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Annual cycle of growth and population structure of the estuarine crab Hemigrapsus crenulatus (Brachyura: Varunidae) off central Chile

Published online by Cambridge University Press:  02 June 2021

Ramiro A. Riquelme-Bugueño*
Affiliation:
Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile Instituto Milenio de Oceanografía Universidad de Concepción, Casilla 160-C, Concepción, Chile
Tomás Luppi
Affiliation:
Facultad de Ciencias Exactas y Naturales, Instituto de Investigaciones Marinas y Costeras (IIMyC), Universidad Nacional de Mar del Plata-CONICET, Mar del Plata, Argentina
Gonzalo S. Saldías
Affiliation:
Departamento de Física, Facultad de Ciencias, Universidad del Bío-Bío, Casilla–5C, Concepción, Chile Centro FONDAP de Investigación en Dinámica de Ecosistemas Marinos de Altas Latitudes (IDEAL), Valdivia, Chile
Marcelo E. Lagos
Affiliation:
Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
Mauricio A. Urbina
Affiliation:
Departamento de Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile Instituto Milenio de Oceanografía Universidad de Concepción, Casilla 160-C, Concepción, Chile
Marco A. Retamal
Affiliation:
Departamento de Oceanografía, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Casilla 160-C, Concepción, Chile
*
Author for correspondence: Ramiro A. Riquelme-Bugueño, E-mail: [email protected]

Abstract

Estuaries and saltmarshes play a fundamental role in the life cycle of many crab species. Diverse studies show that temperature and salinity modulate abundance, size frequency distribution (SFD), sex ratio and growth in crustaceans. These population parameters are usually challenging to estimate due to the high environmental variability of estuaries. Monthly samples of the estuarine crab Hemigrapsus crenulatus were taken from October 2003 to October 2004 (except July 2004) in the Tubul estuary, central Chile. We quantified temporal changes in abundance, size distribution, sex ratio and monthly growth through the annual cycle. A total of 1025 individuals were collected. Sizes ranged from 7.72–33.51 mm carapace length (CL) with a growth rate ranging between 2.13–30.5% mm CL mo−1. Size and growth rates were greater in spring-summer, suggesting a faster growth of younger crabs correlated with increasing sea temperatures in the austral summer. Overall, sex ratio was 1.75:1 in favour of males. Modal analysis identified at least seven cohorts cohabiting throughout the annual cycle. Growth parameters for males and females were the following, respectively: L∞ = 33.6 and 29.6, k = 0.69 and 0.91, t0 = –0.39 and −0.28. Changes in size distribution suggested a recruitment period during autumn and winter seasons when there are lower salinities and temperature fluctuations stresses. Generalized linear models indicated that sea temperature, salinity and chlorophyll were the environmental variables that better predicted the annual patterns in the population structure.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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References

Adiyodi, R (1988) Reproduction and development. In Burggren, W and McMahon, B (eds), Biology of the Land Crabs. Cambridge: Cambridge University Press, pp. 139185.CrossRefGoogle Scholar
Alveal, K (1988) Gracilaria de Tubul. Historia y significado de un recurso. Gayana Botánica 45, 119140.Google Scholar
Baeta, A, Cabral, HN, Neto, JM, Marques, JC and Pardal, MA (2005) Biology, population dynamics and secondary production of the green crab Carcinus maenas (L.) in a temperate estuary. Estuarine Coastal and Shelf Science 65, 4352.CrossRefGoogle Scholar
