Trophic assessment and isotopic niches of two congeneric pipefishes in a wetland of the Aegean Sea


SULE GURKAN
https://orcid.org/0000-0003-4365-4920
PAULA ARAGONESES
DENIZ INNAL
https://orcid.org/0000-0002-1686-0959
CLARA MENDOZA-SEGURA
https://orcid.org/0000-0002-0619-9917
MIQUEL PLANAS
https://orcid.org/0000-0003-1217-5716
Résumé

Pipefishes (family: Syngnathidae) are representative fishes in many European coastal areas associated with vegetal assemblages and other shallow habitats. The polyandrous pipefishes Syngnathus abaster and Syngnathus acus co-occur in Metruk Tuzla (Bargilya Tuzla coastal Wetland - BTW, Aegean Sea, Türkiye ‒a protected but threatened wetland due to anthropogenic disturbances. Both species were sampled to assess the growth and temporal changes on their trophic features using stable isotope (δ13C and δ15N) and gut content analyses. Both species exhibited positive allometric growth with similar length–weight relationships. The isotopic approach revealed that both species occupied similar trophic niches, as evidenced by comparable δ13C and δ15N values (-17.0‰ ± 1.2‰ and 13.2‰ ± 0.6‰, respectively in S. abaster; -17.3‰ ± 1.2‰ and 13.3‰ ± 0.7‰ respectively in S. acus). The niche area for all sex types (undifferentiated specimens, males and females) in S. acus was slightly broader than that in S. abaster. Simulation analysis of the trophic position in both species agreed with the isotopic assessment (trophic position = 3.67 ± 0.61 in S. abaster and 3.46 ± 0.66 in S. acus). Although the trophic positions were consistent with the isotopic assessment, gut content analysis disclosed a notable contribution of copepods, especially Calanipeda aquaedulcis, to the dietary regime in both species. Notably, the diet in S. abaster was nearly monospecific, whereas cladocerans were crucial in S. acus. This study suggests the plausible occurrence of interspecific competition regarding dietary resources. However, we hypothesise that such competition could be mitigated by the occupation of discrete microhabitats in both species. To validate this hypothesis, rigorous investigation and empirical analysis are necessary.

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Biographie de l'auteur
DENIZ INNAL, Mehmet Akif Ersoy University, Science and Art Faculty, Department of Biology, 15100 Burdur, Türkiye

ORCID id: 0000-0002-1686-0959

Références
Altınsaçlı, S., Perçin-Paçal, F., Altınsaçlı, S., 2015. Assessments on diversity, spatiotemporal distribution and ecology of the living ostracod species (Crustacea) in oligo-hypersaline coastal wetland of Bargilya (Milas, Muğla, Turkey). International Journal of Fisheries and Aquatic Studies, 3 (2), 357-373.
Anonymous, 2007. Gediz Delta Wetland Management Plan. T.R. Ministry of Environment and Forestry, General Directorate of Nature Conservation and National Parks, Department of Nature Conservation, Directorate of Wetlands Branch, 2007, 424 p. (in Turkish).
Boeuf, G., Payan, P., 2001. How should salinity influence fish growth? Comparative Biochemistry and Physiology Part C, 130 (4), 411-423.
Boix, D., Gascón, S., Sala, J., Martinoy, M., Gifre, J. et al., 2005. A new index of water quality assessment in Mediterranean wetlands based on crustacean and insect assemblages: the case of Catalunya (NE Iberian Peninsula). Aquatic Conservation: Marine and Freshwater Ecosystems, 15, 635-651.
Brucet, S., Compte, J., Boix, D., López-Flores, R., Quintana, X.D., 2008. Feeding of nauplii, copepodites and adults of Calanipeda aquaedulcis (Calanoida) in Mediterranean salt marshes. Marine Ecology-Progress Series, 355, 183-191.
Cakić, P.M., Lenhardt, D., Mićkovıć, N., Sekulıć, L., Budakov, J., 2002. Biometric analysis of Syngnathus abaster populations. Journal of Fish Biology, 60, 1562-1569.
Campolmi, M., Franzoi, P., Mazzola, A., 1996. Observations on pipefish (Syngnathidae) biology in the Stagnone lagoon (west Sicily). Publicaciones Especiales Instituto Espanol Oceanografia, 21, 205-209.
Cazzolla Gatti, R., 2011. Evolution is a cooperative process: the biodiversity-related niches differentiation theory (BNDT) can explain why. Theoretical Biology Forum, 104, 35-44. PMID: 22220353.
