The oldest domesticated fishes, and the consequences of an epigenetic dichotomy in fish culture.
It is a myth that the common carp was originally domesticated in China, maintained through unfounded repetition but with no evidence. The color aberrations called nishikigoi appeared en masse in the 1950s from the Niigata Prefecture in Japan. These ornamental common carp called koi became the most expensive fish, with some prize-winning individuals valued at more than one million dollars. The criteria for domestication or exploited captives are explained, with special attention to fishes. No attempt is made to resolve the taxonomy of the common carp or goldfish, but some nomenclature data are included to assist future systematic revisions. About 2000 years ago, wild common carp were most abundant in the inland delta of the Danube River at the northern edge of the important Roman province Pannonia. The Romans kept fish in specially built piscinae. Common carp were the hardiest fish available, therefore the most capable of surviving the primitive methods of transport of that time. Keeping carp in ponds became more popular in medieval times, when fasting was enforced and fasting food was in demand. The culture of common carp and the building of special ponds gradually became the most profitable branch of agriculture in central Europe. Some unintentional artificial selection had already taken place between the twelfth and the mid-fourteenth century. Deep bodied and variously scaled or scaleless domesticated forms appeared in nearly every pond system. A domestication of a fish that did occur in China was of the much smaller cyprinid called chi, a fish captured there for food since early times. This silver-grey chi, better known as goldfish, Carassius auratus, occasionally appeared as a xanthic form. These red goldfish have been documented since the beginning of the Sung Dynasty in 960 AD. Releasing such rare xanthic forms into Buddhist ponds of mercy was considered a better deed than releasing an ordinary chi. In the 1200s the fish had become tame and were used as ornamental animals in the garden pools of rich landowners. From the late 13th to the mid 15th century, the Chinese began keeping the golden chi in aquarium-like vessels, and soon rich and poor alike became breeders of fancy domesticated goldfish. The variously shaped monstrosities and color aberrants were freaks, but they became very fashionable at that time and still are. More recently other species, such as the guppy, Poecilia reticulata, and the neon tetra, Paracheirodon innesi, became domesticated in the aquarium hobby. Many other fishes kept as ornamentals such as swordtails and platies, discus and angelfishes, as well as those cultured for food such as rainbow trout, channel catfish and sturgeon are merely exploited captives. The occurrence of alternative phenotypes in some species is explained. These altricial (less specialized) or precocial (more specialized) alternatives are caused by differences in the provision of endogenous food (e.g., yolk) in early development, among other factors, and are a response to changing environments. Life history - from indirect, with an externally food gathering larva, to direct without larvae - is constantly adjusted to fit the fluctuating environment or system created by humans. Recognized in time, these adjustments can have important implications for culture systems.
Es ist ein Irrtum, dass der Karpfen ursprunglich in China domestiziert wurde. Die Farbabweichungen mit dem Namen Nishikigoi tauchten in den 1950er Jahren massenhaft aus der japanischen Prafektur Niigata auf. Diese Zierkarpfen mit der Bezeichnung Koi sollten zu den teuersten Fischen der Welt werden; einige preisgekronte Exemplare erzielten mehr als eine Million Dollar. Die Kriterien der Domestikation oder Nutztierhaltung werden im Hinblick auf die Fische erlautert. Vor rund 2000 Jahren kam der wildlebende Gemeine Karpfen im Binnendelta des Flusses Danubius--der Donau-, am Nordrand der wichtigen romischen Provinz Pannonia, sehr haufig vor. Die Romer hielten die Fische in speziell angefertigten piscinae. Der Gemeine Karpfen war damals der widerstandfahigste Fisch, den man kannte, und er war deshalb am besten geeignet, die primitiven Transportmethoden jener Zeit zu uberstehen. Die Haltung von Karpfen in Teichen wurde erst im Mittelalter ublich, als das Fasten durchgesetzt worden war und der Bedarf an Fastenspeisen anstieg. Die Zucht des Gemeinen Karpfens und der Bau der Teiche entwickelten sich zum profitabelsten Zweig der Landwirtschaft in Mitteleuropa. Ein gewisses Mass an unbeabsichtigter kunstlicher Auslese hatte zwischen dem zwolften Jahrhundert und der Mitte des vierzehnten bereits stattgefunden. In fast jedem Teichsystem tauchten bereits Zuchtformen mit dickem Korper, mit variablem Schuppenmuster und ganz ohne Schuppen auf. In China hatte man eine Zuchtform aus einem viel kleineren Cypriniden namens chi entwickelt, der dort von altersher zu Nahrungszwecken gefangen wurde. Dieser silbergraue chi, besser als Goldfisch bekannt, Carassius auratus, trat ab und zu in einer gelblichen Farbvariante auf. Diese sogenannten roten Goldfische sind bereits seit Beginn der Sung-Dynastie um 960 A.D. belegt. Im 13. Jahrhundert waren die Fische bereits zahm geworden und wurden als Zierfische in den Gartenteichen reicher Landbesitzer gehalten. Vom Ende des 13. bis zur Mitte des 15. Jahrhunderts hielten die Chinesen den goldenen Chi in aquarienahnlichen Gefassen, und bald zuchteten arme wie reiche Leute modische Zierformen des Goldfischs. Die verschiedensten exzentrischen Korperformen und Farbabweichungen fanden damals ihre Liebhaber, teilweise bis heute.
In neuerer Zeit wurden in der Hobby-Aquaristik andere Arten Gegenstand der Domestikation, wie der Guppy, Poecilia reticulata, und der Neonsalmler (-tetra), Paracheirodon innesi. Viele andere Fische werden nur aus wirtschaftlichen Grunden, wie Nutztiere also, gehalten, sei es als Zierfische wie Schwerttrager, Platys, Discus, Kaiserfische, sei es zu Nahrungszwecken wie Regenbogenforelle, Wels und Stor. Das Auftreten abweichender Phanotypen bei einigen Arten wird erklart. Die altricialen (weniger spezialisierten) oder precocialen (mehr spezialisierten) Abweichungen werden durch Unterschiede in der Versorgung mit endogener Nahrung (z.B. Eidotter) und andere Faktoren in der fruhen Entwicklung verursacht und sind eine Reaktion auf Umweltveranderungen. Die Entwicklung von Lebewesen, ihre Naturgeschichte--die indirekte mit Larven mit auBerer Nahrungsaufnahme bis hin zur direkten ohne Larven--wird standig nachkorrigiert, um zu der sich wandelnden Umwelt oder Systemen, die von Menschen geschaffen sind, zu passen. Wenn man diesen Wandel rechtzeitig erkennt, kann man wichtige Schlussfolgerungen daraus fur Aufzucht Systeme ziehen.
Que la carpe commune ait ete, a l'origine, domestiquee en Chine est un mythe. Les aberrations chromatiques, appelees nishikigoi, sont apparues en masse dans les annees 1950, originaires de la prefecture japonaise Niigata. Ces carpes communes ornementales, nommees koi, sont devenues les poissons les plus couteux, certains exemplaires vainqueurs de concours etant estimes a plus d'un million de dollars. On expose ici les criteres de domestication ou d'exploitation d'especes captives, avec une attention speciale consacree aux poissons. Il y a 2000 ans environ, les carpes communes sauvages abondaient surtout dans le delta interieur du Danube, a la limite nord de la grande province romaine de Pannonie. Les Romains maintenaient les poissons dans des piscinae construites a cette fin. Les carpes communes etaient les poissons disponibles les plus resistants et donc a meme de survivre aux methodes de transport primitives de cette epoque. Gerder des carpes dans des etangs est devenu populaire au moyen age, quand le careme etait bien observe et qu'il y avait demande de nourriture maigre. L'elevage de la carpe commune et l'amenagement d'etangs ad hoc ont constiue petit a petit le secteur le plus florissant de l'agriculture en Europe centrale. Une certaine selection artificielle non intentionnelle a deja eu lieu entre le 12e et la moitie de 14e siecle. Des formes domestiquees au corps plus haut et a ecailles variables ou sans ecailles sont apparues dans presque chaque complexe d'etangs. La domestication d'un poisson qui vivait effectivement en Chine a concerne le cyprinide bien plus petit, appele chi, une espece qu'on y pechait pour se nourrir depuis des temps recules. Ce chi gris argente, mieux connu sous l'appellation de poisson rouge, Carassius auratus, presentait a l'occasion une forme xanthique. Ces poissons rouges figurent dans des documents qui datent du debut de la dynastie Sung, en 960. Introduire de telles formes xanthiques, rares, dans des etangs bouddhistes d'action de grace etait considere comme plus benefique que d'y lacher un chi ordinaire. Dans les annees 1200, les poissons ont ete apprivoises et utilises comme ornement dans les etangs des jardins de riches proprietaires terriens. Depuis la fin du 13e jusqu'a la moitie du 15e siecle, les Chinois ont commence a maintenir les chi dores dans des recipients en guise d'aquariums et bientot, riches et pauvres sont devenus eleveurs de poissons rouges de fantaisie domestiques. Les formes monstrueuses tres variees etaient accidentelles, mais elles ont ete tres demandees a cette epoque et encore maintenant. Plus recemment, d'autres especes, comme le guppy, Poecilia reticulata, et le tetra neon, Paracheirodon innesi, ont ete domestiquees pour l'aquariophilie. Beaucoup d'autres poissons d'ornement, les porte-epees et les platys, les Discus et les scalaires, aussi bien que ceux qu'on eleve pour l'alimentation comme la truite arc-en-ciel, le poisson-chat et l'esturgeon, ne sont en fait que des especes captives exploitees. On explique l'occurrence de phenotypes alternatifs pour certaines especes. Ces phenomenes de type altriciel (moins specialise) ou precociel (plus specialise) sont provoques par une alimentation endogene (p. ex., du vitellus) a un stade precocoe, parmi d'autres facteurs, et constituent une reaction a des changements environnementaux. L'histoire de la vie--indirectement, avec un alevin collectant une nourriture externe, ou directement, sans alevins--s'adapte constamment aux fluctuations de l'environnement ou aux systemes crees par l'homme. Reconnues a temps, ces adaptations peuvent avoir des implications importantes sur les systemes d'elevage.
Secondo la leggenda i primi allevamenti della comune carpa furono intrapresi in Cina. L'aberrazione cromatica nota come nishikigoi apparve improvvisamente negli anni '50 nella Prefettura di Niigata Prefecture in Giappone. Queste varianti ornamentali, chiamate koi, sono oggi molto costose ed alcuni esemplari sono stati valutati anche a prezzi superiori al milione di dollari. In questo articolo sono descritti i criteri su cui si basa l'allevamento di questi pesci, con particolare attenzione alla specie. Circa 2000 anni fa la carpa comune era molto abbondante nel delta del Danubio a nord dell'importante provincia romana della Pannonia. I romani, infatti, mantenevano questi pesci in particolari vasche (piscinae). La carpa era il pesce piU resistente, in grado di sopravvivere ai primitivi metodi di trasporto di quei tempi. Il mantenimento della carpa in laghetti artificiali divenne popolare durante il Medio Evo, quando le carestie erano frequenti. L'allevamento della carpa con la costruzione di apposite vasche divenne gradualmente una delle attivita piU redditizie dell'Europa centrale. Alcune varieta erano gia selezionate non intenzionalmente tra il XII e la meta del XIV secolo. Forme domestiche dal corpo elevato e senza scaglie apparvero un po' ovunque in questi stagni artificiali. Anche la domesticazione di un'altra specie di ciprinide, piU piccolo, noto come chi e oggetto di pesca da secoli, comincio in Cina. Il chi e in genere di colore grigio-argento, ma spesso si presenta con una vivace colorazione rossa ed e quindi piU conosciuto come pesce rosso. Il suo nome scientifico e Carassius auratus. Queste varianti rosse sono note sin dalla dinastia Sung del 960. La loro immissione nei laghetti sacri buddisti era considerato di miglior auspicio del rilascio del comune chi. Nel 1200 il pesce entro nella sfera domestica divenendo un animale ornamentale negli stagni dei giardini di ricchi possidenti. Dal XIII al XV secolo, i cinesi cominciarono a mantenere il pesce rosso in vasche simili ai moderni acquari e ben presto sia ricchi che poveri furono in grado di mantenere allevamenti di varieta di pesci rossi. Le varie mostruosita e aberrazioni cromatiche divennero fenomeni da baraccone, ma al tempo stesso ricercati come oggetti di moda e lo sono tuttora. Recentemente altre specie, come il guppy, Poecilia reticulata, e il pesce neon, Paracheirodon innesi, sono state addomesticate per gli amanti dell'acquario. Molte altre specie sono allevate sia a fini ornamentali, come ad esempio lo swordtail e il platy, i discus e i pesci angelo, sia a scopi alimentari come le trote, i pesci gatto e gli storioni. In questo articolo si da spiegazione anche della comparsa di fenotipi alternativi. Queste varianti altricial (meno specializzate) o precocial (piU specializzate) sono causate, soprattutto, da differenze nelle riserve endogene di cibo (ad esempio, il tuorlo) nelle prime fasi di sviluppo e rappresentano una risposta all'ambiente mutevole. La storia naturale--variabile da una forma indiretta, con una larva attiva nel procacciarsi il cibo ad una diretta senza stadio larvale--e costantemente aggiustata per adattarsi alle fluttuanti condizioni ambientali o anche in seguito all'intervento dell'uomo. Riconosciuti da tempo, questi adattamenti possono avere importanti implicazioni per l'allevamento.
