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Potential for bias in using hybrids between common carp (Cyprinus carpio) and goldfish (Carassius auratus) in endocrine studies: a first report of hybrids in Lake Mead, Nevada, U.S.A.

INTRODUCTION

Common carp (Cyprinus carpio) belong to the carp and minnow family, Cyprinidae, and are native to Asia. During the period of 1880-1896, the U.S. Fish Commission distributed an estimated 2.4 million common carp across the country (Nico and Fuller, 1999). There are no records of introductions into the Colorado River but common carp were introduced to Nevada in 1881 and Arizona in 1885 and were present throughout the lower Colorado River before construction of the Hoover Dam in 1928 (Allen and Roden, 1978). Although common carp in Lake Mead are not important as a recreational species, they are relatively abundant, lending to their use as monitors of environmental health (Bevans et al., 1997; Patino et al., 2003; Goodbred et al., 2007).

Goldfish (Carassius auratus) are in the same family as common carp. They are native to eastern Asia where selective breeding of visible mutations like color, shape, and fin and eye structure have been extensively developed for use in aquaria (Hulata, 1995). In the U.S. goldfish were initially brought from Europe during the 1600s and by midcentury were numerous in the Hudson River (Nico and Fuller, 1999). In Lake Mead they have been a popular live bait fish, which probably accounts for their presence in the lake (Minckley, 1973) where four goldfish were collected in 1975 (Allen and Roden, 1978).

Common carp have been routinely sampled for environmental studies in Lake Mead for almost 20 y. Since goldfish are also present in Lake Mead there is a possibility of hybridization between the two species. The objective of this study was to look for presence of hybrids using morphology and meristics under a larger endocrine and reproductive health study in Lake Mead, Nevada and Arizona.

MATERIAL AND METHODS

We sampled 363 common carp in Mar. 2008 using seine and electrofishing techniques. Detailed methods can be found in Patino et al. (2012) and a brief summary follows. We electrofished in shallower water (<4 m) adjacent to shorelines where cover was present. Fish were collected and placed in a live well for processing on shore where we collected morphometric and meristic measurements, including condition factor, lateral line scale counts, and presence or absence of anterior barbels. Condition factor was calculated by; K (TL) = W [10.sup.5]/[L.sup.3] where W is total weight in grams and L is total length in millimeters. Methods for processing fish gonads followed those described by Patino et al. (2003). Gonads were dissected then the testes were preserved in 10% buffered formalin for histological analysis using standard procedures (Luna, 1992). Samples were embedded in paraffin blocks and sections cut at 6 [micro]m and stained with hematoxylin and eosin. Microscopical observations were made with a compound microscope and photographs taken with an Olympus digital camera (DP70; Tokyo, Japan). Criteria to differentiate hybrid common carp/goldfish from common carp or goldfish were based on Taylor and Mahon (1977), Hume et al. (1983), and Pullan and Smith (1987). These include lateral line scale counts (LLSC) of 37-40 for common carp, 28-31 for goldfish; the presence of both anterior and posterior barbels (two sets) in common carp, and the absence of barbels in goldfish.

RESULTS

Two specimens we collected at Overton Arm (Lat: 36[degrees]26.77'N, Long: 114[degrees]21.54'W) appeared to be different in body shape and color than common carp (Fig. 1). A female collected on 19 Mar. 2008 had a total length (TL) of 426 ram, total weight (TW) of 1115 g, condition factor [K(TL)] of 1.44, gonad weight (GW) of 113.8 g, LLSC of 34, and posterior barbels were present with no anterior barbels. A male was collected on 20 Mar. 9008 with a TL of 410 mm, TW of 1145 g, K(TL) of 1.66, GW of 27.8 g, LLSC of 34, and posterior barbels were present with no anterior barbels. We did not perform histological evaluation on the female hybrid, but a gross external examination of the ovaries (Fig. 2A) showed what appeared to be normal ovarian follicles at various stages of development. A general histological evaluation of the testis from the male hybrid revealed lobule-like structures with open lumens, but germ cells were absent (Fig. 2B) suggesting this fish was sterile.

