Aggregations and reproductive events of the narrownose smooth-hound shark (Mustelus schmitti) in relation to temperature and depth in coastal waters of the south-western Atlantic Ocean (38–42°S)
Mariano Elisio A B E , Jorge H. Colonello A , Federico Cortés A , Andrés J. Jaureguizar A C , Gustavo M. Somoza B D and Gustavo J. Macchi A B
+ Author Affiliations
- Author Affiliations
A Instituto Nacional de Investigación y Desarrollo Pesquero, Mar del Plata, Argentina.
B Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina.
C Comisión de Investigaciones Científicas de la Provincia de Buenos Aires, La Plata, Argentina.
D Laboratorio de Ictiofisiología y Acuicultura, Instituto de Investigaciones Biotecnológicas – Instituto Tecnológico de Chascomús (CONICET-UNSAM), Chascomús, Argentina.
E Corresponding author. Email: melisio@inidep.edu.ar
Marine and Freshwater Research 68(4) 732-742 https://doi.org/10.1071/MF15253
Submitted: 4 July 2015 Accepted: 8 March 2016 Published: 20 June 2016
Abstract
Knowledge of environmental influence on reproductive dynamics in chondrichthyans is critical for effective management. The present study assessed the potential influences of temperature and depth on aggregations and reproductive events of the narrownose smooth-hound shark (Mustelus schmitti), using an analysis criterion based on the co-occurrence of different reproductive stages. Data were collected from 363 sample sites during six research surveys, covering an area of ~47 744 km2 along the coast (38–42°S, depth of <50 m). Aggregations of M. schmitti adults were mostly associated with the warmer spring surveys, with the aggregation sites being significantly warmer than those of non-aggregation. Evidence of pupping and ovulation was observed, almost simultaneously, during all spring surveys. However, the occurrence of these reproductive events showed a clear interannual variability pattern that was significantly explained by water temperature. Particularly, the occurrence of ovulation was associated with temperatures above 16–17°C. These results suggest that M. schmitti adults may follow the warming gradient along the environment and, thus, they aggregate in shallow and productive waters during the course of spring. Their reproductive events could be induced by temperature increase. This scenario suggests that changes in the patterns of bottom temperature may be important drivers of the reproductive dynamics of M. schmitti.
Additional keywords: coastal ecosystem, elasmobranchs, environmental cues, reproductive aggregations.
References
Alverson, D., and Pereyra, W. (1969). A study of demersal fishes and fisheries of the northeastern Pacific Ocean. An evaluation of exploratory fishing methods and analytical approaches to stock size and yield forecast. Journal of the Fisheries Research Board of Canada 26, 1985–2001.| A study of demersal fishes and fisheries of the northeastern Pacific Ocean. An evaluation of exploratory fishing methods and analytical approaches to stock size and yield forecast.Crossref | GoogleScholarGoogle Scholar |
Bres, M. (1993). The behaviour of sharks. Reviews in Fish Biology and Fisheries 3, 133–159.
| The behaviour of sharks.Crossref | GoogleScholarGoogle Scholar |
Carlisle, A. C., and Starr, R. M. (2009). Habitat use, residency, and seasonal distribution of female leopard sharks Triakis semifasciata in Elkhorn Slough, California. Marine Ecology Progress Series 380, 213–228.
| Habitat use, residency, and seasonal distribution of female leopard sharks Triakis semifasciata in Elkhorn Slough, California.Crossref | GoogleScholarGoogle Scholar |
Casterlin, M. E., and Reynolds, W. W. (1979). Shark thermoregulation. Comparative Biochemistry and Physiology. A. Comparative Physiology 64, 451–453.
| Shark thermoregulation.Crossref | GoogleScholarGoogle Scholar |
Colautti, D., Baigun, C., Lopez Cazorla, A., Llompart, F., Molina, J. M., Suquele, P., and Calvo, S. (2010). Population biology and fishery characteristics of the smooth-hound Mustelus schmitti in Anegada Bay, Argentina. Fisheries Research 106, 351–357.