Cerim, H., 2017. Determination of some biological and population parameters of common sole (Solea solea Linnaeus, 1758) in Güllük Bay trammel net fishery. PhD Thesis dissertation, Muğla Sıtkı Koçman University, Muğla, Turkey, (in Turkish).
Cherry, J. A., 2011. Ecology of Wetland Ecosystems: Water, Substrate, and Life. Nature Education Knowledge, 3 (10), 16.
Chunco, A.J., Jobe, T., Pfennig, K.S., 2012. Why do species co-occur? A test of alternative hypotheses describing abiotic differences in sympatry versus allopatry using spadefoot toads. PLoS One, 7 (3), e32748.
Çolak, M.A., Öztaş, B., Özgencil, İ.K., Soyluer, M., Korkmaz, M. et al., 2022. Increased water abstraction and climate change have substantial effect on morphometry, salinity, and biotic communities in lakes: Examples from the semi-arid Burdur Basin (Turkey). Water, 14, 1241.
Cole, J.J., Carpenter, S.R., Kitchell, J., Weidel, B., 2020. Strong evidence for terrestrial support of zooplankton in small lakes based on stable isotopes of carbon, nitrogen, and hydrogen. Biological Sciences, 108 (5), 1975-1980.
Curebal, I., Efe, R., Soykan, A., Sonmez, S, 2015. Impacts of anthropogenic factors on land degradation during the Anthropocene in Turkey. Journal of Environmental Biology, 36 (1), 51-58.
Davis, T., Blasco, D., Carbonell, M., 1997. The Ramsar Convention manual: a guide to the Convention on wetlands (Ramsar, Iran, 1971). IUCN: International Union for Conservation of Nature, Gland, Switzerland, 161 pp.
Dawson, C.E., 1986a. Syngnathidae. p. 628-639. In: Fishes of the north-eastern Atlantic and the Mediterranean. Whitehead, P.J.P. (Ed). Unesco, Paris, France.
Dawson, C.E., 1986b. Syngnathidae. p. 628-639. In: Fishes of the North-eastern Atlantic and the Mediterranean Volume 2. Whitehead, P.J.P., Bauchot, M.-L., Hureau, J.-C., Nielsen, J., Tortonese. E. (Eds). Unesco, Paris.
de Lussanet M.H.E, Muller, M., 2007. The smaller your mouth, the longer your snout: predicting the snout length of Syngnathus acus, Centriscus scutatus and other pipette feeders. Journal of The Royal Society Interface, 4561-573.
Deegan, L.A., Peterson, B. J., Portier, R., 1990. Stable isotopes and cellulase activity as evidence for detritus as a food source for juvenile Gulf menhaden. Estuaries, 13, 14-19.
Demirak, A., Balcı, A., Demirhan, H., Tüfekçi, M., 2001. The reasons of the pollution in the Güllük Bay. p. 383-388. In: Proceedings of the 4th National Ecology and Environment Congress (in Turkish).
Demirak, A., Balci, A., Tüfekçi, M., 2006. Environmental impact of the marine aquaculture in Güllük Bay, Turkey. Environmental Monitoring and Assessment, 123 (1-3), 1-12.
Demirhindi, U., 1972. The preliminary planktonic investigations in the coastal lagoons and several brackish water lakes of Turkey. Istanbul Universitesi Fen Faktiltesi Mecmuasi, 37, 205-232.
Didenko, A., Kruzhylina, S., Gurbyk, A., 2018. Feeding patterns of the black-striped pipefish Syngnathus abaster in an invaded freshwater habitat. Environmental Biology of Fishes, 101, 917-931.
Franzoi, P.R., Maccagnani, R.R., Ceccherelli, V.U., 1993. Life cycles and feeding habits of Syngnathus taenionotus and Syngnathus abaster (Pisces, Syngnathidae) in brackish bay of the Po River delta (Adriatic Sea). Marine Ecology-Progress Series, 97, 71-81.
Fritzsche, R.A., 1980. Revision of the Eastern Pacific Syngnathidae (Pisces: Syngnathiformes), including both recent and fossil forms. Proceedings of the California Academy of Sciences, 42, 181-227.
Fry, B., 1988. Food web structure on Georges Bank from stable C, N and S isotopic compositions. Limnology and Oceanography, 33, 1182-1190.