DISCUSSION

Common carp and goldfish hybrids were reported as early as 1887 in the Laurentian Great Lakes and are now a common occurrence (Taylor and Mahon, 1977). They are particularly abundant in Lake Erie, where goldfish escaped into the lake from a rearing pond during a storm and interbred with the already established common carp populations (Hubbs, 1955). Before our study distribution in the U.S. was limited to the Midwest and included 48 records from Illinois with one each from neighboring Missouri and Ohio (U.S. Geological Survey, 2012). These types of hybrids are also found in New Zealand (Pullian and Smith, 1987); Australia (Hume et al., 1983); Russia (Zelinskij et al., 1992); and Britian (Wheeler, 1998). In areas where crucian carp (Carassius carassius) are located (Britain, Central and Eastern Europe) in addition to goldfish and common carp, identification of hybrids becomes more difficult without using microsatelite arrays (Hanfling et al., 2005).

The fish from our study are clearly hybrids because of LLSCs of 34 that placed them outside (between) metrics for common carp or goldfish and the absence of anterior barbels. Condition factor was not as useful to separate hybrids from the parent species. The male hybrid with a K (TL) of 1.66 was at the highest range (0.88-1.69), seen in 207 male common carp from our study, whereas, the female with a K(TL) of 1.44 was within the range of 1.07-2.20, from 156 female common carp from our study. Both of these condition factors were at the very low end of the range reported for goldfish of 1.4-3.35 (Carlander, 1969). To our knowledge, these are the first hybrids of common carp and goldfish that have been reported west of the Mississippi River in the continental United States. Common carp sampling for environmental studies has been conducted in Lake Mead since 1995 (Bevans et al., 1996; Patino et al., 2003; Patino et al., 2012). However, among the several hundreds of fish collected during these earlier studies, no evidence of hybrids was noticed based on external appearance although no deliberate examinations for the presence of hybrids were performed.

Because goldfish are closely related to common carp [they are both tetraploid and have similar chromosome numbers ([approximately equal to]100; Chistiakov and Voronova, 2009) and kayrotypes] and have similar spawning behaviors, hybridization between the species occurs both naturally and artificially (Hubbs, 1955; Trautman, 1957; Minckley, 1973; Scott and Crossman, 1973). Early genetic studies of hybrids between common carp and goldfish in the field (Dauzmann and Down, 1982) could not clearly determine the maternal or paternal species. However, a more recent study by Smith and McVeagh (2005) based on mitochondrial DNA analysis reported that hybridization occurred at several locations in New Zealand and also that either species could serve as the maternal parent. In another study using microsatellite DNA markers, Hanfling et al. (2005) found common carp and goldfish hybrids in both the United Kingdom and New Zealand and were also able to distinguish maternal and paternal genetic contributions. Because we did not conduct DNA analysis on the hybrids from this present study, we could not determine to which of the two possible combinations of hybrids they belong (goldfish X common carp or common carp X goldfish); thus, we chose not to use an X to designate these hybrids.

The indication that our male hybrid was sterile is supported by experimental evidence indicating that males from goldfish X common carp are not fertile (Matsui et al., 1956). The cause of sterility in male hybrids is not clearly understood but might be related to germ cell dysfunction or death during spermatogenesis (Ojima, 1973; Ojima et al., 1975). Chromosomal studies of common carp X goldfish hybrids found them to be triploids (Zelinskij et al., 1992), and by implication they would be also sterile. Yamaha et al. (2003) also indicated that common carp X goldfish hybrids are infertile because of spermatocyte abnormalities and the absence of spermatids and spermatozoa in the testes. Although these results are consistent there is another study (Hume et al., 1983) that found no testicular abnormalities in six male common carp X goldfish hybrids and also reported spent male hybrids in the field concluding that they could successfully spawn producing an F2 generation. Apparently fertility of male hybrids may be quite variable depending on the particular cross and other factors.

