumption of larger particles, cannibalism, and swimbladder inflation) suggested that energy expenditures occurring during fluvial transport were necessary for appropriate developmental synchrony.

Distribution, community structure and production of fishes in the upper Speed River, Ontario: a preimpoundment study

SynopsisThe upper Speed River, on which a dam was under construction, was surveyed through fourteen qualitative and six quantitative collections to determine the distribution of fishes in the river above Guelph, Ontario and in a tributary, Luteral Creek. At the quantitative localities the removal method was used to estimate density and standing crop of all species. At three of these localities age and growth of the dominant species were determined and total ecological production calculated.Two approaches to the estimation of production for the 0–1 age class were compared and found to result in differences of 33–39% in the estimates of total production, thus illustrating the extent to which methodology may affect such estimatesThe dominant species in the river were, Semotilus atromaculatus, Notropis cornutus, Pimephales notatus, Rhinichthys atratulus, Hypentelium nigricans, Catostomus commersoni, Ambloplites rupestris, Micropterus dolomieui and Etheostoma flabellare. Density ranged from 11126 to 74765 individuals per hectare and standing crop from 32.4 to 190.0 kg ha−1. Production values at the three localities were 15, 19 and 54 kg ha−1 yr−1 , and are low compared with estimates for other fluvial systems. Comparison with a 1951 survey of the Speed River revealed considerable changes in the composition and distribution of fish species. The ranges of several cold-water species had contracted towards the headwaters, whereas several warm-water species had extended their ranges up the river

Fish assemblages in a river with unusual gradient (Luongo, Africa-Zaire system), reflections on river zonation, and description of another new species

SynopsisFish distribution in a river within the drainage system of Zaire headwaters and with an unusual gradient was studied. The Luongo River has high gradient upper and lower sections, separated by a long middle section of no gradients, and bordered by rapids and waterfalls. On the basis of Luongos hydrographic history, topography and fish taxocenes the river is divided into saltatory zones, each zone inhabited by separate homeostatic fish communities. The problem of river natural zonation is argued. Luongo River is, furthermore, unique for its high richness (49 species), biogeographical correlations, and the number of undescribed species found (14%), of which one,Chetia mola, is described in this study. The probable reasons for the richness and for the discontinuous fish assemblages are discussed.

The theory of saltation and its application in the ontogeny of fishes: steps and thresholds

The view that development proceeds gradually is so engraved in our minds that any other possibility is not only treated with disbelief but viewed with distaste. Gould (1977, p. 409) put it admirably: ‘The reconciliation of our gradualistic bias with the appearance of discontinuity is a classical problem of intellectual history. We have sought to reduce the external phenomena of saltation to an underlying continuity of process to reduce the qualitative to the quantitative. Philosophies of change and progress have wrestled with this dilemma and have tried to resolve it by formulating such laws as the ‘transformation of quantity into quality’ of the Hegelian dialectic: the addition of quantitative steps will lead eventually to a qualitative leap . ..‘. It seems it is more comfortable to believe that ontogeny and phylogeny are gradual. Gradual ontogeny can be ‘proved’ by arbitrarily and leisurely sampling a sequence of stages, gradual phylogeny by expectations of finding every ‘missing link’. First, to alleviate the bad taste, I propose to talk of saltation instead of discontinuity. Saltation (Liem 1974, Ruse 1977) seems to be a better term for this phenomenon because it means ‘an advance by a leap or leaps rather than by continuous gradation’. Development is not interrupted, but merely ‘advancing in spurts’ (Webster’s New International Dictionary of the English Language, 1960). The theory was first applied to the ontogeny of fishes by Vasnetsov (1953)’ and Kryzhanovsky et al. (1953). They invented a sequence of ‘etapes’ of quantitative morphogenesis and growth, separated by a combination of brief but distinct qualitative changes in a developmental process. Brody (1945) and Martin