Hybridization is the mating of genetically differentiated individuals or groups and may involve crossing individuals within a species (also known as line crossing or strain crossing) or crossing individuals between separate species. This breeding technique is used by aquaculturists in the hope of producing aquatic organisms with desired traits. Commonly, the desired goal is to produce offspring that perform better than both parental species (hybrid vigor or positive heterosis). Hybridization may also be used to transfer other desirable characteristics from one group or species to another, to combine valuable traits from two species into a single group, and to produce sterile individuals. This article focuses on the hybridization between different species, i.e. inter-specific hybridization, and we will limit the coverage to species of finfish.

The use of inter-species hybrids in aquaculture and their reporting to FAO

D. M. Bartley, K. Rana and A. J. Immink

Much of the early work on finfish hybridization in aquaculture was conducted on salmonids, but, in general, these species did not produce hybrids of commercial advantage because of insufficient growth improvement and lower survival. As a result, there was or perhaps still is, an impression that hybrids do not hold much attraction for aquaculturists. With the expansion of the sector and the increased number of species being bred and farmed, there are hybrids that now account for a substantial proportion of aquaculture production, and other hybrids may be emerging through further development. The increased use of induced spawning techniques such as hypophysation (the use of pituitary gland extract to induce ovulation) and synthetic hormones, in-vitro fertilisation technologies and increased knowledge of reproductive biology will enable the aquaculturist to overcome many of the behavioural, biological and geographical reproductive isolating mechanisms that prevent fish from hybridizing in nature.

The purpose of this article is to point out some of the hybrids used in aquaculture to draw attention to their growing contribution to aquaculture production. We also wish to point out the problem that hybrids presently cause with regard to their inclusion in FAO databases.

The use of hybrid finfish in aquaculture

Hybridization is widely used to increase growth rate, manipulate sex ratios, produce sterile animals, improve flesh quality, increase disease resistance, and improve environmental tolerance (Table 1). Hybridization between some species of tilapias such as Oreochromis niloticus x O. aureus results in the production of predominantly male offspring and reduces unwanted natural reproduction in growout ponds (Rosenstein and Hulata, 1993). Most of the tilapia production in Israel is based on this hybrid and reported by FAO as Oreochromis spp. The African x Thai catfish hybrid (Clarias gariepinus x C. macrocephalus) is preferred to the Thai catfish because it has the desired flesh quality of the Thai catfish and the fast growth of the African. The Thai National Inland Fisheries Institute indicated that nearly 80% of the Thai catfish aquaculture is based on this hybrid, however this is not reflected in official statistics which simply lists production as "Clarias spp.". In the USA the striped bass, Morone saxatilis, x white bass, M. chrysops, hybrid is the sixth most cultured "fish species". It accounts for 1.4% of the production and has only recently been included in FAO statistics. The production of Colossoma macropomum in Venezuela accounts for 29% of total aquaculture according to official information provided to FAO, but government aquaculture experts now believe that most of this production is of the hybrid between C. macropomum and Piaractus brachypoma (Photo 1). Other popular hybrids that are not found in government reports to FAO include the "bester" a sturgeon cross between the Beluga, Huso huso and the sterlet, Acipenser ruthenus, and the blue, Ictalurus furcatus, x channel, I. punctatus, catfish.

Hybrids may be used to exploit degraded aquatic environments. Lakes affected by acid rain may not be suitable for native salmonids, yet they are suitable for splake, a hybrid between lake trout, Salvelinus namaycush, x brook trout, S. fontinalis, that can tolerate low pH levels (Snucins, 1993).

Chromosome-set manipulation (eg Polyploidization) can be combined with hybridization to increase the viability of fishes and provide increased developmental stability during early life history stages. Polyploid hybrid salmon appear to be better suited for culture than either polyploid or hybrid salmon are on their own. Although many diploid salmonid hybrids are not used for culture, triploidization of the hybrids may confer increased viability on the hybrids (viability refers to the ability of the hybrid to survive and grow, but does not infer that the hybrid is fertile or capable of reproducing) (Gray et al., 1993). Hybridization and polyploidization utilized in tandem have improved developmental stability in salmonid x hybrids, for example triploidization of Atlantic salmon, Salmo salar, x European (brown) trout, S. trutta, hybrids crossed to produce sterile salmon, increased their survival and growth rate to a level comparable to diploid Atlantic salmon (Galbreath and Thorgaard, 1997). Triploid