| Population biology and fishery characteristics of the smooth-hound Mustelus schmitti in Anegada Bay, Argentina.Crossref | GoogleScholarGoogle Scholar |
Collins, A. B., Heupel, M. R., and Motta, P. J. (2007). Residence and movement patterns of cownose rays Rhinoptera bonasus within a south-west Florida estuary. Journal of Fish Biology 71, 1159–1178.
| Residence and movement patterns of cownose rays Rhinoptera bonasus within a south-west Florida estuary.Crossref | GoogleScholarGoogle Scholar |
Colonello, J. H., Lucifora, L. O., and Massa, A. M. (2007a). Reproduction of the angular angel shark (Squatina guggenheim): geographic differences, reproductive cycle, and sexual dimorphism. ICES Journal of Marine Science 64, 131–140.
Colonello, J. H., Christiansen, E. H., and Macchi, G. J. (2007b). Escala de madurez sexual para peces cartilaginosos de la Plataforma Continental Argentina. Technical report of the National Institute for Fisheries Research and Development number 74, Mar del Plata, Argentina.
Colonello, J. H., Cortés, F., and Massa, A. M. (2014). Species richness and reproductive modes of chondrichthyans in relation to temperature and fishing effort in the southwestern Atlantic Shelf (34–54°S). Fisheries Research 160, 8–17.
| Species richness and reproductive modes of chondrichthyans in relation to temperature and fishing effort in the southwestern Atlantic Shelf (34–54°S).Crossref | GoogleScholarGoogle Scholar |
Conrath, C. L., and Musick, J. A. (2002). Reproductive biology of the smooth dogfish, Mustelus canis, in the northwest Atlantic Ocean. Environmental Biology of Fishes 64, 367–377.
| Reproductive biology of the smooth dogfish, Mustelus canis, in the northwest Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |
Cortés, E. (2000). Life history patterns and correlations in sharks. Reviews in Fisheries Science 8, 299–344.
| Life history patterns and correlations in sharks.Crossref | GoogleScholarGoogle Scholar |
Cortés, F. (2007). Sustentabilidad de la explotación de gatuzo, Mustelus schmitti, en el ecosistema costero bonaerense. M.Sc. Thesis, National University of Mar del Plata, Argentina.
Cortés, E. (2012). Hábitats esenciales de condrictios (Chondrichthyes) costeros, y su relación con los procesos oceanográficos. Ph.D. Thesis, National University of Mar del Plata, Argentina.
Cortés, F., Jaureguizar, A. J., Menni, R. C., and Guerrero, R. A. (2011). Ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in two southwestern Atlantic coastal areas. Hydrobiologia 661, 445–456.
| Ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in two southwestern Atlantic coastal areas.Crossref | GoogleScholarGoogle Scholar |
Cousseau, M. B. (1986). Estudios biológicos sobre peces costeros con datos de dos campañas de investigación realizadas en 1981 VI. El gatuzo (Mustelus schmitti). Publicaciones de la Comisión Técnica Mixta del Frente Marítimo 1, 60–65.
Cousseau, M. B., Carozza, C. R., and Macchi, G. J. (1998). Abundancia, reproducción y distribución de tallas del gatuzo (Mustelus schmitti). Resultados de una campaña de evaluación de recursos demersales costeros de la provincia de Buenos Aires y del litoral uruguayo: noviembre, 1994. Technical report of the National Institute for Fisheries Research and Development number 21, Mar del Plata, Argentina.