Domestication, origin, common carp, goldfish, guppy, neon tetra, exploited captives, alternatives in fish culture, altricial and precocial
A domestic animal can be defined as one that has been bred in captivity for purposes of economic profit to a human community that maintains total control over its breeding, organization of territory, and food supply.
Juliet Clutton-Brock (1999: 32) in A Natural History of Domesticated Mammals
Domestication by humans, particularly of fishes
The definition of domestication by Clutton-Brock should apply also to fishes subject to some amendments (e.g., Diamond, 2002). First, allow me to repeat some of my earlier musing on that subject (Balon, 1995b: 5): "The questions of where and how organisms were first domesticated have occupied many scholars. Definitive answers are rarely produced (Zeuner 1963, Isaac 1970) because most of these domestications started already in the Neolithic (roughly 14,000 years ago). 'In the study of domestication the scientist and the cultural historian join forces, each playing a role which the other discipline, by its very nature, cannot fill' (Isaac 1962). (...) In a truly domesticated organism, (a) the individual is valued and kept for a specific purpose, (b) its breeding is subject to human control, (c) its behaviour is different from that of the wild ancestor, and (d) its morphology (including size, coloration and physiology) exhibits variations never seen in the wild, (e) some of which would not survive without human protection."
The best known examples of domestication are the transformations of wolves into breeds of dogs, the aurochs into cattle, the guanaco into llama and alpaca, the wild boar into domestic swine, Przewalski's wild horses into domestic horses, and the red jungle fowl into domestic chickens. Dependence is the most important among the more obvious criteria. "All domesticated animals depend for their day-to-day survival upon their owners. The capacities of wild self-sufficiency having long since been subtracted from them, they must depend upon whatever prosthetic devices their owners see fit to provide" (Livingston, 1994: 14).
However, the matter of dependence also applies to animals at the first stage of domestication which Clutton-Brock (1999) calls exploited captives and others call tamed or cultured. Most recently wapiti deer have become such captives on farms neighbouring our residence in Canada. Many attempts at domestication remain only at that level. Most fish cultured as food and as ornamentals also remain merely exploited captives, especially in cases where wild individuals are occasionally brought into the stock bred in captivity. To be a true domesticate, therefore, the earlier mentioned criteria (d) and (e) must apply, i.e., shape, size and coloration exhibit variations never or rarely seen in the wild ancestor. Some of these variants would not survive without human protection in captivity. Furthermore, the original criterion of Clutton-Brock (1999), that of economic profit, may only partially apply to domesticates as pets. Fishes that are introduced by humans into waters other than their native waters and become established there are termed naturalized by Lever (1996). We are not interested in these in this treatise.
Fishes became objects of domestication much later than the domestication of many other animals and plants, now fixed by Diamond (2002) at around 10,500 years ago at the earliest. Even adding their time as exploited captives, in a strict sense only two fish species qualify: the wild common carp, Cyprinus carpio Linnaeus, 1758, acquired by humans about 2000 years ago, and the wild chi better known as goldfish, Carassius auratus (Linnaeus, 1758) selected and released into ponds of mercy about 1000 years ago; the former by the Romans in south central Europe (Balon, 1974, 1995a, b), and the latter in China (Chen, 1956; Wang et al., 2000). Only recently some other fish species may qualify, although confusion reigns because different criteria are used. At best, statements like "only the common carp, the crucian carp (Carassius carassius) and the goldfish (Carassius auratus) have been truly domesticated with the management of all stages in the life cycle, particularly reproduction for a longtime" (Billard, 1999: 4) are justified, but the crucian carp does not belong here (see later). This study is about domestication. The taxonomy of the common carp and goldfish is not attempted but significant data related to nomenclature of these species, so far ignored by systematicists, are included. A putative and brief synthesis of these data is designed as a guideline for the future solution of the complex problem.
The two closely related cyprinids, the wild common carp and the wild goldfish, began to be changed into true domesticated animals in early medieval times, though in different parts of the world and for different purposes (Chen, 1956; Balon, 1969, 1974, 1995b). The other, very few modern domesticated fishes are rather poorly defined and of questionable status (Zeuner, 1963). In contrast to the extinct aurochs, ancestors of domestic cattle or the nearly extinct in nature Przewalski horse, only the wild common carp may be close to extirpation at its area used for initial domestication, replaced in the wild by the feral progeny of domesticated forms (Fig. 1).
[FIGURE 1 OMITTED]
The loss of the ancestral wild forms of any domesticated organism means a tragic loss of epigenetic potential. Clutton-Brock (1999: 30) believes "that animals bred under domestication evolve into new species as a result of reproductive isolation from their wild progenitors..." (my italics). Domesticates released into the wild to fend for themselves usually perform poorly and, while in time some revert their shape to resemble their wild ancestors, the process is nearly always incomplete. All such feral forms remain poor facsimiles of their progenitors (Livingston, 1994). Following the above criteria, I will classify fishes kept by humans first as exploited captives that are little changed from the wild ancestral forms, and can usually be returned to the wild. Nevertheless, exploited captives are often the first step in domestication with profound changes in behaviour (Price, 1999). Animals become domesticates when they change in form, function, color and behavior from their wild ancestors, and if returned or accidentally released into the wild without human protection they survive poorly as feral forms, often only partially resembling their ancestors.
Several more domesticates have been produced in the aquarium industry for ornamental (e.g., guppy, swordtails, platies, mollies, neon tetras, discus, angelfishes) or research (medaka, zebrafish) purposes. These are few and mostly of very recent origin or of questionable status. Fishes reared in captivity for human food like the channel catfish, salmon, the Chinese and Indian pelagic spawning carp, tilapia or sturgeon, to mention just a few, are exploited captives. Artificial propagation of rainbow trout, Oncorhynchus mykiss, for food or stocking has led to the creation of hatchery forms that Behnke (2002: 103) considers domesticates. In spite of color changes and "a loss of the ability (...) to compete with non-game fishes for a common food supply" these trout are merely exploited captives. However, the few that are undergoing purposeful artificial selection as color aberrants will qualify as domesticates (Goryczko and Dobosz, 2004).
The epigenetic processes that act in domestication also modify the life histories of the fishes, allowing survival of both altricial and precocial forms (Balon, 1990, 2004a,b). The existence of alternative forms and their life-history modifications are explained in the final section, including some aquaculture implications.
Domestication of the common carp did not originate in China!
The origin of common carp domestication is still confusing authors as evidenced in the recent work by Liu (2003), in spite of much more precise data given by Banarescu, Grzimek and Ladiges in the first edition of the same encyclopedia. The reason for the frequent claims that common carp domesticates came to Europe from China is that common carp and goldfish were not only misidentified in the past but also occur in places that are far apart, and so it is "one of those things which somebody said a long time ago, having no real or precise knowledge of the subject, and that it has been slavishly copied ever since" (Burton, 1969, inside cover of issue 48), from one book to another (e.g., Leonhardt, 1906; Tamura, 1961; Hickling, 1962; Rudzinski, 1961; Steffens, 1967, 1980; Borgese, 1980; Liu, 2003). Bloch (1782: 93) clearly stated: "Das Vaterland des Karpfen ist ohnstreitig in den sudlicheren Theilen Europens zu suchen", and so earlier authors (e.g. Day, 1865 or Taylor, 1884: 7) were correct in stating "it is all but certain that the carp was brought from southern Europe to the more northerly parts; its great size and esteemed flavour rendering it a favourite."
Details of this argument concerning the common carp have already been given by Balon (1974: 21): "The latest Chinese study (the following quotations are from the Russian translation, Anonymous, 1961) on pond culture stated that 'thanks to the creative efforts of the Chinese people for many generations, breeding of the carp in this country has proceeded successfully for more than 2,000 years. From China the breeding of this fish spread all over the world. (...) From Asia the rearing of the carp spread to Europe and later to America, Australia, and Africa' [my translation from Russian]."
Let us finally put this myth to rest (Balon, 1995b: 8-9): " 'Kwai Sin Chak Shik, a book written during the Sung Dynasty in A.D. 1243, describes how carp fry were transported in bamboo baskets in much the same way as they are transported and traded today. The fry were collected in rivers and reared in ponds; this is recorded in A Complete Book of Agriculture, written in A.D. 1639.' But if the fish 'fry were collected in rivers' it is doubtful whether they were the common carp, Cyprinus carpio, which is not a riverine pelagic spawner. It is more likely that they were the young of other carps, such as the grass carp Ctenopharyngodon idellus (Valenciennes, 1844), the silver carp Hypophthalmichthys molitrix (Valenciennes, 1844), the bighead carp Aristichthys nobilis (Richardson, 1845), and the black carp Mylopharyngodon piceus (Richardson, 1846), of which, some are true riverine pelagic spawners and cannot be bred in pond or rice paddy conditions." Furthermore, no domesticated forms of common carp, like the mirror or leather, or even the high-bodied forms (Pokorny et al., 1995), were ever reported from China prior to known introductions from Europe (Wohlfarth, 1986). Kottelat (1997: 57) writes that "Balon (1974, 1995) discussed the origin of domesticated carps and concluded that the European ones originated from a rheophilic stock from the Danube. I agree with him and Hoffmann (1995a) that it is unlikely to have been imported from China, as is often assumed" (see also Zeuner, 1963). And, therefore, in addition to the above "It may be noted [concluded Wohlfarth, 1984: 377] that in most of the traits in which the races differ, the Chinese carp are more similar to wild carp than the European. The Chinese common carp should be regarded as a semi-domesticated animal, since wild fish are frequently added to breeding stocks." So the myth of common carp domestication in China more than two thousand years ago is just that--a myth. In China the common carp remains at best as an exploited captive or a feral form of the introduced European domesticates.
The European domestic forms were later introduced to eastern Asia (e.g., Basavaraju et al., 2003). The still lingering myth that carp came to Europe from China seems impossible. "Common carp were known and used in the fish culture of western Europe well before any direct European contact with China [emphasizes Hoffmann, 1995a: 75]. The fish culture methods used in the west since at latest around 1200 were, with their emphasis on special ponds kept permanently filled for several years growth of a single age class and then dry for a time after harvest, are quite the reverse of a fish culture integrated with rice paddy cultivation. And finally, given the known locations of common carp in Europe and of the earliest European fish culture enterprises, we can rule out the indirect route from China via the Middle East..."
The common carp, Cyprinus carpio
"Aristocrat! Aristocrat!" he cried. Luckily, knowing him better, I was able to explain. Far from wishing to send anyone to the guillotine, what he meant was that trout were aristocratic fish, the plaything of the rich, whereas effort would be better devoted to popularising carp culture, the ideal pond fish, he averred, for hungry villagers.
Peter B. N. Jackson (2001: 40-41) in Freshwater Fishery Research Organisations in Central and Eastern Africa. A Personal Recollection.
The earliest domesticate and the most important fish in aquaculture, the common carp, Cyprinus carpio Linnaeus, 1758, was made taxonomically also the most confusing species. According to the latest review by Barus et al. (2002: 87) it remains without a holotype and was described "using specimens from a pond culture, designating Europe as the terra typica. Presuming that all domestic European forms originated as wild carps from the Danube, specimens from the Danube River can be considered as typical."
Most of the confusion comes from giving taxonomic names to local or feral specimens or populations. The common carp is very variable and forms easily distinct local morphotypes (see fig. 6-8 in Balon, 1995b). Since earliest times, these forms have tempted authors to give these deviants separate names (e.g., Bloch, 1782; Heckel and Kner, 1858; Antipa, 1909; Zhou and Chu, 1986). These morphotypes were later proven to develop relatively fast from the wild common carp in pond culture (see e.g., Tuca, 1958; Bastl, 1961; Misik and Tuca, 1965). For example, Zhou & Chu (1986) list 12 "species" from Yunan Province, China, and Barus et al. (2002) ended up with a rough count of more than 30 synonyms and over 10 subspecies, varieties and morphs from across its range in comparison with Kottelat's (1997) about 15 and 8, respectively. Barus et al. (2002: 115), after a tortuous review using the best data available (e.g., Misik, 1958), concluded that at the present time only three subspecies of wild C. carpio can be recognized: "1. The European and central Asian wild common carp, Cyprinus carpio carpio (...); 2. The east Asian wild common carp, Cyprinus carpio haematopterus (...); [and] 3. The south-east Asian wild common carp, C. carpio viridiviolaceus (...)." None of the data are convincing, nor is the claimed occurrence of C. c. haematopterus throughout east Asia from the Amur River across China, Korea and Japan (Svetovidov, 1933). C. haematopterus was described as a separate but now invalid species (Eschmeyer, 1998: 701) from the area of Nagasaki, Japan, in von Siebold's Fauna Japonica by Temminck and Schlegel (1845); the #2400 holotype parades among the "stuffed" specimens in the Rijksmuseum van Natuurlijke Historie, Leiden, Netherlands.
