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Marine Biology

, 166:54 | Cite as

Size-dependent change in body shape and its possible ecological role in the Patagonian squid (Doryteuthis gahi) in the Southwest Atlantic

  • Jessica B. JonesEmail author
  • Graham J. Pierce
  • Fran Saborido-Rey
  • Paul Brickle
  • Frithjof C. Kuepper
  • Zhanna N. Shcherbich
  • Alexander I. Arkhipkin
Original paper

Abstract

Cephalopods are a versatile group with several mechanisms in place to ensure the success of future generations. The Patagonian long-finned squid (Doryteuthis gahi) populations on the southern Patagonian shelf are believed to be genetically homogenous, but the mechanisms connecting them geographically and temporally are unresolved. Individual growth is highly variable within cephalopod populations and is likely to affect individual patterns of migration and, thus, population connectivity as a whole. Therefore, this study aimed to make inferences about population structure by analysing the size at which individuals were mature and aimed to describe the intrapopulation growth (allometric) trajectories of body shape, using landmark-based geometric morphometric techniques to describe phenotypes. Samples were collected from June 1999 to November 2017 around 52°S and 58°W. Smoothing curves from binomial generalised additive models (GAMs) suggested two size modes of maturity in females and one or multiple modes in males dependent on year and season. There was a gradual elongation of the mantle and an increase in the relative fin size throughout ontogeny. Shape scores from geometric morphometric shape coordinates revealed a continuous non-linear allometric trajectory with a significantly different slope angle for males exceeding 20.1 cm dorsal mantle length (DML). At the extreme of this continuum, the largest ‘super-bull’ form had a substantially more elongated body shape, a heavier fin and a larger fin area compared to the rest of the population, a body shape associated with enhanced swimming performance which may help to maintain population connectivity. The prevalence of these rare super-bulls in the fishery varied widely between years, suggestive of phenotypic plasticity. This study provides evidence that the D. gahi population on the southern Patagonian shelf has a complex population structure with high intraspecific variation.

Notes

Acknowledgements

This study was supported by funding from the Falkland Islands Government. We are grateful to the scientific observers from the Falkland Islands Fisheries Department for sample collection and Beverley Reid for collecting traditional morphometric measurements and to three referees for their comments which greatly improved the manuscript. We thank the Director of Fisheries, John Barton, for supporting this work. The MASTS pooling initiative (Marine Alliance for Science and Technology for Scotland, funded by the Scottish Funding Council and contributing institutions; Grant reference HR09011) is gratefully acknowledged. Thanks are due to FCT/MCTES for financial support to CESAM (UID/AMB/50017/2019) through national funds and ERDF co-financing, under the Partnership Agreement for the PT2020 and Compete 2020 programs.

Compliance with ethical standards

Conflict of interest

The authors have no conflict of interest to declare.

Research involving human participants and/or animals

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Supplementary material

227_2019_3501_MOESM1_ESM.png (71 kb)
Appendix 1 Estimated smoother from MN1 for the effect of dorsal mantle length (DML) in male Doryteuthis gahi with dotted lines indicating 95% confidence intervals. Expected degrees of freedom given in smoothing term (PNG 70 kb)
227_2019_3501_MOESM2_ESM.tif (571 kb)
Appendix 2 Contour plots for the partial effects from the GAM MN7 (Table 2) for a – males and b - females of longitude/latitude. Higher values indicate mature individuals. Position of the Falkland Islands included; thick white line indicates the Falkland Islands conservation zones (FICZ and FOCZ) (TIFF 570 kb)
227_2019_3501_MOESM3_ESM.tif (239 kb)
Appendix 3 The corresponding shape scores for Doryteuthis gahi included in the study as a function of log(centroid size) coloured by year and season, with symbols indicating whether an individual is male (circles) or female (triangles) (TIFF 238 kb)
227_2019_3501_MOESM4_ESM.docx (50 kb)
Supplementary material 4 (DOCX 50 kb)