Bas, CC and Spivak, ED (2000) Effect of salinity on embryos of two Southwestern Atlantic estuarine grapsid crab species cultured in vitro. Journal of Crustacean Biology 20, 647656.CrossRefGoogle Scholar
Bas, CC and Spivak, ED (2003) Effects of embryonic salinity exposure on larval development in two populations of the estuarine crab Chasmagnathus granulatus Dana, 1851 (Crustacea: Brachyura). Invertebrate Reproduction & Development 43, 117123.CrossRefGoogle Scholar
Bas, C, Luppi, T and Spivak, E (2005) Population structure of the South American Estuarine crab, Chasmagnathus granulatus (Brachyura: Varunidae) near the southern limit of its geographical distribution: comparison with northern populations. Hydrobiologia 537, 217228.CrossRefGoogle Scholar
Bas, C, Nuñez, J, Spivak, E and Luppi, T (2019) Inter-population differences in feeding ecology under nitrogen-limited diets: field growth and the role of cannibalism in limiting/improving reserve accumulation. Marine Ecology 40, e12547. doi: 10.1111/maec.12547.CrossRefGoogle Scholar
Bhattacharya, CG (1967) A simple method of resolution of a distribution into Gaussian components. Biometrics 23, 115135.CrossRefGoogle ScholarPubMed
Bianchini, A, Lauer, MM, Nery, LEM, Colares, EP, Monserrat, JM and dos Santos Filho, EA (2008) Biochemical and physiological adaptations in the estuarine crab Neohelice granulata during salinity acclimation. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 151, 423436.CrossRefGoogle ScholarPubMed
Botter-Carvalho, M, Santos, P and Carvalho, P (2007) Population dynamics of Callichirus major (Say, 1818) (Crustacea, Thalassinidea) on a beach in northeastern Brazil. Estuarine, Coastal and Shelf Science 71, 508516.CrossRefGoogle Scholar
Botto, F and Iribarne, O (2000) Contrasting effects of two burrowing crabs (Chasmagnathus granulata and Uca uruguayensis) on sediment composition and transport in estuarine environments. Estuarine Coastal and Shelf Science 51, 141151.CrossRefGoogle Scholar
Brockerhoff, AM and McLay, CL (2005) Mating behaviour, female receptivity and male-male competition in the intertidal crab Hemigrapsus sexdentatus (Brachyura: Grapsidae). Marine Ecology Progress Series 290, 179191.CrossRefGoogle Scholar
Brousseau, DJ, Filipowicz, A and Baglivo, JA (2001) Laboratory investigations of the effects of predator sex and size on prey selection by the Asian crab, Hemigrapsus sanguineus. Journal of Experimental Marine Biology and Ecology 262, 199210.CrossRefGoogle ScholarPubMed
Brylawski, BJ and Miller, TJ (2006) Temperature-dependent growth of the blue crab (Callinectes sapidus): a molt process approach. Canadian Journal of Fishery and Aquatic Sciences 63, 12981308.CrossRefGoogle Scholar
Cannicci, S, Fusi, M, Cimo, F, Dahdouh-Guebas, F and Fratini, S (2018) Interference competition as a key determinant for spatial distribution of mangrove crabs. Bmc Ecology 18, 8. doi: 10.1186/s12898-018-0164-1CrossRefGoogle ScholarPubMed
Carvalho-Batista, A, Pescinelli, RA, Garcia, JR, Guerra, PGM, Pardo, LM and Mantelatto, FL (2015) Crypsis in the mud crab Panopeus americanus saussure, 1857 (Decapoda, Panopeidae): relationship to sexual maturity. Crustaceana 88, 963977.CrossRefGoogle Scholar
Chan, BKK and Williams, GA (2004) Population dynamics of the acorn barnacles, Tetraclita squamosa and Tetraclita japonica (Cirripedia: Balanomorpha), in Hong Kong. Marine Biology 146, 149160.CrossRefGoogle Scholar
Chen, LH, Yang, JL and Barnes, MD (2014) Effect of natural disturbance on migrations and population dynamics of a catadromous species, Eriocheir japonicus, along the Lo-Mei stream in northern Taiwan. Hydrobiologia 726, 179194.CrossRefGoogle Scholar
Christy, JH (2007) Predation and the reproductive behavior of fiddler crabs (genus Uca). In Emmett Duffy, J. and Theil, M (eds), Evolutionary Ecology of Social and Sexual Systems. New York, NY: Oxford University Press, pp. 211231.CrossRefGoogle Scholar
