A PHOTO STUDY OF THE EASTERN PACIFIC HYBRID ABALONES (GENUS HALIOTIS)

Buzz Owen
P.O. Box 601
Gualala, California 95445
buzabman@mcn.org

Part 9

THE BACK CROSSES OF HYBRIDS TO OTHER
SPECIES AND PARENT SPECIES.

H. rufescens Swainson, 1822 x H. sorenseni Bartsch, 1940 X H. corrugata Wood, 1828
H. corrugata x H. fulgens Philippi, 1845 X H. rufescens
H. corrugata x H. walallensis Stearns, 1899 X H. rufescens
H. rufescens x H. sorenseni X H. rufescens

ABSTRACT

Three of the four known specimens of three extremely rare hybrid abalone are illustrated with high-resolution color photography. Two specimens of each of the respective parent species are also illustrated for comparison purposes. Reasons for the necessity of this review of the West American hybrid Haliotis are further discussed.

INTRODUCTION

Review of Earlier Papers: The present work is the ninth and final report in a series of nine papers that have illustrated each of the fourteen interspecific Eastern Pacific Haliotis hybrids that are currently known as having been retrieved from natural populations. An earlier un-numbered paper (herein designated as Part 10 [Of Sea and Shore, Vol. 24, No. 3]), began the series with the treatment of two hybrids of H. cracherodii Leach, 1814 (with H. fulgens Philippi, 1845, and H. corrugata Wood, 1828), then Parts one and two treated H. rufescens Swainson, 1822 x H. corrugata (Vol. 25, No. 2), and H. corrugata x H. walallensis Stearns, 1899 (Vol. 25, No. 3). Parts three and four covered H. corrugata x H. fulgens (Vol. 25, No. 4), and H. rufescens x H. kamtschatkana assimilis Dall, 1878 (Vol. 26, No. 2), while Part five treated H. corrugata x H. sorenseni Bartsch, 1940 (Vol. 26, No. 3). Part six continued our review with the examination of H. rufescens x H. sorenseni (Vol. 26, No. 4), followed by Part seven which began our treatment of the extremely rare hybrids, exploring H. kamtschatkana assimilis x H. sorenseni; H. rufescens x H. walallensis; and H. kamtschatkana assimilis x H. walallensis (Vol. 27, No. 1). Part eight continued with the rarest of the two-species hybrids examined in this series, H. rufescens x H. fulgens; H. sorenseni x H. walallensis; and H. corrugata x H. kamtschatkana assimilis (Vol. 27, No. 2). The series ends with this report which illustrates three unique specimens that represent hybridization of three of these hybrid varieties with a third Haliotis species, and a single specimen which represents a back cross of a hybrid to one of its parent species.

Hybridization of the Eastern Pacific Haliotis has been well documented. Owen (1961) presented a report on six varieties found in Southern California and the adjacent Channel Islands. Owen et al. (1971) expanded this report to include six additional hybrid varieties. These 12 crosses involved all west coast species with the exception of H. cracherodii, however, as mentioned earlier, Owen and Leighton (2002) described two hybrids of H. cracherodii crossed with H. corrugata and H. fulgens. Hybrid Haliotis have been further discussed and reported in South and Western Australia, by Owen and Kershaw (2002, 2003).

Beginning in the early 1980s, a severe decline was noticed in abalone populations at the Southern California Channel Islands. Consequently few, if any, of these hybrids were retrieved by commercial Haliotis divers (C. Sites, J. Marshall pers. comm.). The reasons for this decline remain unclear. Commercial over-fishing doesn’t appear to have been the exclusive contributing factor as two species that were never taken commercially in that area, H. walallensis, and H. kamtschatkana assimilis, suffered a marked decline during the same period as well.

This severe population decline continued in all Haliotis species throughout Southern California and the adjacent Channel Islands and finally led to closure of the sport and commercial fisheries in these areas in 1997. This closure is still in effect. It appears clear that few, if any, of the very rare hybrid varieties (hybrids other than the most common: H. rufescens x H. sorenseni) were taken after the period from 1975 to 1980. Thus, virtually all known specimens exist in either the Buzz Owen Collection (BOC), Gualala, California, or in the Los Angeles County Museum of Natural History (LACM). The LACM specimens were deposited by Owen as reference for the earlier paper on Eastern Pacific hybrids (Owen et al. 1971). The primary purpose of this first work was to demonstrate the natural occurrence of hybrid Haliotis specimens. Thus, only a single shell specimen was photographed in black and white for each hybrid variety illustrated. This led to much confusion in subsequent years when Haliotiphiles tried to use this paper as an identification guide during searches of commercial Haliotis shell piles, where the vast majority of hybrid Haliotis specimens have been found to date. This has proven to be especially true in Lower California, Mexico, where a commercial fishery still exists (2007). Therefore, the primary impetus for this reappraisal is to illustrate a number of specimens of each hybrid in color so as to facilitate a greater understanding of each variety and make it possible to accurately identify hybrid Haliotis shell specimens.

Until August, 1967, the fertility of Haliotis hybrids was unknown. Abalone aquaculture was in its infancy, and the two or three small laboratories just beginning operations were hardly aware that hybrids existed – much less possessed any living specimens to experiment with. In fact, the paper describing hybridization in Eastern Pacific Haliotis wasn’t published until four years later (Owen et al. 1971). Thus, no knowledge was available concerning possible hybrid Haliotis fertility. It was simply not known whether these hybrids could cross back with their parent species, much less with a third, non-parent, species. Then, between 1967 and 1970, a series of spawnings in a marine shellfish hatchery in Northern California, proved that at least four different hybrids were fertile. These four crosses were shown to be able to not only cross back with their respective parent species, but also to cross with a third species as well (Owen and Meyer, unpublished report. 1972). In natural populations, such backcrosses appear to be excessively rare – at least in respect to a hybrid crossing with another (third) species; only three such specimens, live-taken and identified by shell and animal morphology, are known to exist. The progeny of hybrids crossing back with their parent species is probably far more common, but due to genomic combinations, one would expect half or fewer of the crosses to reveal morphological characters of both parental species, and when doing so, to represent each more or less equally (D. Leighton, pers. comm.). For example, a female H. rufescens x H. sorenseni hybrid crossed back with a male H. rufescens, would produce progeny resembling either H. rufescens, or typical H. rufescens x H. sorenseni hybrids. A single exception exists: a specimen taken near Point Conception which clearly exhibited, both with shell and animal, what could best be described as “3/4 H. rufescens, 1/4 H. sorenseni” morphology (Pl. 4). In this case it is conceivable that genotypic variability within the parent stock masked or augmented the shell features observed in the hybrid progeny.

MATERIAL AND METHODS

Abbreviations of Collections: LACM: Los Angeles County Museum of Natural History; BOC: Buzz Owen Collection.
All three known backcrosses of hybrids to other species are unique – only single specimens exist of each. All are in the BOC. They were live-taken by Owen while diving commercially for abalones with compressed air. The specimen of an H. rufescens x H. sorenseni hybrid crossed back with H. rufescens is also unique and was live-taken by Owen as well. The animal was preserved in isopropyl alcohol and is in the LACM. Marine shellfish-hatchery-produced backcrosses of hybrids to a third species, and to parent species, were cultured by Owen in the marine shellfish hatchery where he worked for 14 years.

Photography was performed with a Canon G6 digital camera and the resulting images processed with an iMac computer using Adobe Photoshop 9.

RESULTS

1) Haliotis rufescens x H. sorenseni X H. corrugata.
This unique specimen was live-taken on the south side of Anacapa Island in September, 1960, in about 20 meters. It was at first suspected to be a specimen of H. rufescens x H. corrugata, though the morphology of H. sorenseni was clearly visible in both animal and shell as well. This confusion was caused in part by the fact that it wasn’t known in 1960 that hybrids could cross back with other species, and also because H. rufescens x H. corrugata wasn’t well understood as it had only recently been discovered and few specimens were available for study.

2) Haliotis corrugata x H. fulgens X H. rufescens.
In common with the hybrid backcross described above, this unique specimen was retrieved on the south side of Anacapa Island. It was live-taken in mid-October, 1960, in very shallow water (<6 m). At first, it was also misidentified as an H. rufescens x H. corrugata hybrid, for the same reasons as the above specimen, though the presence of H. fulgens was clearly visible in the morphology of both shell and animal.

3) Haliotis corrugata x H. walallensis X H. rufescens.
This specimen was found near Gull Rock (Island) on the south side of Santa Cruz Island, in 15 meters depth, in late 1962. The presence of H. walallensis was strongly visible in the epipodium of the animal: short, round, “stubby” papillae were present, with the “cauliflower-floret”-like multi-faceted surface on the larger papillae (or “warts”), dominating the entire surface between the margins. These “bumps” were slightly less “exaggerated”, and clearly showed the influence of the other parent species involved. The pigment and markings showed H. rufescens and H. corrugata strongly, and like the other two back crosses, this specimen was also listed briefly as “H. rufescens x H. corrugata”, but with a circled question mark. The animal was initially preserved and then lost. The shell is in the BOC.

4) Haliotis rufescens x H. sorenseni backcrossed to H. rufescens.
This unique specimen was found about 12 miles east of Point Conception in May, 1963. It was immediately recognized as being so unusual, that the day it was taken an entire page of the author’s logbook was used to describe it. Simply stated, both shell and animal strongly exhibited the morphology of H. rufescens, but also demonstrated weak characteristics of H. sorenseni. The classic details of the epipodial processes of H. sorenseni were present, but much reduced. To date (February, 2007), this is the only example that has come to the author’s attention. This specimen is a definite exception to the “rule” in Haliotis genetics that states that a hybrid back crossed to a parent species produces progeny that resemble either that hybrid, or the parent species crossed back to. This specimen, simply stated, appears to be “75% H. rufescens and 25% H. sorenseni”. As many elements of the genome dictate morphological features of shell and body, it is likely that in a simple backcross, complexities of chromosomal pairing, cross-overs, and deletions, together with gene expression, will affect all aspects of the final hybrid. A section of the epipodium of this hybrid is deposited in the LACM. The shell is in the BOC (Pl. 4).

DISCUSSION

It is suspected that the sex of the hybrid parent of a “three species” cross would very likely be female. This conclusion is based on propagation experiments carried out by the author in a marine shellfish hatchery between 1965 and 1979. During this period, in addition to conducting several hundred conspecific crosses, and a number of “two species” fertilizations, several “three species” hybrids were attempted. In all these crosses, both conspecific and hybrid, the resultant egg/sperm interactions were carefully studied, and notes taken. In all such crosses studied, the experiments with conspecific animals always resulted in rapid sperm/egg interactions. For example: when gametes of male and female H. rufescens were combined, sperm cells could be observed rapidly penetrating the protective gelatin envelope surrounding the egg, and shortly after, the presence of polar bodies was observed, which indicated that successful fertilization had occurred. When non-conspecific crosses were attempted, egg/sperm interactions were feeble and sluggish, and fertilization rates were low (Owen and Meyer, 1972; Leighton and Lewis, 1982). This being the case, if a hybrid spawning in a natural population was a male, and spawning females of non-parent species were nearby, the eggs from the latter would more likely be fertilized by sperm from conspecific males (rapid egg/sperm interaction), than by the slow interacting non-conspecific hybrid sperm cells. Conversely, if the spawning hybrid was a female, the eggs would almost always have to be fertilized (if at all) by one of its parent species, or, as in the case of three of the back-crosses considered herein, a third (non-parent) species. This would almost certainly be the case, as the likelihood of a male hybrid of similar parentage being in the general area would be almost non-existent, being that hybrids are extremely rare. Additionally, it is highly probable that many potential “multi-species” hybrids are formed in natural populations, but don’t survive through early settled stages or to adulthood due to differential, selective factors, including limitations of their own genetic composition restricting their adaptability, and behavior in a specific environment (D. Leighton, pers. comm.).

Final remark: This concludes this ten-part study of the hybrid Haliotis of the Pacific coast of North America. It essentially constitutes an up-date of the earlier work originally published by the LACM (Owen et al. 1971). Due to the recent disappearance of nearly the entire population of all species of Haliotis south of Point Conception (exception: H. rufescens at San Miguel Island), the possibility of new hybrid specimens coming to light seems remote. As stated throughout this series, the reasons for this decline remain unclear at this time. One of the species, H. sorenseni, has been listed as an “Endangered Species” under the Endangered Species Act of 1973, and several others have reduced populations as a result of disease (H. cracherodii with “Withering Foot Syndrome”), or unexplained causes (H. kamtschatkana assimilis and H. walallensis).
Comment of May, 2006: Recent evidence has indicated that successful recruitment of H. corrugata and H. rufescens has occurred off Point Loma, and, additionally, H. cracherodii at San Nicolas Island. Perhaps in the future, hybrids will again be found in natural populations.

(click here for plate 1)
(click here for plate 2)
(click here for plate 3)
(click here for plate 4)

ACKNOWLEDGEMENTS

I would like to thank David Leighton for his constructive review of the manuscript, and his description and clarification of the complex genetic factors involved in some of these crosses. I also wish to thank Stephen Browning and Tom Grace for providing helpful comments and editing suggestions. Finally, I am grateful to the many commercial abalone divers who contributed much material to the ten papers of this series, most notably Bob McMillen and Chuck Snell.

LITERATURE CITED

Leighton, D. L., and C. A. Lewis. 1982. Experimental Hybridization in Abalones. International Journal of Invertebrate Reproduction. 5:273-282.