References

  1. Adams DC, Otárola-Castillo E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods Ecol Evol 4(4):393–399CrossRefGoogle Scholar
  2. Adams DC, Rohlf FJ, Slice DE (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Ital J Zool 71(1):5–16.  https://doi.org/10.1080/11250000409356545 CrossRefGoogle Scholar
  3. Alcock J (2003) Animal behavior: an evolutionary approach, 7th edn. Sinauer Associates, Sunderland, p 560Google Scholar
  4. Arkhipkin AI, Middleton DA (2002) Sexual segregation in ontogenetic migrations by the squid Loligo gahi around the Falkland Islands. Bull Mar Sci 71(1):109–127Google Scholar
  5. Arkhipkin AI, Roa-Ureta R (2005) Identification of ontogenetic growth models for squid. Mar Freshw Res 56(4):371–386.  https://doi.org/10.1071/mf04274 CrossRefGoogle Scholar
  6. Arkhipkin AI, Laptikhovsky VV, Middleton DAJ (2000) Adaptations for cold water spawning in loliginid squid: Loligo gahi in Falkland waters. J Molluscan Stud 66(4):551–564.  https://doi.org/10.1093/mollus/66.4.551 CrossRefGoogle Scholar
  7. Arkhipkin AI, Grzebielec R, Sirota AM, Remeslo AV, Polishchuk IA, Middleton DA (2004) The influence of seasonal environmental changes on ontogenetic migrations of the squid Loligo gahi on the Falkland shelf. Fish Oceanogr 13(1):1–9.  https://doi.org/10.1046/j.1365-2419.2003.00269.x CrossRefGoogle Scholar
  8. Arkhipkin AI, Middleton DA, Barton J (2008) Management and conservation of a short-lived fishery resource: Loligo gahi around the Falkland Islands. Am Fish Soc Symp 49(2):1243Google Scholar
  9. Arkhipkin AI, Hatfield EM, Rodhouse PG (2013) Doryteuthis gahi, patagonian long-finned squid. In: Rosa R, O’Dor R, Pierce GJ (eds) Advances in squid biology, ecology and fisheries. Nova Science Publishers Inc, Part I-myopsid squids, pp 123–158Google Scholar
  10. Arkhipkin AI, Weis R, Mariotti N, Shcherbich Z (2015) ‘Tailed’ cephalopods. J Molluscan Stud 81(3):345–355.  https://doi.org/10.1093/mollus/eyu094 CrossRefGoogle Scholar
  11. Augustyn CJ, Llpiński MR, Sauer WHH (1992) Can the Loligo squid fishery be managed effectively? A synthesis of research on Loligo vulgaris reynaudii. S Afr J Mar Sci 12(1):903–918CrossRefGoogle Scholar
  12. Barón PJ, Ré ME (2002) Reproductive cycle and population structure of Loligo sanpaulensis of the northeastern coast of Patagonia. Bull Mar Sci 71(1):175–186Google Scholar
  13. Bartol IK, Krueger PS, Thompson JT, Stewart WJ (2008) Swimming dynamics and propulsive efficiency of squids throughout ontogeny. Integr Comp Biol 48(6):720–733.  https://doi.org/10.1093/icb/icn043 CrossRefPubMedGoogle Scholar
  14. Bookstein FL (1992) Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge.  https://doi.org/10.1017/cbo9780511573064 CrossRefGoogle Scholar
  15. Boyle PR, Boletzky SV (1996) Cephalopod populations: definition and dynamics. Phil Trans R Soc Lond B 351(1343):985–1002.  https://doi.org/10.1098/rstb.1996.0089 CrossRefGoogle Scholar
  16. Boyle P, Rodhouse P (2008) Cephalopods: ecology and fisheries. Wiley, Hoboken.  https://doi.org/10.1002/9780470995310 CrossRefGoogle Scholar
  17. Boyle PR, Pierce GJ, Hastie LC (1995) Flexible reproductive strategies in the squid Loligo forbesi. Mar Biol 121(3):501–508.  https://doi.org/10.1007/bf00349459 CrossRefGoogle Scholar
  18. Braga R, Crespi-Abril AC, Van der Molen S, Bainy MCRS, Ortiz N (2017) Analysis of the morphological variation of Doryteuthis sanpaulensis (Cephalopoda: Loliginidae) in Argentinian and Brazilian coastal waters using geometric morphometrics techniques. Mar Biodivers 47(3):755–762.  https://doi.org/10.1007/s12526-017-0661-z CrossRefGoogle Scholar