Crawshaw, L. I., and Hammel, H. T. (1973). Behavioral temperature regulation in the California horn shark, Heterodontus francisci. Brain, Behavior and Evolution 7, 447–452.
| Behavioral temperature regulation in the California horn shark, Heterodontus francisci.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2c%2FjtVCntQ%3D%3D&md5=1379071d1d57512bc586966e99a7b178CAS | 4752795PubMed |
Di Santo, V., and Bennett, W. A. (2011). Is post-feeding thermotaxis advantageous for elasmobranch fishes? Journal of Fish Biology 78, 195–207.
| Is post-feeding thermotaxis advantageous for elasmobranch fishes?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7hslykug%3D%3D&md5=f595e811038e9c0d9f3eac71243969b6CAS | 21235555PubMed |
Dobson, S., and Dodd, J. M. (1977). The roles of temperature and photoperiod in the response of the testis of the dogfish, Scyliorhinus canicula L. to partial hypophysectomy (ventral lobectomy). General and Comparative Endocrinology 32, 114–115.
| The roles of temperature and photoperiod in the response of the testis of the dogfish, Scyliorhinus canicula L. to partial hypophysectomy (ventral lobectomy).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE2s7os1aguw%3D%3D&md5=6a06f6647b1c0b8618ee959e3362d4ceCAS | 863219PubMed |
Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L. N. K., Fordham, S. V., Francis, M. P., Pollock, C. M., Simpfendorfer, C. A., Burgess, G. H., Carpenter, K. E., Compagno, L. J. V., Ebert, D. A., Gibson, C., Heupel, M. R., Livingstone, S. R., Sanciangco, J. C., Stevens, J. D., Valenti, S., and White, W. T. (2014). Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590.
| Extinction risk and conservation of the world’s sharks and rays.Crossref | GoogleScholarGoogle Scholar | 24448405PubMed |
Economakis, A. E., and Lobel, P. S. (1998). Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, central Pacific Ocean. Environmental Biology of Fishes 51, 129–139.
| Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, central Pacific Ocean.Crossref | GoogleScholarGoogle Scholar |
Espinoza, M., Farrugia, T. J., and Lowe, C. G. (2011). Habitat use, movements and site fidelity of the gray smooth-hound shark (Mustelus californicus Gill 1863) in a newly restored southern California estuary. Journal of Experimental Marine Biology and Ecology 401, 63–74.
| Habitat use, movements and site fidelity of the gray smooth-hound shark (Mustelus californicus Gill 1863) in a newly restored southern California estuary.Crossref | GoogleScholarGoogle Scholar |
Francis, M. P. (1988). Movement patterns of rig (Mustelus lenticulatus) tagged in southern New Zealand. New Zealand Journal of Marine and Freshwater Research 22, 259–272.
| Movement patterns of rig (Mustelus lenticulatus) tagged in southern New Zealand.Crossref | GoogleScholarGoogle Scholar |
Francis, M. P., and Mace, J. M. (1980). Reproductive biology of Mustelus lenticulatus from Kaikoura and Nelson. New Zealand Journal of Marine and Freshwater Research 14, 303–311.
| Reproductive biology of Mustelus lenticulatus from Kaikoura and Nelson.Crossref | GoogleScholarGoogle Scholar |
Hall, S. J. (2009). Area and time restrictions. In ‘Fishery Manager’s Guidebook’, 2nd edn. (Eds K. L. Cochrane and S. M. Garcia.) pp. 196–219. (FAO: Rome; and Wiley-Blackwell: Oxford, UK.)
Heupel, M. R., Whittier, J. M., and Bennett, M. B. (1999). Plasma steroid hormone profiles and reproductive biology of the epaulette shark, Hemiscyllium ocellatum. The Journal of Experimental Zoology 284, 586–594.
| Plasma steroid hormone profiles and reproductive biology of the epaulette shark, Hemiscyllium ocellatum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt1Sjt7Y%3D&md5=8fc7e51de7e13fec66287fba949d2ac4CAS | 10469996PubMed |
Hight, B. V., and Lowe, C. G. (2007). Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence for behavioural thermoregulation? Journal of Experimental Marine Biology and Ecology 352, 114–128.
| Elevated body temperatures of adult female leopard sharks, Triakis semifasciata, while aggregating in shallow nearshore embayments: evidence for behavioural thermoregulation?Crossref | GoogleScholarGoogle Scholar |
Hopkins, T. E., and Cech, J. J. (2003). The influence of environmental variables on the distribution and abundance of three elasmobranchs in Tomales Bay, California. Environmental Biology of Fishes 66, 279–291.
| The influence of environmental variables on the distribution and abundance of three elasmobranchs in Tomales Bay, California.Crossref | GoogleScholarGoogle Scholar |
Hozbor, N., and Massa, A. M. (2008). Distribución espacio-temporal de condrictios en la zona común de pesca Argentino Uruguaya. Technical report of the National Institute for Fisheries Research and Development number 2, Mar del Plata, Argentina.