More than 200 years earlier, "the first Portuguese and Dutch colonies were established at Nagasaki. By then common carp culture was widespread in the European homelands of these colonists and it is therefore possible that the common carp was introduced by them to Japan" (see Balon, 1995b, caption to fig. 5 on p. 10). The Nagasaki Municipal Museum is below and next to the Atomic Bomb Museum. If one escapes the horrors above, tableware decorated with common carp images once belonging to these early Dutch colonists can be seen on display (e.g., Fig. 2). At the very least this demonstrates an interest in the common carp by Dutch colonists of the sixteenth and seventeenth centuries. While the species of common carp described from the area as "haematopterus" erroneously became the nominal subspecies for the huge area of China more than two centuries later, it is more correct to consider the common carp even there as feral descendants of European domesticates that escaped or were introduced to Japan and possibly China. So far the results from molecular markers have been largely inconclusive (e.g., Froufe et al., 2002; Kohlmann et al., 2003). Hence, before this taxonomic confusion can be resolved, if ever, it would be more prudent to consider the wild ancestor of the common carp as a single species, Cyprinus carpio, widely distributed from the Danube to the Amur rivers, as feral forms elsewhere (but see Kottelat, 1997) and as naturalized "wherever suitable conditions prevail" (Lever, 1996: 92). Do books like Guidon's (1983) The World According to Carp or Bradley's (1997) This Book is Full of Carp merely illustrate unjust American disgust with the fish or its popularity?
Wild common carp, the ancestor of the domesticated forms
All data so far point to the wild common carp from the Danube River as the most ancestral form (Fig. 3) that was initially kept as exploited captives and later domesticated. The inland delta of this river, recently badly damaged (Balon and Holcik, 1998, 1999) by the infamous Gabcikovo water works, was the area closest to cultural events opportune to interest in the carp. Carp remnants found in archeological excavations of Roman settlements in this area confirm that common carp was indeed already then of interest (Balon, 1995b). We will therefore focus entirely on describing the wild common carp from this area before it was extirpated or replaced by feral forms.
[FIGURES 2-3 OMITTED]
Around 1955 large schools of the wild common carp were still spawning every year over many inundated meadows along the Slovak part of the Danube and Lesser Danube (see Misik, 1957; Bel, 1962). As it was assumed that these fish were the direct descendants of much larger schools of wild common carp exploited by the Celts and Romans in the same area about two millennia earlier, I initiated detailed studies of these fish with my late laboratory assistants Victor Misik and Julius Bel (Balon and Misik, 1956; Balon, 1957, 1958a,b; Misik, 1958). There follows a brief summary of these studies already presented earlier by Balon (1995a,b) and again compiled by Barus et al. (2002).
The wild common carp had a long, round, torpedo-shaped body with the transition from head to the trunk forming an almost straight line dorsally, and not showing the depression (notch), typical for most domesticated or feral carps (Fig. 4). Very regular, large scales covered the entire body, each scale pigmented dark at its joining edge, giving the body a mesh-like appearance. The basic coloration was a golden body, darker on the dorsum and lighter at the ventrum, head and dorsal and caudal fins greenish-brown, the ventral parts of the caudal fin, anal and pelvic fins, lips and barbels light with an orange tinge (Fig. 3). The lateral line pores pierced scales through the middle of the sides and were complete but barely visible on live individuals.
[FIGURE 4 OMITTED]
The females have, on average, longer heads than males. The average length of the front barbels is about half that of the rear barbels. The females have a broader forehead than males. At spawning time males develop breeding tubercles which appear as pinhead sized white granules on the scales above and below the lateral line, on the caudal peduncle and on the head, especially on the anterior parts of opercles, preopercles and under the eyes. Tubercles occur even along the insides of first rays of the pectoral and pelvic fins, and along the unbranched rays of the dorsal, anal and caudal fins. Breeding tubercles develop also in some females, but only on the head; never on scales or fins.
The morphometric characters are given in Table I. The number of spines and rays in the dorsal fin of the Danubian wild common carp was (II) III-IV 18-21 (22); the number of spines and rays in the anal fin was (II) III 4-5 (in both fins the last spine was a large bone strongly serrated along its posterior edge, one of the best bones for carp identification in archeological samples); the number of spines and rays in the caudal fin was IV--VIII 16-18 IV--VIII; the number of spines and rays in pelvic fins was II 7-9 with no significant difference between females and males. The number of scales in the lateral line was (34-35) 36-39 (40) with no difference between left or right side or between sexes, and the number of scales above and below the lateral line was always 5-7/5-7. Number of gill rakers outside/inside was 22-28/29-34 with the inside number always higher and no difference between sexes. The pharyngeal teeth were moliform with clear grooves on the crushing surfaces, in three rows as 1.1.3-3.1.1. The differences between these characters of the wild common carp from the Danube are insignificant in comparison with these from the common carp of the Amur River. Overall, the variation in characters compiled by Barus et al. (2002) greatly overlap and subspecific differences appear only if forced statistically. Similarly, the differences in morphometric characters between the Danubian and Amur River wild common carp are insignificant (Table I). The Danube females were larger than the males (498.5 [+ or -] 11.17 versus 447.5 [+ or -] 6.95 mm standard length).
The karyotype of the wild common carp is 100 (2n) of somatic chromosomes. There is a remarkably large number of ??chromosomes; no sex chromosomes were ever found. "Karyotype of the wild common carp, C. carpio, from the Danube is identical with those of the cultured domestic Rumanian, Hungarian and Ukrainian forms of the carp (Raicu et al. 1972) as well of the French ones (Hafez et al. 1978). Similarly, no substantial differences exist between the karyotypes of European carps and some Chinese subspecies (Zhan & Song 1980; Rab 1995). Rab (1994) stated that there is no difference between the karyotype of carps from wild populations in the Danube and that of wild carps from the Amur River" (Barus et al., 2002: 94-95).
The life history and ecology of the wild common carp was compiled in detail by Balon (1967b, 1974, 1995a,b) and again by Barus et al. (2002). For the sake of brevity only some selected highlights will be repeated here.
In the Danube the wild common carp females released two or three portions of eggs within 10 to 14 day intervals. In 1955 the carp spawned in large schools on the inundated meadows above the village of Kolarovo (Fig. 5). The first spawning occurred on May 6th and 7th, but because of receding water and a sudden drop in temperature the spawning was interrupted. It resumed between the 5th and 7th June when the flood returned and the temperature rose to 18[degrees]C. Although various forms of the domesticated carps--deep bodied and of irregular scalation--stocked into this area were present in the vicinity, only rarely were one or two such individuals caught within the school of hundreds typical wild common carp. Furthermore, such single domestic forms caught with the wild common carp were always immature or not in spawning condition. Later Lelek (1987; Brunken et al., 1989) established that the feral carp in the Rhine, morphed close to the ancestral wild common carp, also maintained spawning allochrony from the domesticated forms. Is the "species recognition concept" advanced by Paterson (1985, 1993) that precise?
[FIGURE 5 OMITTED]
The age and growth of the wild common carp, determined from scales of the subsample from the spawning school at the inundated meadows near Kolarovo, is shown in Table II (Balon, 1957). Males belonged to age groups 3 to 15, mostly group 5, and females to age groups 5 to 9, most of them in age group 7.
The activated eggs of the wild common carp have a yellowish tint and are 1.5 to 1.8 mm in diameter. The outer egg envelope is adhesive and sticks to grass blades, preventing the eggs from falling onto the anoxic bottom of freshly flooded grassland. At about 20[degrees] to 23[degrees]C, most embryos hatch in three days. For about two days after hatching the free embryos hang in a vertical position on the grass blades. Five days after activation, the posterior part of the swimbladder is filled and swimming horizontally, the larvae start to capture and ingest external food (Balon, 1958a, 1995b).
"When we subsequently witnessed [writes Balon, 1995b: 19] similar turbulent mating of wild carp groups on other freshly flooded meadows along the Lesser and main Danube's inundation areas, by then already grossly restricted by flood dikes, it became obvious to me that the original floodplain of this piedmont zone of the Danube (e.g., Makkai, 1985) must have been clearly dominated by this fish during Celtic and Roman times. (...) Holcik (1995b) recently noted: 'The wild carp was commercially harvested four decades ago (...) At present, however, its distribution is restricted to the minor part of the main channel of the Danube. Only single specimens are occasionally caught. Of 1536 fish taken, tagged and released in the Danube at Gabcikovo in 1993, only 5 (0.3%) were a carp but only one still displayed the typical characters of the wild form! (...) The extinction of (...) the wild carp is expected within a decade...'." (see also Holcik, 2003).
Lucullan demands, Pannonia and the first carp captives
Whereas the genuine wild common carp thrived in the area described above more than 2000 years ago, still lived in historical times, and was abundant enough only 50 years ago to lend itself for major studies (Fig. 6), none may be left now. Two significant historical events coincided and contributed to the fact that for the first time wild common carp from this area became not only a major food source but also exploited captives:
(1) In the last years BC and in the first and second century AD, an extraordinary luxury, even excess, of food consumption, and the associated importation of foreign foods developed among the Romans (Friedlander, 1936). Sergius Orata, the teacher of Cicero, devised special reservoirs where fishes for the kitchen were stored. These reservoirs called piscinae soon became very fashionable, for they ensured a permanent supply of a variety of fresh fishes independent of weather conditions and fishing success (Zeuner, 1963). Fish rearing in piscinae was adopted, for example, by Lucinius Muraena, who began adding freshwater fishes to the initially stored marine ones (Pliny the Elder AD 24--79; in translation 1958-1962). The patricians soon competed in building such piscinae. To bring water to his ponds, a reputed gourmet, Consul Lucullus (75 BC), dug a trench that cost more than his villa through a hill near Naples. Varro (116-27 BC; 1912) and Columella (~50 AD; 1941-1968) claimed that the Roman patrician preferred seawater ponds, and that freshwater ponds (piscinae dulces) were considered plebeian, but the documented prejudice is proof of their existence. Also, the existence of "plebeian" owned fish ponds may signify that the desire to transport wild common carp from the Danube to patrician piscinae in "Italia" was applicable also to plebeian troops and the accompanying tradesmen and artisans (but see Hoffmann, 1995, Appendix A).
(2) In the first years AD, the Roman Empire expanded its northern boundary beyond the barrier of the Alps right up to the banks of the Danube River (Sitwell, 1981). The northernmost province Pannonia faced formidable forces of Celts and Germans across the Danube and the Empire had to establish a strong military presence quickly (Fig. 6). "In the second century, the comparatively short stretch of river between Vienna and Budapest, about 150 miles long, required no less than four legions to guard it--X Gemina at Vienna itself, XIV Gemina Martia Victrix (...) at Carnuntum, I Adiutrix at a place called Brigetio (...), and II Adiutrix at Aquincum (now Budapest). By contrast, all of Roman Britain in the second century required only three legions; Roman North Africa managed with a single one" (Sitwell 1981, p. 120). "To paraphrase further from Sitwell's synthesis [continued Balon, 1995b: 23-24], these at least 20 000 fighting legionnaires were accompanied by supporting troops, wives, mistresses, children, slaves and tradesmen to a total of more than 100 000 Romans, in addition to 'indigenous communities (civitates) [which] came under the military control of a high-ranking officer (...) from a neighboring Roman unit. (...) there was at least one auxiliary unit for every two civitates' (Mocsy 1974, p. 49). These together formed a human population large enough to establish a carp-eating tradition, if a wild common carp was, as I believe at least seasonally, the most abundant and most easily caught fish in the area. The influence of this youngest province and its army was so strong that 'instead of Rome controlling the Danube frontier, it would be nearer the truth to say that men from that frontier controlled Rome' (Sitwell 1981, p. 122)."
[FIGURE 6 OMITTED]
Movements of legionnaires, troops, auxiliary units and civilians from Pannonia across or around the Alps to Poetovio, Emona via north-eastern Italia to Rome [...] required the construction of relatively good roads (see also fig. 59 in Mocsy, 1974), one of which ended as the Roman branch of the Amber Road at Devin--Marus (Morava) River entry into the Danube--and crossed the Danube north into the Celtic, German and Sarmatian territory toward the Baltic Sea as a footpath. Legionary fortresses and Roman towns were established at the edge of the largest floodplain area within the piedmont zone of the Danube: castra and colonia Carnuntum upstream and castella Gerulata (now Rusovce) downstream of the Morava (Marus) River entry into the Danube at the upper end of the floodplain. Castellas Ad Flexum, Quadrata, Arrabona and Ad Statuas before the larger castra and colonia Brigetio (now Szony) at the Vah (Duria) River entry opposite the castella Celamantia (near today's village Iza) at the floodplain's downstream end. This floodplain area was utilized as the westernmost spawning grounds of the wild common carp, Cyprinus carpio. So the carp must have been well known to the Romans in Pannonia.