In contrast to the male hybrid the female appeared to have normal ovaries (Fig. 2A) which is supported by experimental evidence (Matsui et al., 1956) and field evidence (Trautman, 1957). Field evidence indicated that common carp X goldfish hybrids (both female and male) are fertile and that these FI hybrids may have actually backcrossed with the parent species. Trautman (1957) reported that in western Lake Erie hybrids backcrosses frequently comprised 30-90% of fish sampled. This finding is further supported by a more recent and reliable molecular/genetic study showing a low frequency of backcrossing in common carp X goldfish hybrids (Hanfling et al., 2005). However, Yamaha et al. (2003) could not histologically detect any oocytes in the ovaries of goldfish X common carp hybrids beyond the yolk globule stage , therefore could not confirm fertility.

Although the maternal and paternal species could not be determined, our study provides strong evidence for the occurrence of hybrids between common carp and goldfish in Lake Mead. However, due to the relative abundance of both species near urbanized areas, it is likely that hybrids are also present at other western U.S. locations. Because common carp are frequently used as field model for environmental studies, not only in Lake Mead but throughout the world (Ahokas et al., 1994; Goodbred et al., 1997; Alam et al., 2002; Patino et al., 2003; Stansley and Washuta, 2007), it becomes necessary to carefully identify specimens collected for analysis. Inadvertently including hybrids of common carp and goldfish in environmental samples could bias some of the measured endpoints. For example, common carp X goldfish hybrids in the Laurentian Great Lakes had different endocrine profiles and a higher incidence of gonadal tumors than common carp (Taylor and Mahon, 1977). Bauman (1992) also concluded that hybrid fish are not suitable for monitoring environmental health because of their genetic susceptibility to tumors. Potential differences between hybrids and common carp in other traits of interest to environmental studies, such as contaminant body burdens, are unknown. The simplest procedure for screening common carp and goldfish hybrids is by determining the number of pairs of barbels (hybrids have only one pair), counting lateral line scales, and examining the general appearance and shape of the body (condition factor). However, if backcrosses between hybrids and parental stocks do occur in the field, attempts to separate hybrids and their progeny from the parent species would be complicated because hybrid identification using standard morphometric and meristic measurements depends on the occurrence of intermediate traits (Gilbert, 1961). More reliable molecular/genetic techniques may be required to determine if backcrossing and introgression are occurring or if multiple cyprinid species are present.

Acknowledgments.--Funding for this study was provided in part by the Southern Nevada Public Land Management Act. We appreciate the help and assistance of the Lake Mead National Recreation Area staff and the National Park Service. The Texas Cooperative Fish and Wildlife Research Unit are jointly supported by U.S. Geological Survey, Texas Tech University, Texas Parks and Wildlife Department, The Wildlife Management Institute, and U.S. Fish and Wildlife Service. The use of trade names or products does not constitute endorsement by the U.S. government.

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STEVEN L. GOODBRED (1), U.S. Geological Survey (Emeritus), High Point, North Carolina 27262; REYNALDO PATINO, U.S. Geological Survey, Texas Cooperative Fish and Wildlife Research Unit, Texas Tech University, Lubbock 79409; ERIK ORSAK (2), U.S. Fish and Wildlife Service, Las Vegas, Nevada 89144; PRAKASH SHARMA, Department of Biological Sciences and Texas Cooperative Fish and Wildlife Research Unit, Texas Tech University, Lubbock 79409; and SHANE RUESSLER, U.S. Geological Survey, Southeast Ecological Science Center, Gainesville, Florida 32653. Submitted 4 May 2012; Accepted 17 July 2012.

(1) Corresponding author: Telephone (336) 887-2187; e-mail: sgoodbred@usgs.gov

(2) present address: U.S. Fish and Wildlife Service, Arlington, Texas 76011
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Title Annotation:Notes and Discussion
Publication:The American Midland Naturalist
Article Type:Report
Geographic Code:1U8NV
Date:Apr 1, 2013
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