  19. Carvalho GR, Pitcher TJ (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. J Exp Mar Biol Ecol 126(3):243–258.  https://doi.org/10.1016/0022-0981(89)90190-1 CrossRefGoogle Scholar
  20. Coelho ML, Quintela J, Bettencourt V, Olavo G, Villa H (1994) Population structure, maturation patterns and fecundity of the squid Loligo vulgaris from southern Portugal. Fish Res 21(1–2):87–102.  https://doi.org/10.1016/0165-7836(94)90097-3 CrossRefGoogle Scholar
  21. Collins MA, Burnell GM, Rodhouse PG (1995) Reproductive strategies of male and female Loligo forbesi (Cephalopoda: Loliginidae). J Mar Biol Assoc UK 75(3):621–634.  https://doi.org/10.1017/s0025315400039059 CrossRefGoogle Scholar
  22. Collins MA, Boyle PR, Pierce GJ, Key LN, Hughes SE, Murphy J (1999) Resolution of multiple cohorts in the Loligo forbesi population from the west of Scotland. ICES J Mar Sci 56(4):500–509.  https://doi.org/10.1006/jmsc.1999.0485 CrossRefGoogle Scholar
  23. Crespel A, Dupont-Prinet A, Bernatchez L, Claireaux G, Tremblay R, Audet C (2017) Divergence in physiological factors affecting swimming performance between anadromous and resident populations of brook charr Salvelinus fontinalis. J Fish Biol 90(5):2170–2193.  https://doi.org/10.1111/jfb.13300 CrossRefPubMedGoogle Scholar
  24. Crespi-Abril AC, Morsan EM, Barón PJ (2010) Analysis of the ontogenetic variation in body and beak shape of the Illex argentinus inner shelf spawning groups by geometric morphometrics. J Mar Biol Assoc UK 90(3):547–553.  https://doi.org/10.1017/s0025315409990567 CrossRefGoogle Scholar
  25. Drake AG, Klingenberg CP (2008) The pace of morphological change: historical transformation of skull shape in St Bernard dogs. Proc R Soc Lond B Biol Sci 275(1630):71–76.  https://doi.org/10.1098/rspb.2007.1169 CrossRefGoogle Scholar
  26. Fang Z, Chen X, Su H, Thompson K, Chen Y (2017) Evaluation of stock variation and sexual dimorphism of beak shape of neon flying squid, Ommastrephes bartramii, based on geometric morphometrics. Hydrobiologia 784(1):367–380.  https://doi.org/10.1007/s10750-016-2898-0 CrossRefGoogle Scholar
  27. Fang Z, Fan J, Chen X, Chen Y (2018) Beak identification of four dominant octopus species in the East China Sea based on traditional measurements and geometric morphometrics. Fish Sci 84(6):975–985.  https://doi.org/10.1007/s12562-018-1235-0 CrossRefGoogle Scholar
  28. Forsythe JW (1993) A working hypothesis of how seasonal temperature change may impact the field growth of young cephalopods. In: Okutani A, O’Dor RK, Kubodera T (eds) Recent advances in cephalopod fisheries biology. Tokai University Press, Tokyo, pp 133–143Google Scholar
  29. Forsythe JW (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Mar Freshw Res 55(4):331–339.  https://doi.org/10.1071/mf03146 CrossRefGoogle Scholar
  30. Forsythe JW, Walsh LS, Turk PE, Lee PG (2001) Impact of temperature on juvenile growth and age at first egg-laying of the Pacific reef squid Sepioteuthis lessoniana reared in captivity. Mar Biol 138(1):103–112.  https://doi.org/10.1007/s002270000450 CrossRefGoogle Scholar
  31. Fraser DJ, Bernatchez L (2005) Adaptive migratory divergence among sympatric brok charr populations. Evolution 59(3):611–624.  https://doi.org/10.1554/04-346 CrossRefPubMedGoogle Scholar
  32. Guerra A, Rocha F (1994) The life history of Loligo vulgaris and Loligo forbesi (Cephalopoda: Loliginidae) in Galician waters (NW Spain). Fish Res 21(1–2):43–69.  https://doi.org/10.1016/0165-7836(94)90095-7 CrossRefGoogle Scholar