Under the rule of caesar Hadrian (117-136 AD) and later of Marcus Aurelius (161-180 AD), the Romans built a smaller military fort (castellum) Celamantia across the river from Brigetio, within the Danube floodplain. Repeatedly repaired, the stone fort was finally abandoned shortly after
the death of caesar Valentinius I (375 AD). Archeological excavations at Celamantia were resumed over the past 20 years because of its possible submersion by the Gabcikovoaqua Nagymaros water works (Rajtar, 1990, 1992). In earlier such excavations at Carnuntum and Brigetio interest in Roman man-made artefacts prevailed. At Celamantia on this occasion fish remains were also carefully sampled, revealing that the bones of the wild common carp outnumbered all other fish bones (K. Hensel, personal communication). Together with those from Novae on the lower Danube (Szymczyk, 1987) and Nicopolis ad Istrum from 100-450 AD (Irving, 1994) these samples from Celamantia (Fig. 7) constitute the first direct evidence that Romans knew the wild common carp of the Danube well. It is most likely therefore, that, while living on the Danube in Pannonia the Romans, not only consumed the wild common carp but also transported them alive to other Roman provinces, because of the popular fashion at that time of keeping fishes in piscinae. Returning to "Italia", many thousands of soldiers probably demanded to be served their customary fish, so influencing the importation of common carp. After all, the common carp was the largest, tastiest fish that might have survived the rigors of transport.
[FIGURE 7 OMITTED]
There is so far no written or archeological evidence of common carp being kept in piscinae or vivaria in Rome 2000 years ago (Zeuner, 1963; Hoffmann, 1995a). Since written records from this time are generally scarce even regarding activities that have been proven for that period by other means, the keeping of carp by Romans in those times is still highly likely. After all, Walton (1676: 146) claimed "Tis said (by Jovius [who probably was Paolo Govio, a papal physician, who wrote about fishes on the Roman market in 1524, Richard Hoffmann, personal communication], who hath writ of fishes) that in the lake Larius [Lake Como] in Italy carps have thriven to be more than fifty pounds weight." These early introductions of the wild common carp west of the middle Danube were probably only using the animal as an exploited captive.
The history of common carp domestication Andreska (1987: 32) states in the chapter on the common carp and ponds that "old chroniclers in their writings dealt not with unessential details. They have written mainly about saints, rulers, wars and wondrous celestial signs. About who was the first in bringing (...) seeds of the carp, they left not the slightest record" (my translation). The earlier assumption that the keeping of common carp in monastery ponds continued after the collapse of the Roman Empire and the establishment of Christianity is a pure conjecture regarding the period from the early middle ages to the tenth century (Hoffmann, 1995a). It is based on two logical assumptions. First, that monasteries began to be founded in the fifth and sixth centuries and soon acquired land and farms. Second, that Christianity introduced more than 180 fasting days per year which were mainly observed by dutiful monks, nuns and priests, thus interest in the common carp should have survived.
On fasting days the only flesh that might be eaten was that of aquatic animals such as shellfish and fishes--and also in some regions unborn rabbits called laurices--thus these customs are directly linked to Roman tradition (see more in Balon, 1967c, 1995b). The only evidence that the Roman taste for eating common carp continued is from Cassiodorus (AD 490-585;1626) who ordered delivery of the wild common carp from the Danube to Italy for the table of King Theoderic.
The first to write about breeding common carp in ponds was Albertus Magnus in the 1260s (1193-1280; 1861), he may however compete for this privilege with the Count of Champagne who according to Hoffmann (1994a: 142) was breeding common carp in 1258. Hoffmann states that "no remains or verbal mentions from before the twelfth century suggest carp culture or artificial fish ponds. These are wild fish." Ponds with muddy bottoms have been built since the tenth century (Hoffmann, 1985; Andreska, 1987), and wild common carp became established in them in the twelfth century at the latest, judging from the relatively fast process of domestication as reported by Tuca (1958), Bastl (1961) and Misik and Tuca (1965). So it seems that in the common carp the transition from exploited captive to truly domesticated animal took place in the twelfth century.
Modern carp culture: "To build a fishpond, not just a holding tank, is to create a new aquatic habitat. Active construction of ponds for this purpose got under way in the eleventh century [documented Hoffmann, 1995a: 67] and increased rapidly in the twelfth and thirteenth." While initially these ponds were stocked with several local fishes, common carp soon proved to be the best choice for such man-made habitats. Hoffmann (1994a, b, 1995a: 72) compiled the evidence for medieval times in Europe and concluded that: "Verbal and archeological evidence thus together corroborate three phases in the medieval diffusion of common carp west and north from an epicentre at the north-west margin of its native range in Pannonia (the piedmont section of the Danube, Balon 1967a). The first phase between perhaps the seventh and the eleventh centuries principally carried the fish up the Danube and into at least some west-flowing tributaries of the middle Rhine. Some remains also indicate carp in waters north of the Danube. In a second phase (twelfth to the early fourteenth century) common carp radiated across most of the economic and cultural heartland of medieval northwestern Europe, from the lower Rhine/Maas region south to the Paris basin and Burgundy. In a final stage, probably occurring after the mid-fourteenth-century shift of economic trends, extended common carp into the outer periphery of the west, an arc from southwestern France through England and southern Scandinavia into east central Europe. Though carp are recorded in Italy at the end of the Middle Ages, the diffusion pattern at no time accords with radiation from there."
In time more written evidence appeared and by the early fourteenth century culture of the common carp was well established (Pucher, 1987; Hoffmann, 1995b, 2002). Soon the entire procedure of pond carp management was described in the famous Latin manual by Jan Dubravius (1547) (1) written between 1535 and 1540, and by Olbrycht Strumienski (1573) who reported on the Czech and Polish techniques of that time (Strojnowski, 1609; Susta, 1889; Inglot and Nyrek, 1960; Szczygielski, 1967a,b; Berka, 1986). For example, von Hohberg (1687) mused that the rearing methods of the common carp in his time were superior to those used by the Romans who would surely have enjoyed the taste of their contemporary carp. Dubravius (1547) also frequently mentions the Romans in relation to the common carp, but Richard Hoffmann (personal communication) spoiled the fun declaring that "these remarks are more likely a contemporary literary fashion to quote Latin sources than knowledge of the Roman carp culture" (Balon, 1995b: 30). What a pity!
The "golden age" of pond construction for rearing the common carp reappeared when the wars and skirmishes of the fifteenth century had ended. It has been estimated that more than 25,000 carp ponds were built towards the end of the fifteenth century and at the beginning of the sixteenth century in Bohemia and Moravia alone. A special guild of mobile and rogue pond builders flourished. During these 50 years, about 500 ponds per year, i.e., two ponds per day, were constructed (Andreska, 1987). Production of the common carp for food became the most profitable branch of agriculture (Andreska, 1997; Guziur et al., 2003). Various wars and a decline in the price of common carp later led to a dramatic reduction in the number and area of these ponds from a total of 180 000 ha to about 51 000 ha. At 711 ha, Rozemberg pond, which was built in the sixteenth century, one of the 34 largest, still operates on the two to three year cycle of carp production (Kourzil and Guziur, 2004).
Already Dubravius (1547) recommended a system of several specialized ponds for the production of marketable common carp. The smallest of these was the spawning pond with a grassy bottom simulating shallow, freshly flooded meadows into which groups of selected parent fish were released. Soon after spawning, the early juveniles (Balon, 1999) were flushed into nursery ponds at a lower level, then one year later into growing ponds. In some years ponds were left dry in rotation, treated with lime and various chemical and natural fertilizers in order to enhance the carp's food production. Some consider that T. Dubisch, the illiterate Slovak fish master (Morcinek, 1909), invented the system of transferring common carp from one growing pond to the next, while gradually lowering their densities (Billard, 1999; Guziur et al., 2003). While the production of young carp in spawning ponds was recommended for every pond system, it was later replaced, at least partly, by the artificial stripping of gametes under hatchery conditions (Woynarovich, 1962; Billard et al., 1995). The growth of the common carp was enhanced by ever better formulations of supplementary food, the system of sequential, specially fertilized ponds remained. Production increased from 40 to more than 450 kg per ha (Citek et al., 1998), with the growth cycle of marketable common carp reduced from 5-6 to 2-4 years (Fig. 8, 9, 10, 11).
[FIGURES 8-11 OMITTED]
Sooner or later different forms of domestic common carp appeared in the various pond systems. When the wild common carp was introduced into a pond system its torpedo-shaped body naturally started to change to a deep, laterally compressed, hunchbacked body. Soon individuals appeared with no regular, geometrical arrangement of scales. Instead scale arrangements were severely irregular, and scales were reduced or even absent. These variations soon became a source for artificial selection. Ultimately, the domesticated common carp are represented by a variety of forms, such as scaled carp, line carp, mirror carp, and leather or naked carp (e.g., Brylinska, 1986; Pokorny et al., 1995; Gorda et al., 1995).
Comparisons of wild and domesticated common carp: The domesticated common carp underwent internal and physiological changes as well as changes in its external shape, scalation and color. Detailed reviews were published elsewhere by Balon (1974, 1995a,b) and Barus et al. (2002). A brief summary will suffice here: The mouth gape, the first character that Rudzinski (1961) and Steffens (1964) used for clear distinction between the wild and the domesticated common carp, was much smaller in the wild than in domesticates (Table III). "Even more pronounced differences are encountered among the mouth-gape indices calculated by dividing 10 times the mouth gape in square centimeters by the length of the head in cm--4.46 to 5.57 for the wild common carp and 8.12 for domesticates" (Steffens, 1964). Both authors considered the enlargement of the mouth in domesticates to be caused by changes in diet, and possibly the result of artificial selection. Domesticated common carp selected to utilize supplementary food, grew better in ponds when man-made food was added (see Sibbing, 1988). Studies on wild common carp in ponds (Rudzinski, 1961; Leszczynska and Biniakowski, 1967) clearly proved that wild common carp progeny were better suited for stocking natural riverine habitats than were domesticates.
Rudzinski (1961) found and Steffens (1964) confirmed that the intestine of the wild common carp was 15 to 25% shorter than that of a domesticated carp. The index calculated by dividing the length of the intestine by standard length in centimeters was 2.11 for the wild common carp and 2.64 for the domesticates. Longer intestines in domesticates are likely due to utilization of vegetable food not normally consumed by wild common carp. Both authors also found, when comparing the deeper body of the domesticates with the cylindrical one of the wild common carp, that the calculated muscle mass was the same in both, although it appears to be more in the domesticated fish. It means that dressed mass of domesticates is not larger in spite of the different body proportions. Also, both chambers of the swimbladder of the wild common carp are of similar size, whereas in the domesticate the anterior chamber is always much larger and the posterior chamber smaller; the proportion in percent as given by Steffens (1980) is 61:39 for the wild and 90:10 for the domesticate. This may relate to the relative greater mass of the head in domesticated common carp.
The greater strength of the wild common carp was supported by some of the physiological attributes (Steffens, 1964). The wild common carp had 18 to 19% more erythrocytes and hemoglobin than did the domesticate; blood sugar level was 16 to 26% higher in the former. Also, the wild common carp had a much lower water content in muscles and liver than did the domesticate. Furthermore, the wild common carp had greater fat content in individual organs, more glycogen in the liver, and more vitamin A in the eyes, intestine, and liver. In addition its muscles were more vascularized and did not tire as quickly as those of the domesticate. As in some exploited captive salmonids (Balon 1980, 2004), there are some indications that carp domesticates usually produce eggs with less yolk and as a consequence more altricial progeny than the ancestral wild form (Kryzhanovsky et al., 1951; Balon, 1958a; Penaz, 1995). This aspect will be dealt with in the final section.
As already mentioned, specific forms of the domesticated common carp are created and maintained through constant artificial selection in nearly every individual pond culture system. Standardized breeds were developed and new forms are continually tested in places such as the Fish Culture Research Institute at Szarvas, Hungary, the Institute of Ichthyobiology and Pond Culture of the Polish Academy of Sciences at Golysz, Poland, and at the Research Institute of Fishery and Hydrobiology of the Southern Bohemian University at Vodnany, Czech Republic (e.g., Gorda et al., 1995; Pokorny et al., 1995a,b; Flajshans, 1996; Varadi et al., 2002; Guziur et al., 2003; see also Billard and Gall, 1995). The common carp is considered a delicacy in Europe not only at Christmas, at which the main autumn harvest is aimed (Balon, 1966), but also in special restaurants, for which a professional cookery book with more than 84 recipes for domesticated common carp dishes was written around 1927 (Vanha, 1993).