Constabel, SA (1993) Ambientes sedimentarios de los estuarios Tubul y Raqui, VII región, Chile (Dissertation). Concepción (Chile): Universidad de Concepción.Google Scholar
Corotto, FS and Holliday, CW (1996) Branchial Na, K-ATPase and osmoregulation in the purple shore crab, Hemigrapsus nudus (Dana). Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 113, 361368.CrossRefGoogle Scholar
Datry, T, Larned, ST, Fritz, KM, Bogan, MT, Wood, PJ, Meyer, EI and Santos, AN (2014) Broad-scale patterns of invertebrate richness and community composition in temporary rivers: effects of flow intermittence. Ecography 37, 94104.CrossRefGoogle Scholar
Díaz-Jaramillo, M, Ferreira, JL, Amado, LL, Ventura-Lima, J, Martins, A, Retamal, MR, Urrutia, R, Bertran, C, Barra, R and Monserrat, JM (2010) Biomonitoring of antioxidant and oxidative stress responses in Perinereis gualpensis (Polychaeta: Nereididae) in Chilean estuarine regions under different anthropogenic pressure. Ecotoxicology and Environmental Safety 73, 515523.CrossRefGoogle ScholarPubMed
Eggleston, DB, Millstein, E and Plaia, G (2015) Timing and route of migration of mature female blue crabs in a tidal estuary. Biology Letters 115, 20140936 doi: 10.1098/rsbl.2014.0936Google Scholar
Gayanilo, FC Jr, Sparre, P and Pauly, D (2006) FAO-ICLARM Stock Assessment Tools II (FiSAT II). Revised version. User's guide. FAO Computerized Information Series (Fisheries) No. 8. Rome: FAO.Google Scholar
Grabowski, JH, Hughes, AR and Kimbro, DL (2008) Habitat complexity influences cascading effects of multiple predators. Ecology 89, 34133422.CrossRefGoogle ScholarPubMed
Hartnoll, RG (2001) Growth in Crustacea – twenty years on. Hydrobiologia 449, 111122.CrossRefGoogle Scholar
Haye, PA and Ojeda, FP (1998) Metabolic and behavioral alterations in the crab Hemigrapsus crenulatus (Milne-Edwards 1837) induced by its acanthocephalan parasite Profilicollis antarcticus (Zdzitowiecki 1985). Journal of Experimental Marine Biology and Ecology 228, 7382.CrossRefGoogle Scholar
Hulathduwa, YD, Stickle, WB, Aronhime, B and Brown, KM (2011) Differences in refuge use are related to predation risk in estuarine crabs. Journal of Shellfish Research 30, 949956.CrossRefGoogle Scholar
Johnson, PTJ (2003) Biased sex ratios in fiddler crabs (Brachyura, Ocypodidae): a review and evaluation of the influence of sampling method, size class, and sex-specific mortality. Crustaceana 76, 559580.CrossRefGoogle Scholar
Julian, P and Osborne, TZ (2018) From lake to estuary, the tale of two waters: a study of aquatic continuum biogeochemistry. Environmental Monitoring and Assessment 190, 22.CrossRefGoogle ScholarPubMed
Kerner, M (2007) Effects of deepening the Elbe estuary on sediment regime and water quality. Estuarine Coastal and Shelf Science 75, 492500.CrossRefGoogle Scholar
Kim, AKA and O'Connor, NJ (2007) Early stages of the Asian shore crab Hemigrapsus sanguineus as potential prey for the striped killifish Fundulus majalis. Journal of Experimental Marine Biology and Ecology 346, 2835.CrossRefGoogle Scholar
Kirkwood, G, Aukland, R and Zara, S (2001) Length Frequency Distribution Analysis (LFDA), Version 5.0. London: MRAG Ltd.Google Scholar
Koolkalya, S, Thapanand, T, Tunkijjanujij, S, Havanont, V and Jutagate, T (2006) Aspects in spawning biology and migration of the mud crab Scylla olivacea in the Andaman Sea, Thailand. Fisheries Management Ecology 13, 391397.CrossRefGoogle Scholar
Kristensen, E (2008) Mangrove crabs as ecosystem engineers; with emphasis on sediment processes. Journal of Sea Research 59, 3043.CrossRefGoogle Scholar