Hybrid between Colossoma macropomum and Piaractus brachypomus, Papelón Station, Venezuela

Inadvertant hybrid (top), between farmed Nile tilapia O. niloticus (bottom) and an unidentified tilapia (possibly O. mossambicus or O. andersonii), that invaded farm ponds, Chizzizira Hatchery, Mozambique

Pacific salmon hybrids have earlier seawater acclimation times (Seeb et al., 1993). General disease resistance was improved by producing rainbow trout, Oncorhynchus mykiss, x char, Salvelinus spp., triploids and rainbow trout x coho salmon, O. kisutch, triploid hybrids had increased resistance to infectious hematopoetic necrosis virus (IHN), but these hybrids grew more slowly (Dorson et al., 1991).

As the domestication of fish species increases, the possibilities to increase production through appropriate hybridization will also increase. New hybrids will need to be tested as to their performance, viability (their abilty to grow), and fertility (their ability to reproduce). The Kuwait Institute of Scientific Research has produced a hybrid bream, Acanthopagus latus (Sheim) x Sparidentex hasta (sobiaty), that is currently being investigated. It has good growth and body quality and appears to be fertile (Khaled Al-Abdul-Elah, Kuwait Institute of Scientific Research, pers. comm.).

Although many aquaculturists purposefully produce inter-specfic hybrids, some hybrids are produced inadvertently through mixed spawning of different species in a hatchery, misidentification of species by hatchery personnel, or by contamination of the aquaculture facility with wild fish (Photo 2). To produce Indian major carp seed, different species are often induced to spawn in a common spawning pond thus providing the opportunity for unintentional hybridization (Padhi and Mandal 1997). Hybridization with wild fish is especially prevalent in tilapia ponds connected to natural water bodies that contain indigenous or feral tilapia populations. Such uncontrolled and unintentional hybridization could undermine the performance of cultured stocks and make future use of the contaminated stocks as broodstock questionable.

Reporting Hybrid Production to FAO

To collect data on aquaculture production from countries, FIDI (Fisheries Information, Data and Statistics Unit) sends out two questionnaires to each reporting country: a fisheries questionnaire and an aquaculture questionnaire. Total aquaculture production is included in the fisheries questionnaire and a breakdown of aquaculture production is requested in the aquaculture questionnaire. From this information FIDI annually produces the Fisheries Circular No. 815 - Aquaculture Production Statistics. Users of this publication will be aware that the data are available in various forms, but are all based around species or groupings of production from each country. The incorporation of production information on hybrids is

not easily reflected in the FAO database since the taxanomic classification code adopted by FAO cannot accommodate the hybrid nomenclature. The taxomomic code descriptors, as listed in FAO's Aquatic Sciences and Fishereis Information System, for e.g. 1,70(59)051,01 Oreochromis mossambicus are as follows:

As can be seen, there is no provision for hybrids in this coding system. Moreover, the FAO questionnaire on aquaculture requests that respondents report species and consequently hybrids may often be reported to the taxonomic level of genera only, e.g. Clarias spp. or grouped as `nei' (not elsewhere included). The increased tonnage of incompletely identified species reported by FAO reduces the usefulness of the data for monitoring the utilisation of aquatic biodiversity for aquaculture. This problem is not specfic to FAO, most international monitoring organisations require more clarity in the data they are provided with.

As well as information on production, the value of production is also included in the FAO database. Hybrids may command a premium price where their quality, e.g. flesh colour or texture, is superior, requiring that this difference in price be recorded separately. For example hybrid striped bass x white bass in the USA currently sell for $3/lb ($6.6/kg) and freshwater white bass have a market price of $2.44/lb (adapted from USA fishery production statistics).

Within the FAO aquaculture questionnaire, there is provision for each country to supply production data for every species it produces and any "other production", including hybrids. Some countries do report hybrid production, for example tilapia in Israel, but in many cases this reporting is inconsistent. The lack of constant reporting could be the result of limited interest in a hybrid. If the hybrid is well known, it could be reported as such for a short time, after which it is reported in the other groupings, such as family/genus or even as pure species. Tilapia hybrids in Israel were originally reported as the full cross (Oreochromis niloticus x O. aureus), but after two years this reverted to `tilapia hybrids' and eventually to `tilapia nei' (Oreochromis spp.) in 1995.