Jacoby, D. M. P., Darren, P., Croft, D. P., and Sims, D. W. (2012). Social behaviour in sharks and rays: analysis, patterns and implications for conservation. Fish and Fisheries 13, 399–417.
| Social behaviour in sharks and rays: analysis, patterns and implications for conservation.Crossref | GoogleScholarGoogle Scholar |
Jaureguizar, A., Menni, R., Guerrero, R., and Lasta, C. (2004). Environmental factors structuring fish communities of the Rio de la Plata estuary. Fisheries Research 66, 195–211.
| Environmental factors structuring fish communities of the Rio de la Plata estuary.Crossref | GoogleScholarGoogle Scholar |
Jirik, K. E., and Lowe, C. G. (2012). Anelasmobranch maternityward: female round stingrays Urobatis halleri use warm, restored estuarine habitat during gestation. Journal of Fish Biology 80, 1227–1245.
| Anelasmobranch maternityward: female round stingrays Urobatis halleri use warm, restored estuarine habitat during gestation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38rksVOrsA%3D%3D&md5=a75f56b4ced68665a0869bea89fb4bceCAS | 22497381PubMed |
Lucifora, O. L., Menni, R. C., and Escalante, A. H. (2002). Reproductive ecology and abundance of the sand tiger shark, Carcharias taurus, from the southwestern Atlantic. ICES Journal of Marine Science 59, 553–561.
| Reproductive ecology and abundance of the sand tiger shark, Carcharias taurus, from the southwestern Atlantic.Crossref | GoogleScholarGoogle Scholar |
Lucifora, O. L., Menni, R. C., and Escalante, A. H. (2004). Reproductive biology of the school shark, Galeorhinus galeus, off Argentina: support for a single south western Atlantic population with synchronized migratory movements. Environmental Biology of Fishes 71, 199–209.
| Reproductive biology of the school shark, Galeorhinus galeus, off Argentina: support for a single south western Atlantic population with synchronized migratory movements.Crossref | GoogleScholarGoogle Scholar |
Lucifora, O. L., Menni, R. C., and Escalante, A. H. (2005). Reproduction and seasonal occurrence of the copper shark, Carcharhinus brachyurus, from north Patagonia, Argentina. ICES Journal of Marine Science 62, 107–115.
| Reproduction and seasonal occurrence of the copper shark, Carcharhinus brachyurus, from north Patagonia, Argentina.Crossref | GoogleScholarGoogle Scholar |
Mabragaña, E. M., Lucifora, L. O., and Massa, A. M. (2002). The reproductive ecology and abundance of Sympterygia bonapartii endemic to the south-west Atlantic. Journal of Fish Biology 60, 951–967.
Massa, A. M. (1998). Estructura poblacional del gatuzo (Mustelus schmitti) en la costa bonaerense y uruguaya asociado a condiciones ambientales. M.Sc. Thesis, Nationa University of Mar del Plata, Argentina.
Massa, A. M., Lucifora, L. O., and Hozbor, N. M. (2004a). Condrictios de la región costera bonaerense y uruguaya. In ‘El Mar Argentino y Sus Recursos Pesqueros. Los Peces Marinos de Interés Pesquero. Caracterización Biológica y Evaluación del Estado de Explotación’. (Eds E. E. Boschi.) pp. 85–99. (INIDEP: Buenos Aires, Argentina.)
Massa, A. M., Lasta, C., and Carozza, C. (2004b). Estado actual y explotación del gatuzo (Mustelus schmitti). In ‘El Mar Argentino y Sus Recursos Pesqueros. Los Peces Marinos de Interés Pesquero. Caracterización Biológica y Evaluación del Estado de Explotación’. (Eds E. E. Boschi.) pp. 67–83 (INIDEP: Buenos Aires, Argentina.)