Lagos, M, Caceres, CW and Lardies, MA (2014) Geographic variation in acid-base balance of the intertidal crustacean Cyclograpsus cinereus (Decapoda, Grapsidae) during air exposure. Journal of the Marine Biological Association of the United Kingdom 94, 159165.CrossRefGoogle Scholar
Landaeta, MF and Castro, LR (2006) Spawning and larval survival of the Chilean hake Merluccius gayi under later summer conditions in the Gulf of Arauco, central Chile, Fisheries Research 77, 115121. doi: 10.1016/j.fishres.2005.08.006.CrossRefGoogle Scholar
Lardies, MA, Rojas, JM and Wehrtmann, IS (2004) Breeding biology and population structure of the intertidal crab Petrolisthes laevigatus (Anomura: Porcellanidae) in central-southern Chile. Journal of Natural History 38, 375388.CrossRefGoogle Scholar
Leme, MHD and Negreiros-Fransozo, ML (1998) Reproductive patterns of Aratus pisonii (Decapoda: Grapsidae) from an estuarine area of Sao Paulo Northern Coast, Brazil. Revista de Biologia Tropical 46, 673678.Google Scholar
Luppi, TA, Spivak, ED, Bas, CC and Anger, K (2004) Molt and growth of an estuarine crab, Chasmagnathus granulatus (Brachyura: Varunidae), in Mar Chiquita coastal lagoon, Argentina. Journal of Applied Ichthyology 20, 333344.CrossRefGoogle Scholar
Luppi, T, Bas, C, Méndez-Casariego, A, Albano, M, Lancia, J, Kittlein, M, Rosenthal, A, Farías, N, Spivak, E and Iribarne, O (2013) Variations in activity patterns in the estuarine crab Neohelice ( = Chasmagnathus) granulata in different habitats, seasons and tidal regimen. Helgoland Marine Research 67, 115.CrossRefGoogle Scholar
Martinetto, P, Montemayor, DI, Alberti, J, Costa, CSB and Iribarne, O (2016) Crab bioturbation and herbivory may account for variability in carbon sequestration and stocks in South West Atlantic salt marshes. Frontiers in Marine Science 3, 122.CrossRefGoogle Scholar
McLay, CL, Hinnendael, F, Lavery, S and Riquelme-Bugueno, R (2011) Morphological and molecular comparison of Hemigrapsus crenulatus (Milne Edwards, 1837) (Brachyura: Varunidae) from New Zealand and Chile: was Miss Rathbun right? Journal of Crustacean Biology 31, 582589.CrossRefGoogle Scholar
Miyajima, A and Wada, K (2017) Relationships between life history traits and sexual dimorphisms in two varunid crabs, Hemigrapsus takanoi Asakura & Watanabe, 2005 and H. sinensis Rathbun, 1931 (Brachyura: Varunidae). Journal of Crustacean Biology 37, 2128.CrossRefGoogle Scholar
Moksnes, P-O (2004) Self-regulating mechanisms in cannibalistic populations of juvenile shore crabs Carcinus maenas. Ecology 85, 13431354.CrossRefGoogle Scholar
Montagna, PA, Hu, XP, Palmer, TA and Wetz, M (2018) Effect of hydrological variability on the biogeochemistry of estuaries across a regional climatic gradient. Limnology and Oceanography 63, 24652478.CrossRefGoogle Scholar
Moscoso, J, Rudolph, A, Sepúlveda, RD and Suárez, C (2006) Effect of temporary closure of the mouth of an estuary on the benthic macroinfauna: Lenga, Chile: a case study. Bulletin of Environmental Contamination and Toxicology 77, 484491.CrossRefGoogle ScholarPubMed
Munro, JL and Pauly, D (1983) A simple method for comparing the growth of fishes and invertebrates. Fishbyte 1, 56.Google Scholar
Murrell, MC, Caffrey, JM, Marcovich, DT, Beck, MW, Jarvis, BM and Hagy, JD (2018) Seasonal oxygen dynamics in a warm temperate estuary: effects of hydrologic variability on measurements of primary production, respiration, and net metabolism. Estuaries and Coasts 41, 690707.CrossRefGoogle Scholar
Nelson, K (1991) Scheduling of reproduction in relation to moulting and growth in malacostracan crustaceans. In Wenner A and Kuris A (eds), Crustacean Egg Production. Rotterdam: A. A. Balkema, pp. 7116.Google Scholar