  33. Hall KC, Hanlon RT (2002) Principal features of the mating system of a large spawning aggregation of the giant Australian cuttlefish Sepia apama (Mollusca: Cephalopoda). Mar Biol 140(3):533–545.  https://doi.org/10.1007/s00227-001-0718-0 CrossRefGoogle Scholar
  34. Hanlon RT, Messenger JB (1996) Cephalopod behaviour. Cambridge University Press, Cambridge.  https://doi.org/10.1017/s0025315400041060 CrossRefGoogle Scholar
  35. Hanlon RT, Smale MJ, Sauer WH (2002) The mating system of the squid Loligo vulgaris reynaudii (Cephalopoda, Mollusca) off South Africa: fighting, guarding, sneaking, mating and egg laying behavior. Bull Mar Sci 71(1):331–345Google Scholar
  36. Hastie LC, Nyegaard M, Collins MA, Moreno A, Pereira JMF, Piatkowski U, Pierce GJ (2009) Reproductive biology of the loliginid squid, Alloteuthis subulata in the north-east Atlantic and adjacent waters. Aquat Living Resour 22(1):35–44.  https://doi.org/10.1051/alr/2009002 CrossRefGoogle Scholar
  37. Hatfield E (1991) Post-recruit growth of the Patagonian squid Loligo gahi (D’Orbigny). B Mar Sci 49(1–2):349–361Google Scholar
  38. Hatfield EMC (2000) Do some like it hot? Temperature as a possible determinant of variability in the growth of the Patagonian squid, Loligo gahi (Cephalopoda: Loliginidae). Fish Res 47(1):27–40.  https://doi.org/10.1016/s0165-7836(99)00127-7 CrossRefGoogle Scholar
  39. Hatfield EMC, Murray AWA (1999) Objective assessment of maturity in the Patagonian squid Loligo gahi (Cephalopoda: Loliginidae) from Falkland Islands waters. ICES J Mar Sci 56(5):746–756.  https://doi.org/10.1006/jmsc.1999.0514 CrossRefGoogle Scholar
  40. Hirst AG (2012) Intraspecific scaling of mass to length in pelagic animals: ontogenetic shape change and its implications. Limnol Oceanogr 57(5):1579–1590.  https://doi.org/10.4319/lo.2012.57.5.1579 CrossRefGoogle Scholar
  41. Hoar JA, Sim E, Webber DM, O’Dor RK (1994) The role of fins in the competition between squid and fish. Cambridge University Press, Cambridge.  https://doi.org/10.1017/cbo9780511983641.004 CrossRefGoogle Scholar
  42. Jackson GD, Steer BM, Wotherspoon S, Hobday AJ (2003) Variation in age, growth and maturity in the Australian arrow squid Nototodarus gouldi over time and space what is the pattern? Mar Ecol Prog Ser 264:57–71.  https://doi.org/10.3354/meps264057 CrossRefGoogle Scholar
  43. Jiang L, Kang L, Wu C, Chen M, Lü Z (2018) A comprehensive description and evolutionary analysis of 9 Loliginidae mitochondrial genomes. Hydrobiologia 808(1):115–124.  https://doi.org/10.1007/s10750-017-3377-y CrossRefGoogle Scholar
  44. Laptikhovsky V (2008) New data on spawning and bathymetric distribution of the Patagonian squid, Loligo gahi. Mar Biodivers Rec.  https://doi.org/10.1017/s175526720700560x CrossRefGoogle Scholar
  45. Lipinski M (1979) Universal maturity scale for the commercially-important squids (Cephalopoda:Teuthoidea). The results of maturity classification of the Illex illecebrosus (LeSueur, 1821) population for the years 1973–1977. ICNAF Res Doc, pp 1–39Google Scholar
  46. Lombarte A, Rufino MM, Sánchez P (2006) Statolith identification of Mediterranean Octopodidae, Sepiidae, Loliginidae, Ommastrephidae and Enoploteuthidae based on warp analyses. J Mar Biol Assoc U K 86(4):767–771.  https://doi.org/10.1017/s0025315406013683 CrossRefGoogle Scholar
  47. Mangold K (1987) Reproduction. In: Boyle PR (ed) Cephalopod life cycles, vol 2. Academic Press, London, pp 157–200.  https://doi.org/10.1017/s0025315400050190 CrossRefGoogle Scholar