Massa, A. M., Hozbor, N., Chiaramonte, G. E., Balestra, A. D., and Vooren, C. M. (2006). Mustelus schmitti (Narrownose Smoothhound). In ‘IUCN Red List of Threatened Species. Version 2010.3’. (Ed. IUCN2010.) Available at http://www.iucnredlist.org/details/60203/0 [Verified 31 May 2016].
Menni, C. R. (1985). Distribución y biología de Squalus acanthias, Mustelus schmitti y Galeorhinus vitaminicus en el Mar Argentino en agosto-septiembre de 1978 (Chondrichthyes). Revista del Museo de La Plata (Nueva Serie) – Sección Zoología 13, 151–182.
Menni, C. R., Cousseau, M. B., and Gosztonyi, A. E. (1986). Sobre la biología de los tiburones costeros de la Provincia de Buenos Aires. Anales de la Sociedad Científica Argentina 213, 3–26.
Menni, C. R., Jaureguizar, A. J., Stehmann, M. F. W., and Lucifora, L. O. (2010). Marine biodiversity at the community level: zoogeography of sharks, skates, rays and chimaeras in the southwestern Atlantic. Biodiversity and Conservation 19, 775–796.
| Marine biodiversity at the community level: zoogeography of sharks, skates, rays and chimaeras in the southwestern Atlantic.Crossref | GoogleScholarGoogle Scholar |
Mucientes, G. R., Queiroz, N., Sousa, L. L., Tarroso, P., and Sims, D. W. (2009). Sexual segregation of pelagic sharks and the potential threat from fisheries. Biology Letters 5, 156–159.
| Sexual segregation of pelagic sharks and the potential threat from fisheries.Crossref | GoogleScholarGoogle Scholar | 19324655PubMed |
Mull, C. G., Lowe, C. G., and Young, K. A. (2008). Photoperiod and water temperature regulation of seasonal reproduction in male round stingrays (Urobatis halleri). Comparative Biochemistry and Physiology. A. Comparative Physiology 151, 717–725.
| Photoperiod and water temperature regulation of seasonal reproduction in male round stingrays (Urobatis halleri).Crossref | GoogleScholarGoogle Scholar |
Mull, C. G., Lowe, C. G., and Young, K. A. (2010). Seasonal reproduction of female round stingrays (Urobatis halleri): steroid hormone profiles and assessing reproductive state. General and Comparative Endocrinology 166, 379–387.
| Seasonal reproduction of female round stingrays (Urobatis halleri): steroid hormone profiles and assessing reproductive state.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtVCgtbk%3D&md5=4fe1686e0460f88c8483f7ecc0466fcdCAS | 20015450PubMed |
Musick, J. A. (2005). Introduction: management of sharks and their relatives (Elasmobranchii). In ‘Management Techniques for Elasmobranch Fisheries’. (Eds J. A. Musick and R. Bonfil.) pp. 1–5. (FAO: Rome.)
Oddone, M. C., Paesch, L., and Norbis, W. (2005). Reproductive biology and seasonal distribution of Mustelus schmitti (Elasmobranchii: Triakidae) in the Rio de la Plata oceanic front, south-western Atlantic. Journal of the Marine Biological Association of the United Kingdom 85, 1193–1198.
| Reproductive biology and seasonal distribution of Mustelus schmitti (Elasmobranchii: Triakidae) in the Rio de la Plata oceanic front, south-western Atlantic.Crossref | GoogleScholarGoogle Scholar |
Oddone, M. C., Paesch, L., Norbis, W., and Velasco, G. (2007). Population structure, distribution and abundance patterns of the Patagonian smoothhound Mustelus schmitti Springer, 1939. (Chondrichthyes, Elasmobranchii, Triakidae) in the Rio de la Plata and inner continental shelf, SWAtlantic ocean (34°30′–39°30′S). Brazilian Journal of Oceanography 55, 167–177.