Pauly, D (1987) A review of the ELEFAN system for analysis of length-frequency data in fish and aquatic vertebrates. In Pauly, D and Morgan, GR (eds), Length-based Methods in Fisheries Research. Safat, Kuwait: ICLARM, Manila, Philippines and KISR, pp. 734.Google Scholar
Poore, AGB, Campbell, AH, Coleman, RA, Edgar, GJ, Jormalainen, V, Reynolds, PL, Sotka, EE, Stachowicz, JJ, Taylor, RB, Vanderklift, MA and Duffy, E (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecology Letters 15, 912922.CrossRefGoogle ScholarPubMed
Posey, MH, Alphin, TD, Harwell, H and Allen, B (2005) Importance of low salinity areas for juvenile blue crabs, Callinectes sapidus Rathbun, in river-dominated estuaries of southeastern United States. Journal of Experimental Marine Biology and Ecology 319, 81100.CrossRefGoogle Scholar
Potter, IC, Tweedley, JR, Elliott, M and Whitfield, AK (2015) The ways in which fish use estuaries: a refinement and expansion of the guild approach. Fish and Fishery 16, 230239.CrossRefGoogle Scholar
Pozo, K, Perra, G, Menchi, V, Urrutia, R, Parra, O, Rudolph, A and Focardi, S (2011) Levels and spatial distribution of polycyclic aromatic hydrocarbons (PAHs) in sediments from Lenga Estuary, central Chile. Marine Pollution Bulletin 62, 15721576.CrossRefGoogle Scholar
Retamal, M (1969) Hemigrapsus crenulatus (H. Milne Edwards, 1837) en el estero Lenga (Crustacea, Decapoda, Grapsidae). Boletín de la Sociedad de Biología de Concepción 41, 281307.Google Scholar
Retamal, MA (1981) Catalogo ilustrado de los Crustáceos Decápodos de Chile. Gayana, (Zool.) 44, 1110.Google Scholar
Retamal, MA and Moyano, HI (2010) Zoogeografía de los crustáceos decápodos chilenos marinos y dulceacuícola. Latin American Journal of Aquatic Research 38, 302328.Google Scholar
Riquelme-Bugueño, R (2006) Incidence patterns of limb autotomy in the estuarine crab, Hemigrapsus crenulatus (H. Milne Edwards, 1837) (Brachyura, Grapsoidea) from a temperate estuary in the eastern South Pacific. Crustaceana 79, 925932.CrossRefGoogle Scholar
Schultz, DA and Shirley, TC (1997) Feeding, foraging and starvation capability of ovigerous Dungeness crabs in laboratory conditions. Crustacean Research 26, 2637.CrossRefGoogle Scholar
Sicurella, B, Musitelli, F, Rubolini, D, Saino, N and Ambrosini, R (2016) Environmental conditions at arrival to the wintering grounds and during spring migration affect population dynamics of barn swallows Hirundo rustica breeding in Northern Italy. Population Ecology 58, 135145.CrossRefGoogle Scholar
Silva, CC, Schwamborn, R and Oliveira, JEL (2014) Population biology and color patterns of the blue land crab, Cardisoma guanhumi (Latreille 1828) (Crustacea: Gecarcinidae) in Northeastern Brazil. Brazilian Journal of Biology 74, 949958.CrossRefGoogle Scholar
Sokal, R and Rohlf, F (1997) Biometry. The Principles and Practice of Statistics by Biological Research, 3rd Edn. New York, NY: W.H. Freeman and Co.Google Scholar
Spivak, E, Anger, K, Luppi, T, Bas, C and Ismael, D (1994) Distribution and habitat preferences of 2 grapsid crab species in Mar-Chiquita lagoon (province of Buenos-Aires, Argentina). Helgolander Meeresuntersuchungen 48, 5978.CrossRefGoogle Scholar
Spivak, E, Bas, C and Luppi, T (2016) Great unexpected differences between two populations of the intertidal crab Neohelice granulata inhabiting close but contrasting habitats (Crustacea: Decapoda: Brachyura). Zoologia 33, e20160020. doi: 10.1590/ s1984–4689z ool-20160020.CrossRefGoogle Scholar
Stuardo, J, Valdovinos, C, Figueroa, R and Occhipinti, A (1993) Los ambientes costeros del Golfo de Arauco y áreas adyacentes. In Faranda F and Parra O (eds), Monografía Científica No 9. EULA. Universidad de Concepción.Google Scholar
Tankersley, RA, Wieber, MG, Sigala, MA and Kachurak, KA (1998) Migratory behavior of ovigerous blue crabs Callinectes sapidus: evidence for selective tidal-stream transport. Biological Bulletin 195, 168173.CrossRefGoogle ScholarPubMed