  48. Mesnil B (1977) Growth and life cycle of squid, Loligo pealei and Illex illecebrosus, from the Northwest Atlantic. ICNAF Selecte Pap 2:55–69Google Scholar
  49. Moreno A, Pereira J, Cunha M (2005) Environmental influences on age and size at maturity of Loligo vulgaris. Aquat Living Resour 18(4):377–384.  https://doi.org/10.1051/alr:2005023 CrossRefGoogle Scholar
  50. Moreno A, Azevedo M, Pereira J, Pierce GJ (2007) Growth strategies in the squid Loligo vulgaris from Portuguese waters. Mar Biol Res 3(1):49–59CrossRefGoogle Scholar
  51. Neige P (2003) Spatial patterns of disparity and diversity of the recent cuttlefishes (Cephalopoda) across the old world. J Biogeogr 30(8):1125–1137.  https://doi.org/10.1046/j.1365-2699.2003.00918.x CrossRefGoogle Scholar
  52. Neige P, Boletzky SV (1997) Morphometrics of the shell of three Sepia species (Mollusca: Cephalopoda): intra-and interspecific variation. Zool Beitr 38:137–156Google Scholar
  53. O’Dor R (1998) Can understanding squid life-history strategies and recruitment improve management? S Afr J Mar Sci 20(1):193–206.  https://doi.org/10.2989/025776198784126188 CrossRefGoogle Scholar
  54. Olyott LJH, Sauer WHH, Booth AJ (2006) Spatio-temporal patterns in maturation of the chokka squid (Loligo vulgaris reynaudii) off the coast of South Africa. ICES J Mar Sci 63(9):1649–1664.  https://doi.org/10.1016/j.icesjms.2006.06.011 CrossRefGoogle Scholar
  55. Patterson K (1988) Life history of Patagonian squid Loligo gahi and growth parameter estimates using least-squares fits to linear and Von Bertalanffy models. Mar Ecol Prog Ser.  https://doi.org/10.3354/meps047065 CrossRefGoogle Scholar
  56. Pecl GT, Jackson GD (2008) The potential impacts of climate change on inshore squid: biology, ecology and fisheries. Rev Fish Biol Fisher 18(4):373–385.  https://doi.org/10.1007/s11160-007-9077-3 CrossRefGoogle Scholar
  57. Pierce GJ, Guerra A (1994) Stock assessment methods used for cephalopod fisheries. Fish Res 21(1–2):255–285.  https://doi.org/10.1016/0165-7836(94)90108-2 CrossRefGoogle Scholar
  58. Pierce GJ, Sauer W, Allcock AL, Smith JM, Wangvoralak S, Jereb P, Hastie LC, Lefkaditou E (2013) Loligo forbesii, Veined Squid. In: Rosa R, O’Dor R, Pierce GJ (eds) Advances in squid biology, ecology and fisheries. Nova Science Publishers Inc, Part I-myopsid squids, p 73Google Scholar
  59. Raya CP, Balguerías E, Fernández-Núñez MM, Pierce GJ (1999) On reproduction and age of the squid Loligo vulgaris from the Saharan bank (north-west African coast). J Mar Biol Ass UK 79(1):111–120.  https://doi.org/10.1017/s002531549700012x CrossRefGoogle Scholar
  60. Rocha F, Guerra A (1999) Age and growth of two sympatric squid Loligo vulgaris and Loligo forbesi, in Galician waters (north-west Spain). J Mar Biol Ass UK 79(4):697–707.  https://doi.org/10.1017/s002531549800085x CrossRefGoogle Scholar
  61. Rodríguez-Mendoza R, Muñoz M, Saborido-Rey F (2011) Ontogenetic allometry of the bluemouth, Helicolenus dactylopterus dactylopterus (Teleostei: Scorpaenidae), in the Northeast Atlantic and Mediterranean based on geometric morphometrics. Hydrobiologia 670(1):5–22.  https://doi.org/10.1007/s10750-011-0675-7 CrossRefGoogle Scholar
  62. Rohlf FJ (2015) The tps series of software. Hystrix.  https://doi.org/10.4404/hystrix-26.1-11264 CrossRefGoogle Scholar
  63. Sauer W (1995) South Africa’s Tsitsikamma national park as a protected breeding area for the commercially exploited chokka squid Loligo vulgaris reynaudii. S Afr J Mar Sci 16(1):365–371.  https://doi.org/10.2989/025776195784156575 CrossRefGoogle Scholar