| Population structure, distribution and abundance patterns of the Patagonian smoothhound Mustelus schmitti Springer, 1939. (Chondrichthyes, Elasmobranchii, Triakidae) in the Rio de la Plata and inner continental shelf, SWAtlantic ocean (34°30′–39°30′S).Crossref | GoogleScholarGoogle Scholar |
Pereyra, I., Orlando, L., Norbis, W., and Paesch, L. (2008). Variación espacial y temporal de la composición por tallas y sexos del gatuso Mustelus schmitti Springer, 1939 capturado por la pesca de arrastre en la costa oceánica uruguaya durante 2004. Revista de Biología Marina y Oceanografía 43, 159–166.
Robbins, R. L. (2007). Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands South Australia. Journal of Fish Biology 70, 1350–1364.
| Environmental variables affecting the sexual segregation of great white sharks Carcharodon carcharias at the Neptune Islands South Australia.Crossref | GoogleScholarGoogle Scholar |
Schlaff, A. M., Heupel, M. R., and Simpfendorfer, C. A. (2014). Influence of environmental factors on shark and ray movement, behaviour and habitat use: a review. Reviews in Fish Biology and Fisheries 24, 1089–1103.
| Influence of environmental factors on shark and ray movement, behaviour and habitat use: a review.Crossref | GoogleScholarGoogle Scholar |
Schwartz, F. J. (1990). Mass migratory congregations and movements of several species of cownose rays, genus Rhinoptera: a world-wide review. The Journal of the Elisha Mitchell Scientific Society 106, 10–13.
Snelson, F. F., Williams-Hooper, S. E., and Schmid, T. H. (1988). Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 1988, 729–739.
| Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons.Crossref | GoogleScholarGoogle Scholar |
Speed, C. W., Field, I. C., Meekan, M. G., and Bradshaw, C. J. A. (2010). Complexities of coastal shark movements and their implications for management. Marine Ecology Progress Series 408, 275–293.
| Complexities of coastal shark movements and their implications for management.Crossref | GoogleScholarGoogle Scholar |
Speed, C. W., Meekan, M. G., Field, I. C., McMahon, C. R., and Bradshaw, C. J. A. (2012). Heat-seeking sharks: support for behavioural thermoregulation in reef sharks. Marine Ecology Progress Series 463, 231–244.
| Heat-seeking sharks: support for behavioural thermoregulation in reef sharks.Crossref | GoogleScholarGoogle Scholar |
Stevens, J. D., Bonfil, R., Dulvy, N. K., and Walker, P. A. (2000). The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57, 476–494.
| The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems.Crossref | GoogleScholarGoogle Scholar |
Vögler, R., Milessi, A. C., and Quiñones, R. A. (2008). Influence of environmental variables on the distribution of Squatina guggenheim (Chondrichthyes, Squatinidae) in the Argentine–Uruguayan common fishing zone. Fisheries Research 91, 212–221.
| Influence of environmental variables on the distribution of Squatina guggenheim (Chondrichthyes, Squatinidae) in the Argentine–Uruguayan common fishing zone.Crossref | GoogleScholarGoogle Scholar |
Wallman, H. L., and Bennett, W. A. (2006). Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina (Lesueur). Environmental Biology of Fishes 75, 259–267.
| Effects of parturition and feeding on thermal preference of Atlantic stingray, Dasyatis sabina (Lesueur).Crossref | GoogleScholarGoogle Scholar |
Waltrick, D., Jones, S. M., Simpfendorfer, C. A., and Awruch, C. A. (2014). Endocrine control of embryonic diapause in the Australian sharpnose shark Rhizoprionodon taylori. PLoS One 9, e101234.
| Endocrine control of embryonic diapause in the Australian sharpnose shark Rhizoprionodon taylori.Crossref | GoogleScholarGoogle Scholar | 24992673PubMed |
Wearmouth, V. J., and Sims, D. W. (2010). Sexual segregation in elasmobranchs. Biologia Marina Mediterranea 17, 236–239.