Figure 1. Breakdown by taxonomic level of total aquaculture production (including aquatic plants) reported to FAO.

Unclassified groupings, i.e. the production that is not reported as species, accounted for approximately 16 percent of annual global aquaculture production over the last seven years (in 1995 this was 4,669,000 tonnes). Of this unclassified production, the greatest percentage originates from production recorded to the taxonomic level of Order. Hybrids may have been reported in any category, but because most hybrids in Table 1 are of the same Genus, most, but not all, hybrids would probably be reported to Genus, which accounted for 3.6% of total aquaculture production in 1995. An unknown proportion of this production is likely to be hybrids, for example, Clarias spp reported by Thailand. It is assumed that the lack of reporting may be due, on one hand, to the difficulty of assessing parental origins of inter-specific hybrids and, on the other, because of the aggregation of small levels of production. It is also expected that some of the production given as species will include some hybrids. For example, tilapia production in Indonesia is given as Oreochromis niloticus and O. mossambicus, but it is known that a percentage of the production is of Oreochromis hybrids. This is important, not only for assessing aquaculture production in each country and of each species or hybrid, but also to allow for a better understanding of biodiversity. If the levels of production for hybrids are not known, countries could add an attachment to their returned questionnaires suggesting the probable percentages of the production resulting from the culture of each hybrid. Possible means of dealing with these shortcomings are summarized in Table 2.

In concluding, we wish to point out that it is not our intention to promote hybridization as the only method of genetic improvement, but simply as one method of improvement that has potential for some immediate gains. Desirable traits can usually be passed to the hybrid in one generation but it should be appreciated that hybridization can be a hit and miss proposition. In the case of some fertile hybrids, it may be desirable to backcross to either parental line or to breed the hybrids together and then select the best animals, thus combining hybridization and selective breeding. Although hybridization may not require the data management that a long term selective breeding programme would require, proper broodstock management, including the documentation and maintenance of the correct parental lines, avoidance of inbreeding, and the appropriate choice of sex for the matings, will be necessary. Documentation of the use of hybrids will be necessary to evaluate correctly the utility of this technique The reporting of hybrid production to FAO is strongly encouraged. It is of paramount importance to ensure that the correct information is being collected, collated and disseminated so that any decisions made using FAO statistics are done so on the correct knowledge base.

Readers are encouraged to provide additional information on the use of hybrids in aquaculture to the authors.

Literature Cited

Allen, S. K. J. and R. J. Wattendorf, 1987. Triploid grass carp: status and management implications. - Fisheries 12: 20-24.

Henderson-Arzapalo, A. and A. F. Maciorowski, 1994. A comparison of black drum, red drum, and their hybrid in salwater pond culture. - J. World Aquacult. Soc. 25: 289-296.

Brecka, B. J.,C. C. Kohler and D. H. Wahl, 1995. Effects of dietary protein concentration on growth, survival, and body composition of muskellunge, Esox masquinongy, and tiger muskellinge, Esox masquinongy x E. luscius, fingerlings. - J. World Aquacult. Soc. 26: 416-425.

Dunham, R. A. 1987. American catfish breeding programmes. - In: Tiews, K. (ed.), Selection, Hybridization and Genetic Engineering in Aquaculture of Fish and Shellfish, Vol. 2. FAO European Inland Fisheries Advisory Commission and International Council for the Exploration of the Sea, Rome, Italy and Copenhagen, Denmark, pp. 407-416.

Dunham, R. A., R. E. Brummet, M. O. Ella, and R. O. Smitherman, . 1990. Genotype-environment interactions for growth of blue, channel, and hybrid catfish in ponds and cages at varying densities. - Aquaculture 85: 143-151.

Gorshkova, G., S. Gorshova, H. Gordin, and W. Knibb, 1996. Karyological studies in hybrids of Beluga Huso huso (L.)and the Russian sturgeon Acipenser guldenstati Brant. - Isr. J. Aquacult. Bamidgeh 48: 35-39.

Grey, A. K., M. A. Evans and G. H. Thorgaard, 1993. Viability and development of diploid and triploid salmon hybrids. - Aquaculture 112: 125-142.

Head, W. D., A. Zerbi and W. O. Watanabe, 1994. Preliminary observatoins on the maketability of saltwater-cultured Florida red tilapia in Puerto Rico. - J. World Aquacult. Soc. 25: 432-441.