Taylor, HH and Seneviratna, D (2005) Ontogeny of salinity tolerance and hyper-osmoregulation by embryos of the intertidal crabs Hemigrapsus edwardsii and Hemigrapsus crenulatus (Decapoda, Grapsidae): survival of acute hyposaline exposure. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 140, 495505.CrossRefGoogle ScholarPubMed
Theuerkauff, D, Rivera-Ingraham, GA, Roques, JAC, Azzopardi, L, Bertini, M, Lejeune, M, Farcy, E, Lignot, J and Sucré, E (2018) Salinity variation in a mangrove ecosystem: a physiological investigation to assess potential consequences of salinity disturbances on mangrove crabs. Zoological Studies 57, 36.Google Scholar
Urbina, M, Paschke, K, Gebauer, P and Chaparro, OR (2010) Physiological energetics of the estuarine crab Hemigrapsus crenulatus (Crustacea: Decapoda: Varunidae): responses to different salinity levels. Journal of the Marine Biological Association of the United Kingdom 90, 267273.CrossRefGoogle Scholar
Urzua, A and Urbina, MA (2017) Ecophysiological adaptations to variable salinity environments in the crab Hemigrapsus crenulatus from the Southeastern Pacific coast: sodium regulation, respiration and excretion. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 210, 3543.CrossRefGoogle ScholarPubMed
Urzua, A, Bascur, M, Guzman, F and Urbina, M (2018) Carry-over effects modulated by salinity during the early ontogeny of the euryhaline crab Hemigrapsus crenulatus from the Southeastern Pacific coast: development time and carbon and energy content of offspring. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 217, 5562.CrossRefGoogle ScholarPubMed
Valdovinos, C, Sandoval, N, Vasquez, D and Olmos, V (2017) The Tubul-Raqui coastal wetland: a Chilean ecosystem of high conservation value severely disturbed by the 2010 earthquake. In Fariña, J and Camaño, A (eds), The Ecology and Natural History of Chilean Saltmarshes. Cham: Springer, pp. 293–327.Google Scholar
Valle-Levinson, A, Atkinson, LP, Figueroa, D and Castro, L (2003) Flow induced by upwelling winds in an equatorward facing bay: Gulf of Arauco, Chile. Journal of Geophysical Research-Oceans 108, 3054.CrossRefGoogle Scholar
Vega-Aguayo, R, Figueroa-Munoz, G, Retamal, MA and De los Rios, P (2018) Spatial distribution and abundance of Hemigrapsus crenulatus (H. Milne Edwards, 1837) (Decapoda, Varunidae) in the Puerto Cisnes estuary (44°S, Aysen region, Chile). Crustaceana 91, 14651482.CrossRefGoogle Scholar
Vina, N, Bascur, M, Guzman, F, Riera, R, Paschke, K and Urzua, A (2018) Interspecific variation in the physiological and reproductive parameters of porcelain crabs from the Southeastern Pacific coast: potential adaptation in contrasting marine environments. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 226, 2231.CrossRefGoogle ScholarPubMed
Von Bertalanffy, L (1938) A quantitative theory of organic growth. Human Biology 10, 181213.Google Scholar
Waiho, K, Mustaqim, M, Fazhan, H, Norfaizza, WIW, Megat, FH and Ikhwanuddin, M (2015) Mating behaviour of the orange mud crab, Scylla olivacea: the effect of sex ratio and stocking density on mating success. Aquaculture Report 2, 5057.CrossRefGoogle Scholar
Warman, CG, Reid, DG and Naylor, E (1993) Variation in the tidal migratory behavior and rhythmic light-responsiveness in the shore crab, Carcinus maenas. Journal of the Marine Biological Association of the United Kingdom 73, 355364.CrossRefGoogle Scholar
Wenner, AM (1972) Sex ratio as a function of size in marine crustacea. American Naturalist 106, 321350.CrossRefGoogle Scholar
Zar, JH (1999) Biostatistical Analysis, 4th Edn. Englewood Cliffs, NJ: Prentice-Hall.Google Scholar