Fry, B., Sherr, E.B., 1989. δ13C measurements as indicators of carbon flow in marine and freshwater ecosystems. p. 196- 229. In: Stable isotopes in ecological research. Springer New York, New York.
Garcia, E., Rice, C.A., Eernisse, D.J., Forsgren, K.L., Quimbayo, J.P., et al., 2019. Systematic relationships of sympatric pipefishes (Syngnathus spp.): A mismatch between morphological and molecular variation. Journal of Fish Biology, 95 (4), 999-1012.
Gürkan, Ş., Innal, D., 2018. Some morphometric features of congeneric pipefish species (Syngnathus abaster Risso 1826, Syngnathus acus Linnaeus, 1758) distributed in Lake Bafa (Turkey). Oceanological and Hydrobiological Studies, 47 (3), 239-247.
Gürkan, Ş., Innal, D., Gulle, I., 2021. Monitoring of the trophic ecology of pipefish species (Syngnathus abaster, Syngnathus acus) in an alluvial lake habitat (Lake Bafa, Turkey). Oceanological and Hydrobiological Studies, 50, 24-32.
Gürkan, Ş., Taşkavak, E., 2019. The relationships between gut length and prey preference of three pipefish (Syngnathus acus, Syngnathus typhle, Nerophis ophidion Linnaeus, 1758) species distributed in Aegean Sea, Turkey. Iranian Journal of Fisheries Sciences, 18, 1093-1100.
Gürkan, Ş., Taşkavak, E., Hoşsucu, B., 2009. The reproductive biology of the Great Pipefish Syngnathus acus (Family: Syngnathidae) in the Aegean Sea. North-Western Journal of Zoology, 5 (1), 179-190.
Hobson, K.A., Ambrose, Jr.W.G., Renaud, P.E., 1995. Sources of primary production, benthic-pelagic coupling, and trophic relationships within the Northeast Water Polynya: insights from δ13C and δ15N analysis. Marine Ecology-Progress Series, 128, 1-10.
Howard, R.K., Koehn, J.D., 1985. Population dynamics and feeding ecology of pipefishes (Syngnathidae) associated with eelgrass beds of Western Port, Victoria. Australian Journal of Marine and Freshwater Research, 36, 361-370.
Hyslop, E.J., 1980. Stomach content analysis. A review of methods and their application. Journal of Fish Biology, 17, 411-429. IUCN, 2023. The IUCN Red List of threatened species. https:// www.iucnredlist.org/ (Accessed on 12 June 2023).
Jackson, A.L., Inger, R., Parnell, A.C., Bearhop, S., 2011. Comparing isotopic niche widths among and within communities: SIBER – Stable isotope Bayesian ellipses in R. Journal of Animal Ecology, 80, 595-602.
Kehayias, G., Kourouvakalis, D., 2010. Diel vertical migration and feeding of chaetognaths in coastal waters of the eastern Mediterranean. Biologia, 65, 301-308.
Kendrick, A.J., Hyndes, G.A., 2005. Variations in the dietary compositions of morphologically diverse syngnathid fishes. Environmental Biology of Fishes, 72, 415-427.
Killi, N., 2020. Spatio-temporal variation in the distribution and abundance of marine cladocerans in relation to environmental factors in a productive lagoon (Güllük Bay, SW Aegean Sea, Turkey). Oceanological and Hydrobiological Studies, 49 (4), 374-382.
Kolangi-Miandare, H., Askari, G., Fadakar1, D., Aghilnegad, M., Azizah, S., 2013. The biometric and cytochrome oxidase sub unit I (COI) gene sequence analysis of Syngnathus abaster (Teleostei: Syngnathidae) in Caspian Sea. Molecular Biology Research Communications, 2 (4), 133-142.
Lazareva, V.I., 2018. The Mediterranean copepod Calanipeda aquaedulcis Kritschagin, 1873 (Crustacea, Calanoida) in the Volga River reservoirs. Inland Water Biology, 11 (3), 303-309. Le Cren, E.D., 1951. The length-weight relationship and seasonal cycle in gonad weight and condition in the Perch (Perca fluviatilis). Journal of Animal Ecology, 20, 201-219.
Lesser, J.S., James, W.R., Stallings, C.D., Wilson, R.M., Nelson, J.A., 2020. Trophic niche size and overlap decreases with increasing ecosystem productivity. Oikos, 129, 1303-1313.
Liao, H., Pierce, C.L., Larscheid, J.G., 2001. Empirical assessment of indices of prey importance in the diets of predacious fish. Transactions of the American Fisheries Society, 130, 583-591.