The emergence of ornamental "nishikigoi": The common carp was traditionally reared for human food in small terrace ponds alternating with rice paddies between the cities of Nagaoka and Ojiya in the Niigata Prefecture facing the sea of Japan, some 280 km west of Tokyo. The area is reputed to have one of the highest snowfalls in the world; for about six months of the winter the whole area is under at least six meters of snow. These unusual conditions may have contributed to the frequent occurrence of color aberrations in the common carp cultured here. The high incidence of color aberrations may be caused by melatonin production during life in total darkness under the cover of deep snow.
This mountainous area had only few roads in the past and the local farmers were often stranded for many long winter months. It is assumed that selection and cross-breeding of the colored aberrants of the common carp began here 180 years ago (Kataoka, 1989; Kuroki, 1990). There is, however, little evidence to support the appearance of these early "nishikigoi". Plate 16 in volume one of Illustrations of Japanese Aquatic Plants and Animals, published in 1931, shows some colored carp (Fig. 12) but no modern "nishikigoi" (Ishikawa et al., 1931; Balon, 1995b). Consequently, while the appearance of the colored common carp more than 70 years ago is documented (Fig. 13), selection of the true "nishikigoi" (koi for short) probably started on a commercial scale only after the Second World War, in the 1950s. By then improved living standards in Japan and elsewhere allowed more people to afford garden ponds. These garden ponds were fully exploited for decoration with "swimming flowers" particularly in Japan, where land is more precious than in many other parts of the world and where Buddhism encourages a love of animals. The ponds were a logical progression in the development of the miniature garden. At time when the koi began to enjoy international popularity, Amano (1968: 36) wrote that "the number produced in a year is ten million, amounting to 1,000,000,000 yen worth".
[FIGURES 12-13 OMITTED]
The koi, as they are known today (Axelrod et al., 1996) are color aberrations of the common carp, Cyprinus carpio. They probably originated from the domesticated common carp or its feral forms, and from some more recent imports from Europe (doitsu koi). When the color aberrations started to appear more frequently and demands for them increased, production and crossbreeding intensified and their progeny started to be severely culled, leaving only the best colored--1 out of 10 000 or more--for future breeding. The first modern "nishikigoi" come from the 30 hamlets of Yamakoshi united in 1956 in the Niigata Prefecture (Fig. 14) where "87 per cent of the 906 families [are] being fancy carp producers" (Amano, 1971: 37). The beauty of the wild common carp was reinstated here in color, not unlike that of rabbit, chicken or cattle long time ago.
[FIGURE 14 OMITTED]
Today, the Japanese recognize about 15 basic color aberrants of the common carp called koi, each of these aberrants with many varieties (e.g., Phipps, 1989; Kuroki, 1990; and the Nishiki Goi monthly magazine). The standard is the carp body to remain cylindrical and the colors to be viewed from above. The introduction of koi with elongated fins and scale or body deformation is not accepted in Japan but appears frequently from producers in Israel and elsewhere. Even by most careful crossbreeding and parent selection the resultant colors of the severely culled offspring are impossible to predict (Kataoka, 1989) by genecentric ideology (Ho, 1999; Hall et al., 2004). After several cullings only the most promising and appealing colors are retained. "Out of these [enthuses Balon, 1995b: 41-42] grow numerous beautiful nishikigoi, but the winners of shows are but a few unique individuals selected from many hundreds of thousands. In Japan the favorites are the kohaku--the red and white koi, taisho-sanke--red, black and white, and the showa sanshoku--a black koi with white and red imposed (...). As no two specimens are ever alike, the grand champions of modern shows commonly sell for US $ 150 000 or more, others often for more than a million dollars each. These must be the highest prices paid for an individual fish!" Finally, it has been found that koi grow better if allowed to listen to violin music for three hours per day (Vasantha et al., 2003). Expensive music lovers!
The "chi" into goldfish, Carassius auratus
When preliminary studies in 1968 and 1969 indicated that goldfish tended to forget things when drunk, and that Siamese Fighting Fish became more aggressive after a little drink or two, their attraction as experimental animals became irresistible.
William Hartston (1987: 7) in The Drunken Goldfish
"Of all the favourite species [informs Taylor, 1884: 58] the goldfish has long been most domesticated, so that now, like the canary among birds, it seems to be better adapted to confinement than even to a free roving life." It has also been an animal of choice for laboratory experimenting in physiology (e.g., Ostrander, 2000). (2) In spite of all this it is often confused with the crucian carp, Prussian carp or even the common carp (Szczerbowski and Szczerbowski, 1996).
There is no reason to confuse the chi or goldfish with carp for goldfish, unlike common carp, have no barbels. The crucian carp, Carassius carassius (Linnaeus, 1758) differs from the goldfish by (a) having 23 to 33 gill rakers on the first branchial arch while wild goldfish have 37 to 53, (b) having 28 to 29 fine denticles on the posterior edge of the last unbranched spiny ray of the dorsal fin while goldfish have 10 to 11 irregular denticles, (c) by having a light peritoneum while goldfish have a black peritoneum, (d) by having the upper edge of the dorsal fin raised while in goldfish it is concave, and (e) by having a blackish spot at the base of the caudal fin while goldfish have none. Body color of the crucian carp is usually coppery gold while that of the chi, the wild goldfish, is silvery-grey (Fig. 15). In spite of these differences, most FAO statistics erroneously list goldfish, Carassius auratus auratus (Linnaeus, 1758), as crucian carp, but crucian carp, C. carassius, is rarely used in aquaculture and is quite infrequent. The same mistake can be found in some aquarium literature (e.g., Matsui and Axelrod, 1991; Wang et al., 2000), and even in the newest encyclopedia (Liu, 2003) although in the first edition all was again correct and more informative (Grzimek and Ladiges, 1973).
[FIGURE 15 OMITTED]
The crucian carp, C. carassius, occurs in two morphs: the precocial, fast growing and deep bodied and the altricial, dwarfed morpha humilis (see fig. 15 and 16 in Szczerbowski and Szczerbowski, 1996, 2002). The fish occurs in most of Eurasia, except in the northwestern and southwestern parts of Europe, and except in China, Korea and Japan. At many locations it was replaced by the expanding Prussian carp, Carassius auratus gibelio (Bloch, 1783), that Kottelat (1997) recognized as a separate species, C. gibelio. The Prussian carp, silverish in color, is mostly a gynogenetic, all female, triploid subspecies (Pelz, 1987; Halacka and Luskova, 2000) that lives in the peripheral areas of the distribution of the nominal chi or wild goldfish, C. auratus auratus. The latter subspecies occurs with both sexes present. The wild goldfish is native to China, and some adjacent areas. It was introduced to Japan from China between 1502 and 1620 probably already as monstrositas (Matsui, 1934). "Available data show that at least five genetically and morphologically distinct stocks are known in Japan which are considered as distinct species or subspecies [writes Kottelat, 1997: 52, and after saying that] the systematics of the genus Carassius in East Asia is confusing" (see also Hensel, 1971; Kawanabe and Mixuno, 1989).
All three most common Carassius species--the crucian carp, chi or goldfish and Prussian carp reach only an average size of about 35 cm and a body mass of 1 kg, usually much less. The crucian carp and goldfish were already distinguished during the Sung Dynasty after 968 AD, claims Szczerbowski (2002: 14), but since these two species do not naturally occur in sympatry this claim may be without foundation. Anyway, the goldfish, C. auratus auratus, was introduced to Europe and elsewhere from China already as a domesticated monstrosity. "Valenciennes (1842: 108) summarised the history of the introduction of Carassius auratus to Europe [writes Kottelat, 1997: 52]. He states that some authors (but does not say which) consider that it was introduced to Europe as early as 1611 or 1691 and that Yarrell reports that it had been introduced by the Portuguese from Java (...) to South Africa and from there to Lisboa. The first introduction to England dates to 1691 (Pennant, 1812: 490) and to France to 1755 (Hervey & Hems, 1968 ...). It was bred in northern Europe for the first time in Holland in 1728 according to Sterba (1987: 272)." Before this last date domesticated goldfish had to come by boat from China and, therefore, must have been very expensive. As such their owners would guard them from release into natural waters. The invasions from aquaria and garden pools into all suitable habitats around the world came later.
In the Purnel's Encyclopedia of Animal Life (1968: 918) the following statement reveals all: "The more fancy breeds of goldfish are freaks, no matter how attractive some of them may look. To recite their names is enough to make this point: veiltail, eggfish, telescope, calico, celestial, lionhead, tumbler, comet or meteor and pearl scale. There are also the water bubble eye, blue fish, brown fish, brocade, pompon and fantail and many others. Some breeds are monstrosities rather than freaks." There is a Japanese version of calico oranda called azuma nishiki, the modern usage and depiction of most monstrosities to be found especially in Li (1988), Wang et al. (2000) or in Johnson and Hess (2004) and within the Internet, e.g. www.goldfishconnection.com.
Wild "chi", the ancestor of the domesticated color aberrations and monstrosities
The wild "chi", Carassius auratus auratus, has a deep body, silver-grey or olive-green coloration and thick caudal peduncle (Fig. 15). Large cycloid scales cover the body, and the upper edge of the dorsal fin is slightly concave. Its feral forms are mostly slimmer and smaller, much like the altricial morpha humilis common in the crucian carp. However, the low, round body form is also common in the wild ancestor of goldfish, in the silver-grey catches for food by Chinese fishermen. Szczerbowski (2002: 5) gives as the sole distinguishing meristic character between C. auratus auratus and C. auratus gibelio the lateral line pore counts: 21 to 36 for the former and 27 to 35 for C. a. gibelio. Out of the 25 wild chi captured in the River Li waters at Yangshuo I handled on 15 April 2005, lateral line pores ranged from 27 to 31 (mean 40.3).
Gynogenetic forms are not found in the goldfish. Originally, the number of chromosomes was reported to be 94 (2n) in the goldfish (Makino, 1939), and bisexual populations of the Prussian carp (Cherfas, 1966). In Vasilyev's (1985) review, however, goldfish ended up with 100 (2n) chromosomes and in Chiarelli et al. (1969) with 104 (2n) chromosomes. The triploid forms that reproduce by gynogenesis have 141 to 160 (3n) chromosomes (Penaz et al., 1979). The goldfish is the only cyprinid that has morphologically differentiated sex chromosomes (Szczerbowski, 2002).
The goldfish is a portional spawner and releases two to three batches of eggs in each season at 8 to 10 day intervals. It deposits the adhesive eggs on grass blades and fine willow-like roots at water temperatures 18-19[degrees] C, very much like the common carp. Activated eggs of the goldfish are spherical or slightly oblong, 1.05 by 1.14 mm, transparent with a pale yellow or greyish-green tint. The embryos hatch 3 to 8 mm long, still with a large yolksac and hang onto plants shortly before swimming and seeking exogenous food (Battle, 1940; Mansueti and Hardy, 1967).
The chi, wild ancestor of goldfish, is native to lateral-level waters of rivers and lakes of East and Central Asia, with the center of distribution in China (e.g., Chen and Fang, 1999). From escaped domesticated forms and deliberate releases the goldfish has acquired global distribution in temperate and subtropical areas, naturalized, feral "populations developing in more than 20 European countries (...). Outside of Europe, the goldfish has been introduced to South Africa, and to Madagascar and Mauritius, and is widespread in Asia. It was introduced in 1874 to North America (3) (...), to Oceania, and from 1856 to 1930, to various countries in South and Central America and the Caribbean (...). A slightly earlier date for North American introduction is given by Fuller et al. (1999).
In some localities, it occurs in sufficient abundance to be marketed as a food fish" (Szczerbowski, 2002: 20).
The goldfish is one of the most resistant fish to natural environmental perturbations and man-made pollutants. It tolerates a wide temperature range and high water turbidity. It is the only fish that survives in shallow lakes with total oxygen depletion during some years or seasons (e.g., 0.6 mg l-1 O2). The goldfish survives within a pH range of 4.5 to 10.5, but prefers the optimal range of pH 7.2 to 8.4. In water at pH 4.5 it can survive about two weeks. The goldfish is more tolerant than any other fishes to heavy metals or organochlorine insecticides (Szczerbowski, 2002).
The goldfish has been less successful than the common carp in establishing itself in larger water bodies, but does best in small shallow lakes heavily overgrown by aquatic plants. It also grows to much smaller sizes than a common carp. "Females generally grow larger and live longer than males [writes Moyle, 2002: 171 about this fish in California]. As a result the male: female sex ratio changes from 1 : 1 in small fish to 13-16 : 100 in fish measuring more than 15 cm total length. Although fish in the wild rarely live longer than 6-8 years, maximum ages of 30 years have been recorded in aquaria." For example, in 1967 or 1968, goldfish were introduced into Killarbey Lake in New Brunswick, Canada. Only seven years later, in 1974, they yielded 43% of the feral bronze and 57% of variously colored fish. The largest of them measured 34 cm, weighed 1 kg and was 8 years old, having matured at age 2 (Hooper and Gilbert, 1978).