  64. Schroeder R, Schwarz R, Crespi-Abril AC, Alvarez Perez JA (2017) Analysis of shape variability and life history strategies of Illex argentinus in the northern extreme of species distribution as a tool to differentiate spawning groups. J Nat Hist 51(43–44):2585–2605.  https://doi.org/10.1080/00222933.2017.1374484 CrossRefGoogle Scholar
  65. Shashar N, Hanlon RT (2013) Spawning behavior dynamics at communal egg beds in the squid Doryteuthis (Loligo) pealeii. J Exp Mar Biol Ecol 447:65–74.  https://doi.org/10.1016/j.jembe.2013.02.011 CrossRefGoogle Scholar
  66. Team RC (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing 2015, ViennaGoogle Scholar
  67. van der Vyver J, Sauer W, McKeown N, Yemane D, Shaw P, Lipinski M (2016) Phenotypic divergence despite high gene flow in chokka squid Loligo reynaudii (Cephalopoda: Loliginidae): implications for fishery management. J Mar Biol Assoc UK 96(7):1507–1525.  https://doi.org/10.1017/s0025315415001794 CrossRefGoogle Scholar
  68. Vega MA, Rocha FJ, Osorio C (2001) Morfometría comparada de los estatolitos del calamar Loligo gahi d’Orbigny, 1835 (Cephalopoda: Loliginidae) del norte de Perú e islas Falkland. Investigaciones marinas 29(1):3–9.  https://doi.org/10.4067/s0717-71782001000100001 CrossRefGoogle Scholar
  69. Vega MA, Rocha FJ, Guerra A, Osorio C (2002) Morphological differences between the Patagonian squid Loligo gahi populations from the Pacific and Atlantic oceans. Bull Mar Sci 71(2):903–912Google Scholar
  70. Vila Y, Silva L, Torres MA, Sobrino I (2010) Fishery, distribution pattern and biological aspects of the common European squid Loligo vulgaris in the Gulf of Cadiz. Fish Res 106(2):222–228.  https://doi.org/10.1016/j.fishres.2010.06.007 CrossRefGoogle Scholar
  71. Wada T, Takegaki T, Mori T, Natsukari Y (2005) Alternative male mating behaviors dependent on relative body size in captive oval squid Sepioteuthis lessoniana (Cephalopoda, Loliginidae). Zool Sci 22(6):645–651.  https://doi.org/10.2108/zsj.22.645 CrossRefPubMedGoogle Scholar
  72. Wagenmakers EJ, Farrell S (2004) AIC model selection using Akaike weights. Psychon Bull Rev 11:192–196.  https://doi.org/10.3758/bf03206482 CrossRefPubMedGoogle Scholar
  73. Winter A, Arkhipkin A (2015) Environmental impacts on recruitment migrations of Patagonian longfin squid (Doryteuthis gahi) in the Falkland Islands with reference to stock assessment. Fish Res 172:85–95.  https://doi.org/10.1016/j.fishres.2015.07.007 CrossRefGoogle Scholar
  74. Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc Ser B 73(1):3–36.  https://doi.org/10.1111/j.1467-9868.2010.00749.x CrossRefGoogle Scholar
  75. Zelditch ML, Lundrigan BL, David Sheets H, Garland T Jr (2003) Do precocial mammals develop at a faster rate? A comparison of rates of skull development in Sigmodon fulviventer and Mus musculus domesticus. J Evol Biol 16(4):708–720.  https://doi.org/10.1046/j.1420-9101.2003.00568.x CrossRefPubMedGoogle Scholar
  76. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1(1):3–14.  https://doi.org/10.1111/j.2041-210x.2009.00001.x CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of AberdeenAberdeenUK
  2. 2.Falkland Islands Fisheries DepartmentStanleyFalkland Islands
  3. 3.South Atlantic Environmental Research InstituteStanleyFalkland Islands
  4. 4.CESAM and Departamento de BiologiaUniversidade de AveiroAveiroPortugal
  5. 5.Instituto de Investigacións Mariñas (CSIC)VigoSpain

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