Liousia, V., 2015. Study on the biology of the syngnathidae family in Greece. PhD Thesis Dissertation, University of Ioannina, Greece. Logan, J.M., Jardine, T.D., Miller, T.J., Bunn, S.E., Cunjak, R.A. et al., 2008. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology, 77, 838-846.
Lyons, D.O., Dunne, J.J., 2005. Reproductive ecology and operational sex ratio o worm pipefish (Nerophis lumbriciformis) in Irish waters. Biology and environment. Proceedings of the Royal Irish Academy Section B, 105, 9-14.
Lysy, M., Stasko, A.D., Swanson, H.K., 2019. nicheROVER: (Niche) (R)egion and Niche(Over)lap metrics for multidimensional ecological niches. R package version 1.1.0. https://CRAN.R-project.org/package=nicheROVER (Accessed 17 September 2019).
Manent Sintes, P., Abella-Gutiérrez, J., 2004. Aspectos ecológicos y biológicos de Syngnathus abaster (Risso, 1826) en la bahía de Fornells. Revista de Menorca, 88, 89-105.
Manning, C.G., Foster, S.J., Vincent, A.C.J., 2019. A review of the diets and feeding behaviours of a family of biologically diverse marine fishes (Family Syngnathidae). Reviews in Fish Biology and Fisheries, 29, 197-221.
MARA (Ministry of Agriculture and Rural Affairs) Report, 1988. Research project of Gulluk Lagun. Institute of Fishery in Bodrum, Turkey, 41 pp. (In Turkish).
Mayol, J., Grau, A., Riera F., Oliver, J., 2000. Llista vermella dels peixos de les Balears, Conselleria de Medi Ambient- Conselleria d’Agricultura i Pesca, Palma de Mallorca, España.
MEF, 2011. General Directory of Nature Protection and National Parks. http://gis2.cevreorman.gov.tr/mp/ (Accessed 2 June 2023).
Monteiro, N.M., Vieira, M.N., 2017. Rendez-vous at the Baltic? The ongoing dispersion of the black-striped pipefish, Syngnathus abaster. Oceanography & Fisheries Open access Journal, 3, 2, 48-53.
Monteiro, N., Pinheir, S., Magalhãe, S., Tarros, P., Vincent, A., 2023. Predicting the impacts of climate change on the distribution of European syngnathids over the next century. Frontiers in Marine Science, 10, 1138657.
Moser, F.N., Wilson, A.B., 2020. Reproductive isolation following hybrid speciation in Mediterranean pipefish (Syngnathus spp.). Animal Behaviour, 161, 77-87.
Murat, A., Ortaç, O, 2021. Wetland loss in Turkey over a hundred years: implications for conservation and management. Ecosystem Health Sustain, 7 (1),1930587.
Piñeiro-Corbeira, C., Iglesias, L., Nogueira, R., Campos, S., Jiménez, A. et al., 2021. Structure and trophic niches in mobile epifauna assemblages associated with seaweeds and habitats of syngnathid fishes in Cíes Archipelago (Atlantic Islands Marine National Park, NW Iberia). Frontiers in Marine Science, 8, 773367.
Pinnegar, J.K., Polunin, N.V.C., 1999. Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Functional Ecology, 13, 225-231.
Planas, M., 2022. Ecological traits and trophic plasticity in the greater pipefish Syngnathus acus in the NW Iberian Peninsula. Biology, 11 (5), 712.
Planas, M., Piñeiro-Corbeira, C., Bouza, C., Castejón-Silvo, I., Vera, M. et al., 2021. A multidisciplinary approach to identify priority areas for the monitoring of a vulnerable family of fishes in Spanish Marine National Parks. BMC Ecology and Evolution, 21, 4.
Planas, M., Chamorro, A., Paltrinieri, A., Campos, S., Nedelec, K., et al., 2020a. Effect of diet on breeders and inheritance in Syngnathids: Application of isotopic experimentally derived data to field studies. Marine Ecology-Progress Series, 650, 107-123.
Planas, M., Paltrinieri, A., Carneiro, M.D.D., Hernández-Urcera, J., 2020b. Effects of tissue preservation on carbon and nitrogen stable isotope signatures in Syngnathid fishes and prey. Animals, 10, 2301.
Pollom, R., 2016. Syngnathus abaster. The IUCN Red List of Threatened Species 2016: e.T21257A19423178. https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS. T21257A19423178.en (Accessed on 12 June 2023).
Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J. et al., 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia, 152, 179-189.
Quezada-Romegialli, C., Jackson, A. L., Hayden, B., Kahilainen, K. K., Lopes, C. et al., 2018. tRophicPosition, an R package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods in Ecology and Evolution, 9, 1592-1599.
R Core Team, 2018. Stats: The R stats package. https:// https:// www.rdocumentation.org/packages/stats/versions/3.6.2 (Accessed on 23 February 2018). R Core Team, 2020. The R Project for Statistical Computing. Available online: http://www.R-project.org (Accessed on 23 April 2020).
Ramsar Convention Secretariat, 2016. An Introduction to the Convention on Wetlands (previously The Ramsar Convention Manual).
Ramsar Convention Secretariat, Gland, Switzerland, 107 pp. Riccato, F., Fiorin, R., Franco, A., et al., 2003. Population structure and reproduction of three pipefish species (Teleostei, Syngnathidae) in a seagrass meadow of the Venice lagoon. Biologia Marina Mediterranea, 10, 138-145.
Ricker, W.E., Carter, N.M., 1958. Handbook of computations for biological statistics of fish populations, No. 119. The Fisheries Research Board of Canada, Queen’s printer and controller of stationary, Ottawa, 301 pp.
Sağlam, C., Akyol, O., Ceyhan, T., 2015. Fisheries in Güllük Lagoon. Ege Journal of Fisheries and Aquatic Sciences, 32, 145-149.
Seehausen, O., van Alphen, J.J.M., Witte, F., 1977. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science, 277, 1808-1811.
Shokri, M.R., Gladstone, W., Jelbart, J., 2009. The effectiveness of seahorses and pipefish (Pisces: Syngnathidae) as a flagship group to evaluate the conservation value of estuarine seagrass beds. Aquatic Conservation: Marine and Freshwater Ecosystems 19, 588-595.
Silva, K., Monteiro, N.M., Almada, V.C., Vieira, M.N., 2006a. Early life history of Syngnathus abaster (Pisces: syngnathidae). Journal of Fish Biology, 68, 80-86.
Silva, K., Monteiro, N.M., Vieira, M.N., Almada, V.C., 2006b. Reproductive behaviour of the black-striped pipefish, Syngnathus abaster (Pisces, Syngnathidae). Journal of Fish Biology, 69, 1860-1869.
Simal Rodríguez, A., Grau, A., Castro-Fernández, J. et al., 2021. Reproductive biology of pipefish Syngnathus typhle and S. abaster (Syngnathidae) from Western Mediterranean Sea. Journal of Ichthyology, 61, 608-615.
Smith-Vaniz, W.F., 2015. Syngnathus acus. The IUCN Red List of Threatened Species 2015. https://www.iucnredlist.org (Accessed on 12 June 2023).
Somay-Altaş, A.M., 2021. Hydrogeochemical fingerprints of a mixohaline wetland in the Mediterranean: Güllük coastal wetland systems- GCWS (Muğla, Turkey). Turkish Journal of Earth Sciences, 30, 38-58.
Sotiropoulos, M.A., Tonn, W.M., Wassenaar, L.I., 2004. Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: potential consequences for food web studies. Ecology of Freshwater Fish, 13, 155-160.
Stefee, A.S., Westoby, M., Bell, J.D., 1989. Habitat selection and diet in the two species of pipefish from seagrass: sex differences. Marine Ecology Progress Series, 55, 23-30.
Sundin, J., Aronsen, T., Rosenqvist, G. et al., 2017. Sex in murky waters: algal-induced turbidity increases sexual selection in pipefish. Behavioral Ecology and Sociobiology, 71-78.
Swanson, H.K., Lysy, M., Power, M., Stasko, A.D., Johnson, J.D., et al., 2015. A new probabilistic method for quantifying n-dimensional ecological niches and niche overlap. Ecology, 96, 318-324.
Sweeting, C.J., Polunin, N.V.C., Jennings, S., 2006. Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Communications in Mass Spectrometry, 20, 595-601.
Takahashi, E., Connoly, R.M., LEE, S.Y., 2003. Growth and reproduction of double-ended pipefish, Syngnathoides biaculeatus, in Moerton Bay. Queensland, Australia. Environmental Biology of Fishes, 67, 23-33.