The history of goldfish domestication
We may consider ourselves lucky that some 30 years after his detailed studies on goldfish Shisan Chen (1956)(4) of the Academia Sinica and Beijing University decided to review the history of domestication of the chi once more, in spite of a changed political climate. Since Ting-pong Koh's (1934) study on that topic, Chen had amassed additional evidence on the history of domestication of the goldfish. Now "forced" to insert a page where among other "timely" claims he writes: "In the light of Michurin principles the writer reexamines his past labours and discovers many errors and shortcomings, which may be grouped under the following three headings (...)" (Chen, 1956: 288). None of these are relevant. He managed to publish the English version of his study (first published in Chinese 1954) ten years before the rampages of the Red Guards (see e.g. Wong, 1996; Chang, 2003).
The goldfish was created as ornamental fish domesticate in China. Sometimes a xanthic aberration would appear, as is the case in many other fishes (e.g., Balon and Frank, 1953; Balon, 1964), among the silver-grey chi, the most common food fish in China (Fig. 16). These red or yellow aberrations are common but only a few reach fishermen because most of them would be eliminated in nature because of their conspicuous appearance. "People in the old society attached a supernatural significance to the appearance of the wild golden chi and regarded them as sacrosanct (...). But there were places, like the Ninghai District (H.4), where they served as food" (Chen, 1956: 292) (5).
[FIGURE 16 OMITTED]
Buddhism teaches abstinence from taking the life of any creature and urges one to do at least one good deed per day. Setting free a rare golden chi must have been thought a better deed than releasing a common animal. Hence, ever "since the beginning of the Sung Dynasty when Governor Ting Yen-tsan of the Duchy of Wu-yueh discovered golden and yellow chi in a pond outside the city of Kiahsing, that pond came to be called 'Goldfish Pond'. Subsequently, the pond became a pond of mercy. In the goldfish pond were other varieties of fish and turtles besides the golden chi, which were forbidden to catch" (Chen, 1956: 294). Other such ponds followed at the pagodas in Hangzhow and Nanking where the goldfish were cared for by the local monks. The records thus document the beginning of goldfish accumulation in ponds of mercy at the outset of Sung Dynasty, between 968 and 975 AD. However, until at least the year 1089 the goldfish were not different from the wild chi except for color, were afraid of humans and did not take food thrown to them. They were captives exploited for religious purposes.
The documents reviewed by Chen (1956: 299), the Bedside Companion (1214), On Names (1241) and Dreams of the Past (1247) "explain the fact that the fad of the ruling class of the time brought a special, fish-breeding trade called yu-er-huo. These breeders learned to feed the goldfish with a kind of red animalcula (...) found in putrid water [tubifex worms?] and discovered the secrets of propagating goldfish so as to enable them to offer a selection of rare varieties of goldfish to gods on festival days." By the year 1241 the goldfish had become tamed and used to the food offered by humans. While in the ponds of mercy, goldfish lived among the common chi, other fishes and turtles, the private ponds constructed by the rich now contained only xanthic goldfish. It was, therefore, easier to breed them, cross the preferred individuals, and for the first time produce the golden yellow, silver white, and the variegation of black and white (tortoiseshell) goldfish. This initial domestication began "around the year 1163 in the goldfish pond of the Te Shou Palace, east of Hsin Kung Chiao in the city of Hangchow" (Chen, 1956: 299).
In general, ponds and garden pools were affordable only to landowners. The goldfish, now in several color forms, were first kept only by royalty and rich mandarins who constructed more ponds, or rather garden pools, for their keeping and breeding. In 1330 during the Yuan Dynasty, the goldfish were brought to Beijing and later (1506-1521) in large numbers outside the Forbidden City. At that time they were also introduced to Japan.
Chen (1956) marks the transition from pools to aquarium-like vessels from 1276 to 1546. Besides the jade vessels and fancy bowls for keeping goldfish, earthen vessels became common and affordable to everyone (Fig. 17). After 1548, rich and poor alike became keepers and breeders of fancy domesticated goldfish, and the beginning of the aquarium hobby for the masses started.
[FIGURE 17 OMITTED]
"Kwei Yu-kuang (1506-1571), a noted man of letters in the Ming Dynasty, wrote a long poem on 'fire fish':
Kept in water, of no ancient line, The fire fish does in new-styled fashion shine. A perfect marvel of few inches' size, It has the brilliance of the rainbow's dyes, . . . The narrow compass of the vat they take With equanimity as stream and lake . . . The children shout at them in unison, And all day play about the vats for fun . . . This fish in every coastal home being bred, Often has to inland Kiangsu spread." (Chen, op.cit.: 302).
Later the "fire fish" was renamed the "cinnabar fish". In the woodcut edition of Sketches of Scenes in the Imperial Capital by Liu and Yu (1634) many goldfish monstrosities are named and described.
So it seems obvious that the creation of monstrosities in shape (Fig. 18) in addition to already bred color aberrations was closely related to the keeping of indoor aquaria--a very popular hobby after the year 1548. The goldfish became the pet of the masses, a popular pastime in every home and everywhere (claims Li, 1596 in another woodcut edition of Materia Medica). The aquarium culture enabled close observation and selection of the individual fish, something hardly possible in garden pools. In addition to presenting lists of many color varieties in A Handbook on the Cinnabar Fish Chien-te Chang (1596) says: "The beauty of the cinnabar fish lies not only in their extraordinary brilliance of color, but also in their tails, patterns, and bodily form, which distinguish them from the common fish. Whether long or short, the body must have the beauty of plumpness as a primary qualification" (Chen, 1956: 305).
[FIGURE 18 OMITTED]
Selected pairs of the domesticated goldfish three to four years old started to reproduce on aquatic plants in aquaria. After mating and deposition of gametes, the parent fish had to be removed from the tank as quickly as possible, otherwise they would have eaten the eggs. Eggs, embryos and larvae incubated in such aquaria were exposed to numerous and various biological, physical and chemical stresses. These caused epigenetic alterations in their ontogenies, some of which led to the development of new monsters that survived longer thanks to human care. Ultimately, through artificial selection some of these monstrosities underwent genetic assimilation and became more or less inheritable (e.g. Ryder, 1893; Balon, 1990, 2002). (6)
Unintentional artificial selection and crossbreeding played an enormous role in the production of more and more bizarre individuals. For example, most of the future red goldfish appear black when young, so severe culling had to be carried out several times in succession to raise a few "ornamental" individuals.
"So, in the short space of 97 years [stated Chen, 1956: 306] between 1547 and 1643 (the end of the Ming Dynasty) not only did more new varieties make their appearance but the degree of variation also became very great." Varieties such as golden helmet, golden saddle, stork's pearl, brocaded back, seven stars, red head-and-tail, purple eyes, snow eyes, the three tails, four tail, nine tail, bulging eyes, the bicaudal, and the dragon eye--a small selection from Shisan Chen's elegant translation--have became quite common. The double tail was first mentioned in 1579 (Linnaeus later described this variety of goldfish as typical Cyprinus auratus) and the dragon eye in 1592; by 1596 the short body was already in existence, the dragon back without the dorsal fin appeared by 1726, and the duck's-egg fish by 1780 (Chen, 1956). By the year 1848 goldfish breeders in China were already using deliberate artificial selection and obtained lion-head (Fig. 18), goose-head, and narial bouquet goldfish (Fig. 19). (7)
[FIGURE 19 OMITTED]
"Today, according to a Japanese newspaper article [claim Grzimek & Ladiges, 1973: 349], the region of Koriyama alone has 12-14 million goldfish in breeders' tanks. Asian goldfish breeders are concerned with varieties completely different from those which can be bought in pet shops for a small amount of money in Europe. They breed just the rare and expensive varieties. (...) European common goldfish are bred by the hundreds of thousands in Italy (...). In England there are goldfish breeding clubs which have large annual exhibitions. Two English goldfish hobbyists, Hervey and Hems , have written a substantial book about these Chinese fish, filled with fascinating details about them. The title picture is a colored reproduction of an oil painting of a goldfish, by former Prime Minister Winston Churchill." In present China 310 basic varieties of goldfish are recognized (Wang et al., 2000: 200-210).
Are there any other domesticated fishes?
It took centuries to still the fear in some pliable animals--Domestication it's called--but most cannot get over their fear, and I doubt they ever will. Yann Martel (2002: 329) in Life of Pi
There has never been a good reason to treat fishes differently from other animals with respect to domestication, although "fish culturists" are often tempted to do so (e.g., Kim et al., 2004). Therefore Cervus elaphus the wapiti deer, that have recently become so popular and are kept fenced-in on farms should be categorized in the same as, for example, a sturgeon species kept in artificial ponds (Fig. 20). There is no reason to classify the former as an exploited captive and the latter as cultured fish. As yet none of them is a domesticate, like cattle or common carp, according to the criteria given in the Introduction.
[FIGURE 20 OMITTED]
While some (e.g., Hemmer, 1990) consider only mammals as domestic animals--a habit common among veterinarians--it is time to treat fishes as animals. The number of fish species in aquaculture has rapidly increased during the last few decades--some are "cultured" as food fishes, others to be stocked into the wild, to be used as bait, or for the home aquarium hobby. Commercial fish farming is for profit, subsistence fish farming maybe less so, but in both instances the enhanced production of fishes is the goal. "The vast majority of freshwater fishes under aquaculture conditions are raised in ponds, though various other types of culture systems are also employed in specialized instances" (Stickney, 1986: 3). The bottom line is that in each such culture system both exploited captives and/or domesticates can be produced.
Most fishes in culture are still only exploited captives and just a few are on the threshold of becoming domesticates, most of the latter for the aquarium hobby. Juliet Clutton-Brock (1999) distinguished between domesticates like dogs, cattle, sheep, swine and goats, and exploited captives such as cats, elephants, camels, llamas, reindeer, yaks and water buffaloes. Maybe this list will help in classifying captive fishes, but let us not argue about terms.
The best-known example is a little viviparous poeciliid named guppy, Poecilia reticulata Peters, 1859. Their males attain 3 and the females about 5 cm length. They originate from Trinidad and Venezuela but were released worldwide for mosquito control. Populations now live in Africa, India, North America, Italy, and even in the warm springs of Hungary and Slovakia. The wild forms are smaller than the domesticates. When first collected in Trinidad this fish was found in streams on an estate owned by Robert Guppy, hence its vernacular name (E. C. Amoroso, personal communication).
The coloration of wild guppies varies according to the habitat and many populations of different color have been described (Frank, 2002). Endler (1980) explained why the males are much smaller than females, also the color polymorphism in Poecilia reticulata. "Natural populations in Trinidad and north-eastern Venezuela are so polymorphic that no two males are alike (...). The color patterns in a particular population represent a balance between selection for crypsis by predators and selection for conspicuousness by sexual selection" (Endler, 1983: 176). "Melanin spots (black) are voluntarily increased in size during courtship, but reduced in size and intensity at other times. Carotenoid spots (red, orange and yellow) genetically decrease in size and frequency with increased predation (...) and may be direct indicators of male physical fitness ..." (Ibid: 186), claimed this fanatical Darwinist (but see Balon, 2004b).
This predisposition to color variation facilitated artificial selection in captivity where the variety of form and color far exceeds that found in nature. Furthermore, guppies were bred with short fins, long fins and with the natural olive-grey color replaced by another color. Because of inbreeding the short-fin morphs had to be severely culled to avoid vertebral deformities or stunted growth. In guppies, form was simply sacrificed for color, although not as far as in goldfish. The long-finned fish have problems with mating; the males have difficulty inserting the gonopodium and transferring spermatophores. Some breeders anaesthetize the females "to give the males a chance to inseminate them" (Wischnath, 1993: 273). The various color forms are then crossbred, but in some, where both sexes have elongated fins, only artificial insemination enables reproduction. There are standard breeds such as triangle (triangular caudal fin), fantail, veiltail, bannertail, lyretail, topsword, bottomsword, doublesword, speartail, roundtail and spadetail. None of the long-tailed and most colorful fish would survive in the wild and therefore can be considered true domesticates.
Other livebearers common in the aquarium hobby are the swordtails and platies of the genus Xiphophorus, including some 17 species from Central America. Swordtail males have the lower caudal fin rays elongated to various lengths, and the platies have none. Most of the morphs in aquaria have resulted from hybridization and the artificial selection of three species: Xiphophorus helleri Heckel, 1848, Xiphophorus maculatus (Gunther, 1866), and Xiphophorus variatus (Meek, 1904). Natural hybrids are observed only rarely because the different species rarely live in sympatry or are separated in the wild by behavior. Consequently, we must ask if these artificial hybrids are really domesticates? The same applies to the fancy mollies of the genus Poecilia (formerly Mollienesia). The popular black molly was obtained by crossing various Poecilia sphenops and P. latipinna, then P. petenensis was introduced into the cross for the black Yucatan molly. Crossing further with P. velifera, the high-finned molly appeared. "The progenies of wild specimens bred in captivity greatly resemble their parents. The first apparent differences are usually in size. The appearance and behavior of bred captives often remains like that of their ancestors for years. (...) The genera Xiphophorus and Poecilia are among those very variable fishes, even in the wild, that develop many regional and color variants" (Wischnath, 1993: 322). For example, breeders in Singapore are flooding the market with numerous color aberrants. Are these fishes domesticated or just hybrids bred in captivity?
