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Population structure of the seahorse Hippocampus reidi (Syngnathiformes: Syngnathidae) in a Brazilian semi-arid estuary

Abstract

The longsnout seahorse (Hippocampus reidi) is a vulnerable species found along most of the Brazilian coastline, such as semi-arid estuaries with strong rainfall seasonality, hypersalinity, and low depth. To evaluate the population structure of H. reidi over time, we monitored the seahorse population in the Pacoti estuary (Brazil) for one year, based on 248 registered specimens. Salinity, water transparency, sex, pregnancy, body height, and holdfast use were registered. Mixed linear models revealed that sampling month, salinity, and transparency had no influence on population density in the lower zone of the estuary. Pregnant individuals were more frequent in the dry season and at higher salinities. Mean body height (12.7 cm) increased in the dry season. Bright colors were predominant. The seahorses employed nine types of holdfasts, most often mangrove roots, and were found to reproduce throughout the year, peaking in the dry season. Salinity and transparency did not impact population density. In Brazilian semi-arid estuaries, the longsnout seahorse is strongly associated with mangrove vegetation, used as holdfast. Therefore, the conservation of seahorse populations depends on the conservation of the local mangrove forests.

Keywords:
Coastal ecosystem; Distribution; Exploitation; Mangrove; Population density

Resumo

O cavalo-marinho Hippocampus reidi é uma espécie vulnerável encontrada ao longo da maior parte da costa brasileira, incluindo estuários semiáridos com forte sazonalidade de chuvas, hipersalinidade e baixa profundidade. Para avaliar a estrutura populacional do H. reidi ao longo do tempo, monitoramos a população de cavalos-marinhos no estuário do Pacoti (Brasil) por um ano, com base em 248 espécimes registrados. Registramos a salinidade, a transparência da água, o sexo, a gravidez, a altura do corpo e o uso de substratos de fixação. Modelos lineares mistos revelaram que o mês de coleta, a salinidade e a transparência não tiveram influência na densidade populacional na zona inferior do estuário. Indivíduos grávidos eram mais frequentes na estação seca e em salinidades mais altas. A altura média do corpo (12,7 cm) aumentou na estação seca. Cores vibrantes foram predominantes. Os cavalos-marinhos utilizaram nove tipos de substratos de fixação, com maior frequência em raízes de mangue, e foram encontrados se reproduzindo ao longo do ano, com pico na estação seca. Em estuários semiáridos brasileiros, o cavalo-marinho H. reidi está fortemente associado à vegetação de mangue, utilizada como substrato de fixação. Portanto, a conservação das populações de cavalos-marinhos depende da preservação dos manguezais.

Palavras chave:
Densidade populacional; Distribuição; Ecossistema costeiro; Explotação; Manguezal

INTRODUCTION

Seahorses are bony fishes of the family Syngnathidae, classified in a single genus, Hippocampus Rafinesque, 1810. Most species are monogamous and populations are characterized by low density and mobility (Foster, Vincent, 2004Foster SJ, Vincent ACJ. Life history and ecology of seahorses: implications for conservation and management. J Fish Biol. 2004; 65(1):1–61. https://doi.org/10.1111/j.0022-1112.2004.00429.x
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; Vincent et al., 2005Vincent ACJ, Evans KL, Marsden AD. Home range behaviour of the monogamous Australian seahorse, Hippocampus whitei. Environ Biol Fishes. 2005; 72:1–12. https://doi.org/10.1007/s10641-004-4192-7
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) and considered sedentary (Caldwell, