Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T17:39:54.595Z Has data issue: false hasContentIssue false
  • English
  • Français

Phenotypic divergence despite high gene flow in chokka squid Loligo reynaudii (Cephalopoda: Loliginidae): implications for fishery management

Published online by Cambridge University Press:  09 December 2015

J.S.F. Van Der Vyver ,
W.H.H. Sauer ,
N.J. McKeown ,
D. Yemane ,
P.W. Shaw  and
M.R. Lipinski Open the ORCID record for M.R. Lipinski [Opens in a new window]
J.S.F. Van Der Vyver*
Affiliation:
Department of Ichthyology and Fisheries Science, Rhodes University, PO Box 94, Grahamstown 6140, South Africa
W.H.H. Sauer
Affiliation:
Department of Ichthyology and Fisheries Science, Rhodes University, PO Box 94, Grahamstown 6140, South Africa
N.J. McKeown
Affiliation:
Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Aberystwyth SY23 3DA, UK
D. Yemane
Affiliation:
Department of Agriculture, Forestry and Fisheries, Branch: Fisheries Management, Cape Town, South Africa Marine Research Institute, University of Cape Town, Private Bag X2, Rondebosch, 7700 Cape Town, South Africa
P.W. Shaw
Affiliation:
Department of Ichthyology and Fisheries Science, Rhodes University, PO Box 94, Grahamstown 6140, South Africa Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Aberystwyth SY23 3DA, UK
M.R. Lipinski
Affiliation:
Department of Ichthyology and Fisheries Science, Rhodes University, PO Box 94, Grahamstown 6140, South Africa
*
Correspondence should be addressed to:J.S.F. Van der Vyver, Department of Ichthyology and Fisheries Science, Rhodes University, PO Box 94, Grahamstown 6140, South Africa email: frikkie5er@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

The commercially important chokka squid Loligo reynaudii occurring in South African waters is currently managed on a single-unit stock hypothesis. We tested this assumption through a spatial comparison of the morphology throughout the distributional range of the species. Forty-three morphometric characters were measured from 1079 chokka collected off the south coast of South Africa, the west coast of South Africa, and southern Angola. While no significant differences were found in the hard body parts, results from classification analysis showed that though all four types of morphometric attributes (soft body parts, beaks, statoliths, sucker rings) resulted in some separation, the most consistent separation of samples from the three regions was based on soft body part morphometric characters. On average, though dependent on the model, the overall correct classification rate ranged from 0.68–0.99 for males and 0.7–0.99 for females in all three regions. Previous DNA analysis had revealed some genetic differences between west coast and south coast samples, suggesting the confluence of the cold Benguela and warm Agulhas current may act as the approximate point of a phenotypic and possible genetic breakpoint. Finer scale genetic analysis of samples collected across the Benguela–Agulhas confluence reported no significant genetic structuring in this area suggesting environmental heterogeneity and not restriction of genetic flow/isolation as the primary driver of the observed phenotypic divergence.

Keywords

CephalopodsmorphologymicrosatellitesLoliginidaesouthern Africa
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 7 , November 2016 , pp. 1507 - 1525
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allendorf, F.W., England, P.R., Luikart, G., Ritchie, P.A. and Ryman, N. (2008) Genetic effects of harvest on wild animal populations. Trends in Ecology and Evolution 23, 327–337.Google Scholar
Arkhipkin, A.I., Rodhouse, P.G.K., Pierce, G.J., Sauer, W.H.H., Sakai, M., Allcock, L., Arguelles, J., Bower, J.R., Castillo, G., Ceriola, L., Chen, C., Chen, X., Diaz-Santana, M., Downey, N., Gonzales, A.F., Granados Amores, J., Green, C.P., Guerra, A., Hendrickson, L.C., Ibáñez, C., Ito, K., Jereb, P., Kato, Y., Katugin, O.N., Kawano, M., Kidokoro, H., Kulik, V.V., Laptikhovsky, V.V., Lipinski, M.R., Liu, B., Mariátegui, L., Marin, W., Medina, A., Miki, K., Miyahara, K., Moltschaniwskyj, N., Moustahfid, H., Abhitabhata, J.T.N., Nanjo, N., Nigmatullin, C.N., Ohtani, T., Pecl, G., Perez, J.A.A., Piatkowski, U., Saikliang, P., Salinas–Zavala, C.A., Steer, M., Tian, Y., Ueta, Y., Vijai, D., Wakabay Ashi, T., Yamaguchi, T., Yamashiro, C., Yamashita, N. and Zeidberg, L.D. (2015) World Squid Fisheries. Reviews in Fisheries Science and Aquaculture 23, 29–252.Google Scholar
Augustyn, C.J. (1989) Systematics, life cycle and resource potential of the chokker squid Loligo vulgaris reynaudii. PhD thesis. University of Port Elizabeth, Port Elizabeth, South Africa.Google Scholar
Augustyn, C.J. (1991) The biomass and ecology of chokka squid Loligo vulgaris reynaudii off the west coast of South Africa. South African Journal of Zoology 26, 164–181.Google Scholar
Augustyn, C.J. and Grant, W.S. (1988) Biochemical and morphological systematics of Loligo vulgaris vulgaris (Lamarc) and Loligo vulgaris reynaudii (d'Orbigny) nov. comb. (Cephalopoda: Myopsida). Malacologia 29, 215–233.Google Scholar
Augustyn, C.J., Lipinski, M.R., Sauer, W.H.H., Roberts, M.J. and Mitchell-Innes, B.A. (1994) Chokka squid on the Agulhas Bank: life history and ecology. South African Journal of Science 90, 143–154.Google Scholar
Augustyn, C.J. and Roel, B.A. (1998) Fisheries biology, stock assessment, and management of the chokka squid (Loligo reynaudii) in South African waters: an overview. California Cooperative Oceanic Fisheries Investigations Report 39, 71–80.Google Scholar
Augustyn, C.J., Roel, B.A. and Cochrane, K.L. (1993) Stock assessment in the chokka squid Loligo vulgaris reynaudii fishery off the coast of South Africa. In Okutani, T., O'Dor, R.K. and Kubodera, T. (eds) Recent advances in fisheries biology. Tokyo: Tokai University Press, pp. 3–14.Google Scholar
Baron, P.J. and Re, M.E. (2002) Morphometry of the northern Patagonian sympatric populations of Loligo sanpaulensis and Loligo gahi . Journal of Biological Marine Association 82, 269–278.Google Scholar
Begg, G.A., Friedland, K.D. and Pearce, J.B. (1999) Stock identification and its role in stock assessment and fisheries management: an overview. Fisheries Research 43, 1–8.Google Scholar
Bonnaud, L., Rodhouse, P.G. and Boucher-Rodoni, R. (1998) A phylogenetic study of the squid family Onychoteuthidae (Cephalopoda: Oegopsida). Proceedings of the Royal Society London B 265, 1761–1770.Google Scholar
Borges, T.C. (1995) Discriminant analysis of geographic variation in hard structures of Todarodes sagittatus from the North Atlantic. ICES Marine Science Symposium 199, 433–440.Google Scholar
Boyle, P.R. (1990) Cephalopod biology in the fisheries context. Fisheries Research 8, 303–321.Google Scholar
Boyle, P.R. and Ngoile, M.A.K. (1993) Population variation and growth in Loligo forbesi (Cephalopoda: Loliginidae) from Scottish waters. In Okutani, T., O'Dor, R.K. and Kubodera, T. (eds) Recent advances in cephalopod fisheries biology. Tokyo: Tokai University Press, pp. 49–59.Google Scholar
Brunetti, N. and Ivanovic, M. (1991) Morfologia y morfometria de los estatolitos del calamari (Illex argentinus). Frente Maritimo 9, 53–61.Google Scholar
Cadrin, S.X. (2000) Advances in morphometric identification of fishery stocks. Reviews in Fish Biology and Fisheries 10, 91–112.CrossRefGoogle Scholar
Carvalho, G.R. and Nigmatullin, C.M. (1998) Stock structure analysis and species identification. In Rodhouse, P., Dawe, E. and O'Dor, R. (eds) Squid recruitment dynamics. The genus Illex as a model, the commercial Illex species and influence on variability. Rome: FAO, Fisheries Technical Papers 376, pp. 199–232.Google Scholar
Carvalho, G.R. and Pitcher, T.J. (1989) Biochemical genetic studies on the Patagonian squid Loligo gahi d'Orbigny. II. Population structure in Falkland waters using isozymes, morphometrics and life history data. Journal of Experimental Marine Biology and Ecology 126, 243–258.CrossRefGoogle Scholar
Clarke, M.R. (1986) A handbook for the identification of Cephalopod beaks. Oxford: Clarendon Press.Google Scholar
Clarke, M.K. and Maddock, L. (1988) Statoliths from living species of cephalopods and evolution. In Clarke, M.R. and Trueman, E.R. (eds) The Mollusca. Paleontology and neontology of Cephalopods , Vol. 12. San Diego, CA: Academic Press, pp. 169–184.Google Scholar
De'ath, G. and Fabricus, K. (2000) Classification and regression trees: a powerful yet simple technique for ecological data analysis. Ecology 8, 3178–3192.Google Scholar
Forsythe, J.W. (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Marine and Freshwater Research 55, 331–339.Google Scholar
Forsythe, J.W., Derusha, R.H. and Hanlon, R.T. (1994) Growth, reproduction and life span of Sepia officinalis (Cephalopoda, Mollusca) cultured through seven consecutive generations. Journal of Zoology 233, 175–192.Google Scholar
Forsythe, J.W., Walsh, L.S., Turk, P.E. and Lee, P.G. (2001) Impact of temperature on juvenile growth and age at first egg-laying of the Pacific reef squid Sepioteuthis lessoniana reared in captivity. Marine Biology 138, 103–112.Google Scholar
Goudet, J. (1995) Fstat (version 1.2): a computer program to calculate F-statistics. Journal of Heredity 86, 485–486.Google Scholar
Goudet, J., Raymond, M., de Meeus, T. and Rousset, F. (1996) Testing differentiation in diploid populations. Genetics 144, 1933–1940.CrossRefGoogle ScholarPubMed
Guerra, A., Perez-Losada, M., Rocha, F. and Sanjuan, A. (2001) Species differentiation of Sepia officinalis and Sepia hierredda (Cephalopoda: Sepiidae) based on morphological and allozyme analyses. Journal of the Marine Biology Association of the United Kingdom 81, 271–281.Google Scholar
Guo, S.W. and Thompon, E.A. (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48, 361–372.Google Scholar
Haefner, P.A. (1964) Morphometry of the common Atlantic squid, Loligo pealeii, and the brief squid, Lolliguncula brevis, in Delaware Bay. Chesapeake Science 3, 138–144.Google Scholar
Hastie, T., Tibshirani, R. and Friedman, J. (2009) The elements of statistical learning: data mining, inference, and prediction. New York, NY: Springer.Google Scholar
Henriques, R., Potts, W.M., Sauer, W.H.H. and Shaw, P.W. (2012) Evidence of deep genetic divergence between populations of an important recreational fishery species, Lichia amia L. 1758, around southern Africa. African Journal of Marine Science 34, 585–591.Google Scholar
Hernandez-Garcia, V. and Castro, J.J. (1998) Morphological variability in Illex coindetii (Cephalopoda: Ommastrephidae) along the north-west coast of Africa. Journal of the Marine Biological Association of the United Kingdom 78, 1259–1268.CrossRefGoogle Scholar
Horton, N. and Kleinman, K. (2010) Using R for data management, statistical analysis, and graphics. Boca Raton, FL: CRC Press.CrossRefGoogle Scholar
Ihssen, P.E., Booke, H.E., Casselman, J.M., McGlade, J.M., Payne, N.R. and Utter, F.M. (1981) Stock identification: materials and methods. Canadian Journal of Fisheries and Aquatic Sciences 38, 1838–1855.Google Scholar
James, G., Witten, D. and Hastie, T. (2014) An introduction to statistical learning: with applications in R. New York, NY: Springer.Google Scholar
Jereb, P. and Roper, C.F.E. (2010) Cephalopods of the World: an annotated and illustrated catalogue of cephalopod species known to date. FAO Species Catalogue for Fishery Purposes. Number 4, Volume 2. Rome: FAO.Google Scholar
Kashiwada, J. and Recksiek, C.W. (1978) Possible morphological indicators of population structure in the market squid, Loligo opalescens . Californian Department of Fish and Game Bulletin 169, 99–111.Google Scholar
Kassahn, K.S., Donnellan, S.C., Fowler, A.J., Hall, K.C., Adams, M. and Shaw, P.W. (2003) Molecular and morphological analyses of the cuttlefish Sepia apama indicate a complex population structure. Marine Biology 143, 947–962.Google Scholar
Kristensen, T.K. (1982) Multivariate statistical analysis of geographic variation in the squid Gonatus fabricii Lichtenstein 1818) (Mollusca: Cephalopoda). Malacologia 22, 581–586.Google Scholar
Kuhn, M. and Johnson, K. (2013) Applied predictive modeling. New York, NY: Springer Science & Business Media.Google Scholar
Lefkaditou, E. and Bekas, P. (2004) Analysis of beak morphometry of the horned octopus Eledone cirrhosa (Cephalopoda: Octopoda) in the Thracian Sea (NE Mediterranean). Mediterranean Marine Science 5, 143–149.Google Scholar
Liao, C.H., Liu, T.Y. and Hung, C.Y. (2010) Morphometric variation between the swordtip (Photololigo edulis) and mitre (P. chinensis) squids in the waters off Taiwan. Journal of Marine Science and Technology 18, 405–412.Google Scholar
Lipinski, M.R. (1979) Universal maturity scale for the commercially important squids (Cephalopoda: Teuthoidea). In Special Meeting of STACRES, February 1979. ICNAF Res. Doc. 79/11/38.Google Scholar
Lipinski, M.R. (1981) Systematic and evolutionary significance of morphological variability in the squid genus Illex (Cephalopoda). PhD thesis. University of Gdansk, Gdansk, Poland, 291 pp.Google Scholar
Lipinski, M.R., Roeleveld, M.A.C. and Underhill, L.G. (1993) Comparison of the statoliths of Todaropsis eblanae and Todarodes angolensis (Cephalopoda: Ommastrephidae) in South African waters. In Okutani, T., O'Dor, R.K. and Kubodera, T. (eds) Recent advances in fisheries biology. Tokyo: Tokai University Press, pp. 263–273.Google Scholar
Lipinski, M.R. and Underhill, L.G. (1995) Sexual maturation in squid: quantum or continuum? South African Journal of Marine Science 15, 207–223.Google Scholar
Lleonart, J., Salat, J. and Torres, G.J. (2000) Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology 205, 85–93.Google Scholar
Lutjeharms, J.R.E., Monteiro, P.M.S., Tyson, P.D. and Obura, D. (2001) The oceans around Southern Africa and regional effects of global change. South African Journal of Science 97, 119–130.Google Scholar
Martinez, P., Sanjuan, A. and Guerra, A. (2002) Identification of Illex coindetii, I. illecebrosus, and I. argentinus (Cephalopoda: Ommastrephidae) throughout the Atlantic Ocean; by body and beak characters. Marine Biology 141, 131–143.Google Scholar
Nei, M. (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89, 583–590.CrossRefGoogle ScholarPubMed
Neige, P. (2006) Morphometrics of hard structures in cuttlefish. Life and Environment 56, 121–127.Google Scholar
Ogden, R.S., Allcock, A.L., Watts, P.C. and Thorpe, J.P. (1998) The role of beak shape in octopodid taxonomy. South African Journal of Marine Science 20, 29–36.CrossRefGoogle Scholar
Olyott, L.J.H. (2002) A description of spatial and temporal aspects of the lifecycle of chokka squid Loligo reynaudi on the inshore spawning grounds and Agulhas Bank off the South Coast of South Africa . MSc thesis. Rhodes University, South Africa, 148 pp.Google Scholar
Olyott, L.J.H., Sauer, W.H.H. and Booth, A.J. (2006) Spatio-temporal patterns in maturation of the chokka squid (Loligo vulgaris reynaudii) off the coast of South Africa. ICES Journal of Marine Science 63, 1649–1664.CrossRefGoogle Scholar
Olyott, L.J.H., Sauer, W.H.H. and Booth, A.J. (2007) Spatial patterns in the biology of the chokka squid, Loligo reynaudii on the Agulhas Bank, South Africa. Reviews in Fish Biology and Fisheries 17, 159–172.Google Scholar
Pierce, G.J., Hastie, L.C., Guerra, A., Thorpe, R.S., Howard, F.G. and Boyle, P.R. (1994a) Morphometric variation in Loligo forbesi and Loligo vulgaris: regional, seasonal, sex, maturity and worker differences. Fisheries Research 21, 127–148.Google Scholar
Pierce, G.J., Thorpe, R.S., Hastie, L.C., Brierly, A.S., Guerra, A., Boyle, P.R., Jamieson, R. and Avila, P. (1994b) Geographic variation in Loligo forbesi in the Northeast Atlantic Ocean – analysis of morphometric data and tests of causal hypothesis. Marine Biology 119, 541–547.Google Scholar
Pineda, S.E., Hernandez, S.R., Brunetti, N.E. and Jerez, B. (2002) Morphological identification of two southwest Atlantic Loliginid squids: Loligo gahi and Loligo sanpaulensis . Revista de Investigacion y Desarrollo Pesquero 15, 67–84.Google Scholar