Hearn, M. C. 1986. Reproductive viability of sauger-walleye hybrids. - Prog. Fish. Cult. 48: 149-150. (N)

Hooe, M. L., D. H. Buck, and D. H. Wahl, 1994. Growth, survival, and recruitment of hybrid crappies stocked in small impoundments. - N. Am. J. Fish. Manage. 14: 137-142.

Khan, H. A., S. D.Gupta, P. V. G. K Reddy, M. S. Tantia, and G. V. Kowtal, 1990. Production of sterile intergeneric hybrids and their utility in aquaculture and stocking. - In: Keshavanath, P. and Radhakrishnan, K. V. (eds.), Carp Seed Production Technology. Special Publication of the AFS No 2. Asian Fisheries Society, Mangalor, India, pp. 41-48.

Kim, D. S., Y. K. Nam, and I.-S. Park, 1995. Survival and kayological analysis of reciprocal diploid and trploid hybrids bewtween mud loach (Misgurnus mizolepis) and cyrinid loach (Misgurnus anguillicaudatus). - Aquaculture 135: 257-265.

Krasnai, Z. L. 1987. Interspecific hybridization of warm warm finfish. - In: Tiews, K. (ed.), Selection, Hybridization, and Genetic Engineering in Aquaculture, Vol. Vol 2. FAO,EIFAC and ICES, Rome, Italy and Copenhagen, Denmark, pp. 35-45.

Lahav, M. and E. Lahav, 1990. The development of all-male tilapia hybrids in Nir David. - Isr. J. Aquacult. Bamidgeh 42: 58-61.

Lim, C., B. Leamaster, and J. A. Brock, 1993. Riboflavin requirement of fingerling red hybrid tilapia grown in seawater. - J. World Aquacult. Soc. 24: 451-458.

Nwadukwe, F.O. 1995. Hatchery propagation of five hybrid groups by artifical hybridization of Clarius gariepinus(B) and Heterobranchus longifilis (Val.) (Clariidae) using dry, powdered carp pituitary hormone. - J. Aquacult.-Trop. 10: 1-11.

Padhi, B. K. and R. K. Mandal, 1997. Inadvertant hybridization in a carp hatchery as detected by nuclear DNA RFLP. - J. Fish Biol. 50: 906-909.

Salami, A. A., O. A. Fagbenro and D. H. J. Sydenham, 1993. The production and growth of clariid catfish hybrids in concrete tanks. - Isr. J. Aquacult. Bamidgeh 45: 18-25.

Scheerer, P. D. and G. H. Thorgaard, 1983. Increased survival in salmonid hybrids by induced triploidy. - Can. J. Fish. Aquat. Sci. 40: 2040-2044.

Senhorini, J. A., G. M.Figueiredo, N. A. Fontes and J. Carolsfeld, 1988. Larval and fry cultrue of pacu, Piaractus mesopotamicus, tambaqui, Colossoma macropomum, and their reciprocal hybrids. - Boletin Tecnica CEPTA 1: 19-30.

Smith, T. I. J. 1988. Aquaculture of striped bass and its hybrids in North America. - Aquacult. Mag. 14: 40-49.

Snucins, E. J. 1993. Relative survival of hatchery-reared lake trout, brook trout and F1 splake stocked in low-pH lakes. - N. Am. J. Fish. Manage. 12: 460-464.

Steffens, W., H. Jaehnichen, and F. Fredrich, 1990. Possibilities of sturgeon culture in Central Europe. - Aquaculture 89: 101-122.

Suresh, A. V. 1991. Culture of walking catfish in Thailand. - J. Aquacult.-Trop. 2: 10-12.

Tidwell, J. H., C. D. Webster and J. A. Clark, 1992. Growth, feed conversion, and protein utilization of female green sunfish x male bluegill hybrids fed isocaloric diets with different potein levels. - Prog. Fish. Cult. 54: 234-239.

Will, P. S., J. M. Paret and R. J. Sheehan, 1994. Pressure induced triploidy in hybrid Lepomis. - J. World Aquacult. Soc. 25: 507-511.

Wohlfarth, G. W. 1994. The unexploited potential of tilapia hybrids in aquaculture. - Aqua. Fish. Manag. 25: 781-788.