Let us look at it from the view of the most popular fish in the aquarium trade, the neon tetra, Paracheirodon innesi (Myers, 1936). Discovered by chance in one of the Amazon tributaries near the border between Peru and Colombia, some of the small fish reached Paris and then the Hamburg aquarium for $ 500 each, a fortune at that time. Finally the Shedd Aquarium in Chicago acquired five of them for its new exhibition. These fish travelled from Ludwigshafen, Germany, to Lakehurst, New Jersey, on the dirigible airship "Hindenburg" which crashed a short time later. Initially it seemed impossible to breed these fish in captivity; but once this was achieved in the 1950s the species became the most popular aquarium fish of all. Not long after, the neon tetra became domesticated by selection for a long fin (Fig. 21) as well as for golden, diamond head, albino and xanthic morphs and aberrations (Elias, 2003).
[FIGURE 21 OMITTED]
There is little doubt concerning the cichlid fishes from Amazonia, the discus. Selection of some color aberrations formed the basis of many aquarium forms. The majority, however, were achieved by the hybridization of two known species--Symphysodon discus Heckel, 1840, and S. aequifasciatus Pellegrin, 1904, with some contribution from the questionable subspecies S. discus willischwartzi Burgess, 1981, S. aequifasciatus axelrodi Schultz, 1960 and S. aequifasciatus haraldi Schultz, 1960. Each occurs in the wild in many color varieties, especially the green discus, S. aequifasciatus (Degen, 1995).
These cichlids are unique in having a strongly laterally compressed discoidal shape, similar to the marine butterflyfishes of the genus Chaetodon. Approximately the size of a human hand, S. aequifasciatus, which is widespread in the Amazon region from Belem to Peru, has 50 to 61 vertical scale rows from the head to the caudal fin, while S. discus, endemic to the Rio Negro, has 44 to 48. This classification, however, may change at any time (Burgess, 1991). The question now remains whether the color variations of discus, achieved mainly by crossing specimens from various taxa and localities, are simply to be designated as hybrids rather than domesticates. The same question applies to the other cichlid genus of Amazonia, the angelfishes Pterophyllum with three valid species P. leopoldi, P. scalare and P. altum.
So far, the answer to the question posed at the beginning of this section is that in modern aquarium culture, probably only guppies and vaguely neon tetras can be considered domesticates. The zebra fish, Danio rerio (Hamilton, 1822), rushed lately to follow medaka, Oryzias latipes (Temminck & Schlegel, 1846) as research model (Yamamoto, 1975), however, may soon be a true domesticate (see the new journal "Zebrafish"). Other taxa are exploited captives as hybrids and color aberrations in unstable breeding systems with a constant addition of wild conspecifics.
What about fishes in aquaculture for human food, such as the rainbow trout, Oncorhynchus mykiss (but see Behnke, 2002), and the channel catfish, Ictalurus punctatus? Apart from separate hatchery strains, no true domesticated forms are really known except for the color aberrations of rainbow trout (Fig. 22) developed by Krysztof Goryczko at Rutki, Poland (Goryczko and Dobosz, 2004). The same is true for the other artificially propagated and cultured fishes like the Chinese and Indian grass carp, silver carp, bighead carp, catla, rohn, mrigal and colbasu, as well as the salmon, tilapia, bass, zander or walleye, tench, wels, walking catfish, or sturgeon. At this time all are exploited captives with some potential for future domestication.
[FIGURE 22 OMITTED]
Origin of alternative phenotypes
I have more respect for people who change their views after acquiring new information than for those who cling to views they held thirty years ago. Michael Crichton (2005: 627) in State of Fear
In spite of the prevailing practice derived from lay or thoughtless usage (e.g., Kamler, 2002), the ontogeny of organisms should be realistically described based on the saltatory life-history model of embryo, larva, juvenile, adult and senescent periods (e.g., Balon, 1985, 1986, 1999, 2004b), each period separated by natural boundaries. In comparative studies, such a model provides the possibility of recognizing and interpreting shifts in boundaries, which often result in a new life-history style (e.g., Hall, 1984; Bruton, 1989). It elucidates, for example, the ecological significance of not having a larva (Balon, 1977a, 1984b; Matsuda, 1987; Flegler-Balon, 1989) as well as the importance of having a larva despite the cost of metamorphosis (Balon, 1978, 1979, 1984, 1985).
The embryo period of ontogeny is characterized by primarily endogenous feeding, i.e., by the acquisition of nutrients from parental sources. The transition to the oral ingestion of exogenous nutrients and intestinal digestion, i.e., the acquisition of nutrients from the external environment, marks the beginning of the next period of life history, be it a larva period in the case of indirect ontogeny, or a juvenile period in the case of direct ontogeny (Fig. 23).
[FIGURE 23 OMITTED]
Larvae are, in general, more vulnerable than any other life-history stages. Eggs with small, low-density yolks (see Crawford et al., 1999), however, can be produced in larger quantities to compensate for the high mortality of larvae. Being chiefly nutrient-gathering entities, larvae are designed to compensate for the insufficient yolk before a definitive phenotype can be formed. Besides high mortality there is another price to be paid for having a larva period. Numerous cenogenetic (temporary) structures of larvae, specialized for separate habitats and niches, need to be remodeled into permanent organs and shapes at some energy cost. This process of remodelling--metamorphosis--terminates the larva period (e.g., Fostner et al., 1983; Matsuda, 1987). In some cases (e.g., non-parasitic lampreys, elopomorphs, stomatioids) much of the size gained during the larva period must be sacrificed in the remodeling process, thus losing the survival advantage of larger size. This, by the way, provides clear circumstantial evidence that the main purpose of a larva is the acquisition of external nutrients when the endogenous supply is insufficient. In contrast, when sufficient endogenous food is provided at the disadvantage of a lower number of eggs (e.g., Balon, 1984, 1986), elimination of the vulnerable larva period and costly metamorphosis facilitates direct development into a juvenile that is comparatively advanced and often large at the time of its first oral feeding. This is a clear survival advantage. Moreover, fewer larger eggs, greater density of yolk (negative buoyancy), prolonged developments inside the egg envelopes, and sessile stages of embryos even after hatching pave the way to further protection by parental care (Balon, 1975, 1981a,b, 1984; Crawford and Balon, 1996).
It is possible that the increase in vitellogenesis responsible for the larger amount of yolk is mediated by the environment (Gerbilsky, 1956) via endocrine mechanisms (e.g., Campbell and Idler, 1976; Matsuda, 1987). It is likely that the resulting specialization of some individuals in larger, more nutritious food items, may enhance vitellogenesis and produce more precocial progeny (e.g., Goto, 1980, 1982; Balon, 1980, 1985). Even changes in temperature may initiate the epigenetic formation of larger and more specialized individuals (Balon, 1980, 1983, 1985).
The survival of the offspring is enhanced by an increase in the endogenous food supply and parental care (Crawford and Balon, 1996), the evolutionary sequences ranging from scattering of gametes to hiding them, from guarding a clutch on a selected or prepared substratum to bearing a clutch on or inside the parent body (Balon, 1975,1985, 1990). Bearing the offspring internally (i.e., live bearing) further decreases its exposure to predators and avoids some adverse environmental disturbances (e.g., in the case of fishes fluctuations in water level) because the clutch is carried by the mobile parent. The released young are fully differentiated juveniles grown exclusively on an endogenous food supply. Elimination of the larva period from the life history is, therefore, an important ecological and evolutionary phenomenon, which deserves more of our recognition and attention (cf. Balon, 1986, 1999; Flegler-Balon, 1989; Smith et al., 1995).
Most importantly, the final form of a phenotype and its life history are determined during early ontogeny at a time when other than purely exogenous types of feeding operate (endogenous, absorptive, mixed) (Fig. 23). Most changes are introduced at that time. An organism should always be considered over its entire ontogeny, from the single cell at activation until death (Balon, 1985). Focusing on the later parts of ontogeny (juvenile, adult or senescent) restricts us to studies of the definitive phenotypes only, while the processes that create this bewildering diversity of forms and functions cannot be explained anymore, the mechanisms not understood (see e.g., Arthur 2004).
Metamorphosis often is a separate special interval (Balon, 1999; Heyland et al., 2004) that ends the larva period and separates it from the juvenile period. As the larva is the vegetative form, required by organisms with eggs and embryos with a low endogenous food supply, so they may develop into adults capable of reproduction, the beginning of the larva period must be the beginning of exogenous (i.e., ingestion and digestion) feeding. In fishes having larvae, this threshold rarely coincides with hatching.
Furthermore, hatching is never a natural threshold but a "process in which the embryo emerges from the egg envelope (or a fertilization envelope) which encloses it. This process is observed not only in the embryos of oviparous animals but also in those of viviparous animals such as mammals" (Yamagami, 1981: 459). Thus, hatching should not be equated with parturition (birth); it is not an instantaneous event but a process that occurs at various times in different individuals and is influenced by stimuli from the internal and external environment (Cunningham and Balon, 1985, 1986a, b; Helvik, 1991; Helvik and Walther, 1992, 1993a, b; Crawford and Balon, 1994a,b,c).
All of us accept our date of birth as a significant point in our lives (emphasized by the importance of birth certificates); rarely do we realize that this date marks an event erroneous for the biological life history. Individuals born prematurely are older on paper than those born at the normal time; yet they are born in a less developed state than those born at the normal time. A similar paradox also applies to the time of hatching. Both hatching time and time of parturition (birth) are impossible to define in terms of "normality" because both are largely influenced by the environment and do not necessarily occur at a particular state and time of development (Balon, 1981a). Moreover, we often believe that hatching and birth (parturition) are equivalent events in oviparous and viviparous animals, respectively. They are not (Hensel, 1999). Therefore, it is erroneous to time ontogeny from parturition in one instance and from hatching in another.
The life-history model was constructed to reflect the natural intervals of different types of ontogenies and to serve as a sort of standard (Fig. 23). Comparing actual ontogenies to this model helps in recognizing heterochronies specific for various types of indirect and direct developments and in determining the deviations from the standard of intermediate life histories.
Altricial and precocial forms
Following the long accepted terminology for birds (e.g., Nice, 1962; Ricklefs, 1979), we have used the term "altricial" to describe the quasi generalists and "precocial" for the quasi specialists. The main attributes of the two forms are: relatively smaller or incompletely developed young in the altricial form, and relatively larger or more completely developed young in the precocial form. In extreme cases, the definitive phenotype of the altricial form is arrived at via the slow differentiation and remodelling (metamorphosis) of temporary nutrient-gathering larvae, whereas the definitive phenotype of the precocial form differentiates directly into a definitive phenotype because the endogenous food supply (yolk, trophodermy, placentotrophy) is sufficient.
Let us briefly return to the consequences of the mechanisms responsible for the creation of alternative states. Every successive reproductive lineage, as a consequence of ever-changing epigenetic variations and relationships, will produce both altricial and precocial forms with more specialized characters compared to the previous generations. For example, the larva period will become shorter and shorter, and the egg number per reproductive lineage will progressively reduce, but the yolk volume and density will increase until a specialized form develops with, for example, semelparous reproduction or one single large offspring (Balon, 2004b, fig. 3 and 4). By this time a very vulnerable existence, on the verge of extinction, is reached. Under special circumstances this trend can be reversed by juvenilization and thus extinction postponed (Balon, 1985).
The intraspecific differences between altricial and precocial forms in ontogeny are usually very small. The quasi generalists will be a little more inclined toward the attributes of altriciality in comparison to the quasi specialists which will be a little more inclined toward the attributes of precociality (Fig. 24). Fitting examples among fishes are the sympatric "dwarf" and "normal" forms of charr, Salvelinus spp. (e.g., Balon, 1980, 1984; Klemetsen et al., 1985), the dwarf Oreochromis mossambicus of Lake Sibaya (e.g., Bruton, 1979, 1980), the altricial Oreochromis shiranus chilwae and precocial O. shiranus shiranus (Lowe-McConnell, 1982), and the appearance of Cichlasoma minckleyi as an altricial papilliform morph and a precocial molariform morph (Liem and Kaufman, 1984).