Leighton, D. L. 2000. The Biology and Culture of the California Abalones. Dorrance Pub, Co. 216 pp. 68 Fig.

Owen, R. S. 1961. Hybridization in Western American Haliotis (Abstract). American Malacological Union Annual Report. 28:34.

Owen, B., J. H. McLean and R. J. Meyer. 1971. Hybridization in the Eastern Pacific Abalone (Haliotis). Bulletin of the Los Angeles County Museum of Natural History. Science 9:1-37.

Owen, B. and R. J. Meyer. 1972. Laboratory Studies of Hybridization in California Abalones (Haliotis). Unpublished MS. Pacific Mariculture, Inc., Pigeon Point, California. 38 pp.

Owen, B., L. H. DiSalvo, E. E. Ebert, and Erika Fonck. 1984. Culture of the California Red Abalone Haliotis rufescens Swainson (1822) in Chile. The Veliger 27:2:101-105.

Owen, Buzz R. S. and D. L. Leighton. 2002. Shell Specimens from Natural Populations Identified as Hybrids of the Black Abalone, Haliotis cracherodii Leach, 1814. Of Sea and Shore 24:3:135-138.

Owen, B. and D. Potter. 2002. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis). Part 1: Haliotis rufescens Swainson, 1822 x H. corrugata Wood, 1828. Of Sea and Shore 25:2:103-106.

Owen, B. and R. Kershaw. 2002. Hybridization in the South and Western Australian Abalones (Genus Haliotis): A Photo Study and Guide to the Identification of Shell Specimens. Of Sea and Shore 25:1:55-66.

Owen, B. and D. Potter. 2003. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis). Part 2: H. corrugata Wood, 1828 x H. walallensis Stearns, 1899. Of Sea and Shore 25:3:177-180.

Owen, B. and R. Kershaw. 2003. A New Hybrid Haliotis From Western Australia. Of Sea and Shore 26:1:50-53.

Owen, B. and D. Potter. 2003. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis). Part 3: H. corrugata Wood, 1828 x H. fulgens Philippi, 1845. Of Sea and Shore 25:4:246-250.

Owen, B. and D. Potter. 2004. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis) Part 4: H. rufescens Swainson, 1822 x H. kamtschatkana assimilis Dall, 1878. Of Sea and Shore 26:2:119-223.

Owen, B. 2004. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis). Part 5: H. corrugata Wood, 1828 x H. sorenseni Bartsch, 1940. Of Sea and Shore 26:3:154-157; 212.

Owen, B. 2005. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis). Part 6: H. rufescens, Swainson, 1822 x H. sorenseni Bartsch, 1940. Of Sea and Shore 26:4:232-236.

Owen, B. 2005. The Culture of a “Four Species” Haliotis Hybrid in a Marine Shellfish Hatchery. Of Sea and Shore 26:4:269-274.

Owen, B. 2005. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis). Part 7: H. kamtschatkana assimilis Dall, 1878 x H. sorenseni Bartsch, 1940; H. rufescens Swainson, 1822 x H. walallensis Stearns, 1899; H. kamtschatkana assimilis x H. walallensis. Of Sea and Shore 27:1:9-13; 15.

Owen, B. 2005. A Photo Study of the Eastern Pacific Hybrid Abalones (Genus Haliotis). Part 8: H. rufescens Swainson, 1822 x H. fulgens Philippi, 1845; H. sorenseni Bartsch, 1940 x H. walallensis Stearns, 1899; H. corrugata Wood, 1828 x H. kamtschatkana assimilis Dall, 1878. Of Sea and Shore 27:2:109-113; 115.

ADDITIONAL REFERENCES

Cox, K. W. 1962. California Abalones, Family Haliotidae. California Department of Fish and Game Fisheries Bulletin 118:1-131, pls. 1-8.

Geiger, D. L. 1998. Recent Genera and Species of the Family Haliotidae Rafinesque, 1815 (Gastropoda: Vetigastropoda). The Nautilus 111: 85-116.

Geiger, D. L. 2000. Distribution and Biogeography of the Recent Haliotidae (Gastropoda:Vetigastropoda) World Wide. Bollettino Malacologico 35:57-120.

Geiger, D. L. and Poppe, G. T. 2000. Family Haliotidae. In: Poppe, G. T. and Groh, K. (Eds). A Conchological Iconography. Conchbooks, Hackenheim, Germany. 135 pp., 83 pls.

Muñoz Lopez, T. 1975. Descripción de los Híbridos Interspecíficos del Genero Haliotis (Mollusca: Gastropoda). Tesis Biólogo. Universidad Autonoma de Nuevo Leon, México. (In Spanish)