Taşkavak, E., Gürkan, Ş., Severa, T.M., Akalına, S., Özaydına, O., 2010. Gut contents and feeding habits of the great pipefish, Syngnathus acus Linnaeus, 1758, in Izmir Bay (Aegean Sea, Turkey). Zoology in the Middle East, 50, 75-82.
Tesh, F.W., 1971. Age and growth. In: RICKE WE (Ed), Methods for assessment of fish production in fresh waters. Blackwell Scientific Publications, Oxford: 98-130.
Tieszen, L.L., Boutton, T.W., Tesdahl, K.G., Slade, N.A., 1983. Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologica, 57, 32-37.
Tokaç, A., Ünal V., Tosunoğlu, Z., Akyol O., Özbilgin H., Gökçe G., 2010. Fisheries of Aegean Sea, IMEAK Deniz Ticaret Odası İzmir Şubesi Yayınları: İzmir, 371 pp. (in Turkish).
Tomasini, J.A., Quignard, P., Capapé, C., Bouchereau, L., 1991. Facteurs du succès reproductif de Syngnathus abaster Risso, 1826 (Pisces, Teleostei, Syngnathidae) en milieu lagunaire méditerranéen (lagune de Mauguio, France). Acta Oecologica, 12, 331-355.
Tosunoğlu, Z., Ünal, V., Kaykaç, M.H. Ege Dalyanları, 2017. Su Ürünleri Kooperatifleri Merkez Birliği Yayınları SÜRKOOP, Ankara, 322 pp. (in Turkish).
Uriarte, I., Villate, F., Iriarte, A., 2016. Zooplankton recolonization of the inner estuary of Bilbao: influence of pollution abatement, climate and non-indigenous species. Journal of Plankton Research, 38 (3), 718-731.
Valladares, S., Planas, M., 2012. Non-lethal dorsal fin sampling for stable isotope analysis in seahorses. Aquatic Ecology, 46, 363-370.
Vasileva, E.D., 2003. Main alterations in ichthyofauna of the largest rivers of the northern coast of the Black Sea in the last 50 years: A review. Folia Zoologica, 52, 337-358.
Veiga, P., Machado, D., Almeida, C., Bentes, L., Monteiro, P. et al., 2009. Weight-length relationships for 54 species of the Arade estuary, southern Portugal. Journal of Applied Ichthyology, 25, 493-496.
Vieira, R.P., Monteiro, P., Ribeiro, J., Bentes, L., Oliveira, F. et al., 2014. Length-weight relationships of six syngnathid species from Ria Formosa, SW Iberian coast. Cahiers de Biologie Marine, 55, 9-12.
Vincent, A.C.J., Ahnesjö, I., Berglund, A., Rosenqvist, G., 1992. Pipefish and seahorses: are they all sex role reserved? Trends in Ecology and Evolution, 7, 237-241.
Vincent, A., Berglund, A., Ahnesjö, I., 1995. Reproductive ecology of five pipefish species in one eelgrass meadow. Environmental Biology of Fishes, 44, 347-361.
Vizzini, S., Mazzola, A., 2004. The structure of pipefish community (Pisces: Synganthidae) from a western Mediterranean sea grass meadow based on stable isotope analysis. Estuaries, 27, 325-333.
Whittaker, R.H., Likens, G.E., 1973. Carbon in the biota. p. 281-302. In: Carbon in the Biosphere. Woodwell, G. M., Pecan, E. R. (Eds). National Technical Information Service, Springfield, VA.
Wickham, H., Chang, W., Henry, C., Lin Pedersen, T., Takahasi, K. et al., 2023. Create elegant data visualisations using the grammar of graphics. https://CRAN.R-project.org/ package=ggplot2 (Accessed 17 September 2019).
Wilson, A.B., 2006. Interspecies mating in sympatric species of Syngnathus pipefish. Molecular Ecology, 15, 809-824.
Wootton, R.J., 1999. Ecology of Teleost fishes. Springer Dordrecht, Dordrecht , The Netherlands. 386 pp.
Yildiz, T., Uzer, U., Firdes Saadet, K., 2015. Preliminary report of a biometric analysis of greater pipefish Syngnathus acus Linnaeus, 1758 for the western Black Sea. Turkish Journal of Zoology, 39 (5), 19.
Yucel-Gier, G., Pazi, I., Kucuksezgin, F., 2013. Spatial analysis of fish farming in the Gulluk Bay (Eastern Aegean). Turkish Journal of Fisheries and Aquatic Sciences, 13, 737-744.