[FIGURE 24 OMITTED]
Some such intraspecific twin forms have been identified independently as dwarf and large perch Perca fluviatilis (Alm, 1946; Svetovidov and Dorofeyeva, 1963; Oliva et al., 1989), normal and giant tigerfish Hydrocynus vittatus, lake charr and siscowet, Salvelinus namaycush, sea trout Salmo trutta and brown trout Salmo trutta morpha fario, and the deep bodied precocial form of Carassius and dwarfed altricial morph humilis (e.g., Balon, 1977b, 1980). Recognition of such twin forms in a taxon depends to a large extent on the acceptance of the idea and on improved resolution in studies devoted to the life history of a species. Larger differences are evident only when the same concept is applied at species or higher taxon level, considering substrate-nesting cichlids as more altricial than mouth brooders (Balon, 1993).
In most instances, even the simplest variables of early ontogeny are not known. Comparative ontogenies are not available for most species, though the dwarf and normal pairs of charrs are part of the much broader known occurrence of "sibling species" or sympatric "species pairs" reviewed by Taylor (1999). Comparative studies of the early ontogenies in charrs of the genus Salvelinus (Balon 1980) clearly indicated that some females produced smaller eggs than other females, or eggs with denser yolk than others (see Crawford et al., 1999). Incubated separately but under identical conditions, the smaller eggs resulted in more altricial progeny compared with more precocial progeny from larger eggs. When smaller eggs were incubated at two different temperatures (4.4[degrees]C vs. 9.5[degrees]C), the warm incubated progeny was more precocial in comparison to the cold incubated. The same results were obtained with larger eggs.
Alerted to the constantly-appearing dichotomies, a large number of eggs from larger females was followed in detail: again two separate progenies occurred, akin to the previous ones from large and small eggs or two different temperatures (some experiments were reported in Balon 1980 and 1984, some were unpublished). Closer examination revealed that the eggs from each female can be separated into two size groups. Eggs incubated under identical conditions again resulted in separate altricial and precocial progeny. While the differences were very small, all were indicative of the larger differences found in the early ontogeny of several species of charrs from various habitats and even continents.
Portional spawning of some fishes leads to the same effect. As mentioned earlier, common carp and goldfish females release portions of eggs each week or two. By then each portion, with different yolk volume and density develops under different environmental regimes (e.g., temperature, oxygen) resulting in either altricial or precocial progeny.
How does epigenesis of early ontogeny explain the existence of true species pairs? Crawford and Balon (1994c: 371) "compared the morphological development of two closely-related North American killifishes, Lucania parva and Lucania goodei. These species inhabit very different environments, and represent an exceptional 'natural experiment' with which to explore the life-history model described above". At Newport Spring, the site where L. goodei was collected, the conditions were rather stable; the water flowing from an artesian spring showed few diel or seasonal fluctuations. Only 10 km away, the collecting site for L. parva at Tower Pond presented highly unpredictable conditions. It was exposed to sea and fresh water and large diel and seasonal temperature fluctuations. In addition, summer algal blooms caused severe deficits in dissolved oxygen and tides and precipitation caused large changes in salinity and water volume.
Crawford and Balon (1994c: 395) concluded that "the life-history characteristics exhibited by L. goodei can be considered to be more precocial than those of L. parva" (Table IV, Fig. 24). "Adult female L. goodei produced significantly fewer eggs, with significantly more yolk. The offspring of L. goodei developed at more rapid rates than those of L. parva, reaching the definitive (juvenile) phenotype at an earlier age, with lower mortality and with a different body shape". All these differences clearly agreed with the expected differences caused by epigenetic processes ultimately responsible for the true species-pair divergence (explained in detail in Balon, 2002).
Over and above the usually recognized modifications (e.g., Thorpe, 1991, 2004; Huntingford, 2004), captive breeding causes severe endocrineous changes as early as the very beginning of ontogeny. Artificially bred salmonids, for example, often produce eggs with less yolk than their wild ancestors. Hence, the fish developing from these less well-endowed eggs are destined to be more altricial. If such fish are released to grow in ponds, their tendency to mature earlier at smaller sizes is usually compensated for by manipulation of rearing densities and the provision of food. The whole system would benefit from the presence of precocial forms with their tendency to grow longer and mature later. Can this be achieved by selecting for precocial parent fish?
It is commonly believed that cultured fish will grow better and gain more mass when kept at low densities and with an optimal supplementary food regime. This, however, may not be the solution because under these conditions the fish perceive the habitat as sparsely inhabited, like a newly-invaded postglacial water body ready to be colonized, and they will "switch" to an altricial life style best suited to such conditions (Balon, 1985, 1990). If, on the other hand, the fish are crowded at high densities and the habitat is perceived as saturated, some fish will delay maturation and grow for longer to avoid competition, even cannibalising some of the remaining stunted individuals. Thus some precocial giants will emerge from the altricial multitude. Using these large fish as stock for further reproduction will not avoid the stunted altricial alternatives if the low density system is repeated, but should increase the number of precocial desirables. The common solution of adding more food in an attempt to delay early maturation rarely helps because it reinforces the perception that the habitat is still under-utilised and the inhabitants will rush to multiply sooner and faster.
This scenario may only apply to exploited captives, not to true domesticates, because the physiology and morphology of the latter were changed in the domestication process. The domesticated carp, for example, with longer intestines and less haemoglobin may react differently to artificial versus natural food and not respond to densities by balancing altricial ?precocial alternatives. A domesticated fish is also removed from its wild ancestor because of its reaction to environmental changes.
This essay is dedicated to the memory of my father Jozef BaLon and mother Jaromira BaLon for their love and support. I thank historian Rich Hoffmann for his advice and for some archaeological literature, and my wife Christine Flegler-Balon for reading earlier drafts and for her constant support. Thanks are also due for some corrections of style to Robin Welcomme and John Craig, who heavily amputated an earlier version (Balon, 2004c), originally ordered for publication in the Journal of Fish Biology as the introductory J. W. Jones lecture. For this reason it is now published here in full and in layout as originally designed and presented.
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(1) Second edition was published in 1559 probably by demand of Conrad Gessner, third edition appeared in 1596, and in 1599 De Piscinis appeared in English translation (Andreska, 1987).
(2) I have found the most curious use of goldfish in the wonderful autobiography by James Lovelock (2001: 406): "She inserted a live goldfish and, with a flourish and a heave of her powerful vaginal muscles, expelled it into a bowl of water on the other side of the room. She did this several times and missed only once. (...) In the West, such an exhibition might have been criticized as unseemly, but in Japan, it rated as impermanent art."
(3) Innes (1949: 47) states that "marvelous specimens brought to America by Admiral Annon in 1874."
(4) Chinese biologist Chen Zhen (Shisan C. Chen, 1894-1957) began in the 1920s to study the heredity, evolution and variations of goldfish. He published very valuable writings in this realm that have been highly regarded by Chinese and foreign scientists. Under his influence scientists have paid ever more attention to Chinese goldfish" (Li, 1988: 17-18).
(5) Just this once, the evidence discovered by Shisan Chen (H.4): Chen, Chi-ching (122) in The Topography of Chihcheng, woodcut edition of the Sung Family of Linhai in Chia Ching Reign, vol. 25, Ninghai District: "Chuching Pond is forty li west of the city; it winds about the neighbouring hills and has an area of hundreds of acres... It produces gold and silver chi of the most delicious taste. But they are so mysterious that fishing boats approaching them often turn upside down."
(6) "If a strain is carefully watched for several generations and no fish varying from the desired type is allowed to breed, the percentage of young coming true can be kept very high" (Innes, 1949: 74).
(7) The Telescope Goldfish was originated in China and undoubtedly bears a resemblance to Chinese art. It has a sort of beautiful ugliness, a deliberate grotesqueness, intended first to shock and then excite curiosity" (Innes, 1949: 51).
Eugene K. Balon
Department of Integrative Biology, University of Guelph, Guelph, Ontario N1G
Table I. Morphometric characters of 87 individuals from spawning schools of the wild common carp, Cyprinus carpio, in the Slovak parts of the Danube River, collected May 1954 and May 1956 (Misik, 1958), compared to the wild common carp from the Amur River (Gromov, 1973; see also Barus et al., 2002). Measurements Danube range Amur and counts range 1-2 in % of standard length 359-635 mm 518.0 mm 1-3 head length 22.7-26.7 21.6-28.5 1-6 snout length 7.6-10.8 7.6-10.5 6-11 orbit diameter 2.9-3.9 2.6-4.5 7-9 interorbital width 8.9-11.7 7.5-8.5 11-3 postorbital head length 11.2-13.8 8.6-13.5 1-12 predorsal distance 42.1-48.1 43.5-51.5 12-15 body depth 24.6-30.9 26.5-35.5 12-26 body width 13.8-22.0 -- 16-2 caudal peduncle length 18.1-23.2 15.5-20.5 18-19 minimum body depth 11.1-13.6 10.5-13.5 20-13 pectoral origin to pelvic base 20.7-26.4 21.5-25.5 13-14 pelvic base to anal base 27.5-33.1 -- 12-21 base length of dorsal fin 35.8-44.9 35.5-42.5 14-16 base length of anal fin 7.3-10.4 9.0-11.5 20-26 longest pectoral ray length 15.6-20.9 15.5-20.5 13-27 longest pelvic ray length 14.7-19.9 14.5-18.5 12-28 longest dorsal fin ray length 14.0-18.8 10.5-14.5 14-29 longest anal fin ray length 14.3-17.5 10.5-14.5 Table II. Back-calculated mean standard lengths (in mm) for males and females of the wild common carp from the spawning school at the Lesser Danube above Kolarovo. Back-calculated mean SL at the end Mean SL of each growth season Year of Age at time of spawning group capture [l.sub.1] [l.sub.2] [l.sub.3] 1952 males III 422 154 382 410 1951 IV 400 158 298 360 1950 V 428 149 298 354 1948 VII 459 135 228 304 1947 VIII 462 142 196 296 1945 X 548 180 203 246 1944 XI 478 150 230 283 1940 XV 598 148 235 278 152 259 316 1950 females V 418 120 321 366 1949 VI 458 137 228 325 1948 VII 491 136 276 343 1947 VIII 483 150 271 379 1946 IX 527 169 231 323 142 265 347 Back-calculated mean SL at the end of each growth season Year of spawning [l.sub.4] [l.sub.5] [l.sub.6] [l.sub.7] 1952 males 1951 391 1950 391 414 1948 363 398 425 448 1947 358 391 426 445 1945 436 450 472 504 1944 302 341 375 410 1940 335 361 410 422 368 392 422 446 1950 females 390 411 1949 416 430 450 1948 385 422 453 475 1947 404 456 450 468 1946 384 421 452 491 396 424 451 478 Back-calculated mean SL at the end of each growth season Year of spawning [l.sub.8] [l.sub.9] [l.sub.10] 1952 males 1951 1950 1948 1947 1945 522 541 1944 440 460 470 1940 467 485 501 476 495 501 1950 females 1949 1948 1947 478 1946 509 526 493 526 Back-calculated mean SL at the end of each growth season Year of spawning [l.sub.11] [l.sub.12] [l.sub.13] 1952 males 1951 1950 1948 1947 1945 1944 1940 521 536 550 521 536 550 1950 females 1949 1948 1947 1946 Table III. Mouth gape and intestine length indices for the wild common carp and domesticated common carp: o [l.sup.-1] (10 x mouth gape in square centimeters per standard length in centimeters), o [w.sup.-1] (10 x mouth gape in square centimeters per mass in grams), o [lc.sup.-1] (10 x mouth gape in square centimeters per length of head in centimeters); gut l-1 (length of intestine in centimeters per 1 cm of standard length), gut [w.sup.-1] (length of intestine in centimeters per 10 g of wet mass). Index [ol.sup.-1] [ow.sup.-1] o [lc.sup.-1] Wild common carp 1.14 with supplementary diet 1.09 0.10 4.46 with natural diet 1.24 0.08 5.27 Domesticated carp 1.91 with supplementary diet 2.00 0.08 8.12 with natural diet 2.30 0.08 8.12 Index gut [l.sup.-1] gut [w.sup.-1] Wild common carp with supplementary diet 2.11 3.02 with natural diet Domesticated carp with supplementary diet 2.64 2.25 with natural diet Table IV. Comparison of characters between 25 cleavage eggs (step C2) of Lucania parva (LP) and L. goodei (LG). Significant (p < 0.05) differences between means (t-test) and between variances (F-test) are indicated with directional signs (< or >). Mean Variance Character LP LG LP LG Clutch size 12.0 > 6.8 99.0 > 33.9 Activation rate (%) 79.4 > 61.1 602.9 1027.2 Yolk diameter (in mm) 1.060 <1.201 2.6 2.7 Yolk volume (in [mm.sup.3]) 0.628 < 0.911 7.7 1.4 Yolk shrinkage (%) 6.96 6.95 13.460 10.445 Blastodisc height (in mm) 0.153 0.146 1.0 1.0 Blastodisc width (in mm) 0.614 0.645 6.0 8.0 Blastodisc volume (in [mm.sup.3]) 0.029 0.031 2.2 2.0 Blastodisc:yolk ratio (%) 4.8 > 3.5 6.6 3.5