Pörtner, H.O. and Zielinski, S. (1998) Environmental constraints and the physiology of performance of squid. South African Journal of Marine Science 20, 207–221.Google Scholar
Pritchard, J.K., Stephen, M. and Donnelly, P.J. (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.Google Scholar
Raymond, M. and Rousset, F. (1995) Genepop (Version 1.2) population genetics software for exact tests and ecumenicism. Journal of Heredity 86, 248–249.Google Scholar
Roberts, M.J. (2005) Chokka squid (Loligo vulgaris reynaudii) abundance linked to changes in South Africa's Agulhas Bank ecosystem during spawning and the early life cycle. ICES Journal of Marine Science 62, 33–55.Google Scholar
Roberts, M.J., Downey, N.J. and Sauer, W.H.H. (2012) The relative importance of shallow and deep shelf spawning habitats for the South African chokka squid (Loligo reynaudii). ICES Journal of Marine Science 69, 563–571.CrossRefGoogle Scholar
Roberts, M.J. and Mullon, C. (2010) First Langrangian ROMS-IBM simulations indicate large losses of chokka squid Loligo reynaudii paralarvae from South Africa's Agulhas Bank. African Journal of Marine Science 32, 71–84.Google Scholar
Roper, C.F.E. and Voss, G.L. (1983) Guidelines for taxonomic descriptions of cephalopod species. Memoirs of the National Museum of Victoria 44, 49–63.Google Scholar
Sanchez, G., Perry, H.M. and Trigg, C.B. (1996) Morphometry of juvenile and subadult Loligo pealei and L. plei from the northern Gulf of Mexico. Fishery Bulletin 94, 535–550.Google Scholar
Sauer, W.H.H. (1995) South Africa's Tsitsikamma National Park as a protected breeding area for the commercially exploited chokka squid Loligo vulgaris reynaudii . South African Journal of Marine Science 16, 365–371.Google Scholar
Sauer, W.H.H., Downey, N.J., Lipinski, M.R., Roberts, M.J., Smale, M.J., Glazer, J. and Melo, Y. (2013) Loligo reynaudii . In Rosa, R., Pierce, G. and O'Dor, R. (eds) Advances in squid biology, ecology and fisheries. New York, NY: Nova Science Publishers, pp. 33–72.Google Scholar
Sauer, W.H.H., Lipinski, M.R. and Augustyn, C.J. (2000) Tag recapture studies of the chokka squid Loligo vulgaris reynaudi d'Orbigny, 1848 on inshore spawning grounds on the south-east coast of South Africa. Fisheries Research 45, 283–289.Google Scholar
Shaw, P.W., Hendrickson, L., McKeown, N., Stonier, T., Naud, M-J. and Sauer, W.H.H. (2010) Discrete spawning aggregations of Loliginid squid do not represent genetically distinct populations. Marine Ecology Progress Series 408, 117–127.CrossRefGoogle Scholar
Shea, E.K. and Vecchione, M. (2002) Quantification of ontogenetic discontinuities in three species of Oegopsid squids using model II piecewise linear regression. Marine Biology 140, 971–979.Google Scholar
Stonier, T. (2012) Microsatellite and morphometric analysis of chokka squid (Loligo reynaudi) from different spawning aggregations around the South African coast . MSc thesis. Rhodes University, South Africa, 94 pp.Google Scholar
van Oosterhout, C., Hutchinson, W.F., Derek, P.M.W. and Shipley, P. (2004) MICRO–CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.Google Scholar
Vega, M.A., Rocha, F.J., Guerra, A. and Osorio, C. (2002) Morphological differences between the Patagonian squid Loligo gahi populations from the Pacific and Atlantic oceans. Bulletin of Marine Science 71, 903–913.Google Scholar
Voight, J.R. (2002) Morphometric analysis of male reproductive features of Octopodids (Mollusca: Cephalopoda). Biology Bulletin 202, 148–155.Google Scholar
Weir, B.S. and Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution 38, 1358–1370.Google Scholar
Winnepenninckx, B., Backeljau, T. and Dewachter, R. (1993) Extraction of high molecular-weight DNA from molluscs. Trends in Genetics 9, 407.Google Scholar
Zecchini, F., Vecchione, M. and Roper, C.F.E. (1996) A quantitative comparison of hectocotylus morphology between Mediterranean and western Atlantic populations of the squid Illex coindetii (Cephalopoda: Ommastrephidae). Proceedings of the Biological Society of Washington 109, 591–599.Google Scholar
Zuur, A.F., Ieno, E.N. and Smith, G.M. (2007) Analysing ecological data. In Statistics for biology and health. New York, NY: Springer.Google Scholar
Supplementary material: File

Van Der Vyver supplementary material

Table A1-A2 and Figure B-D

Download Van Der Vyver supplementary material(File)
File 6.5 MB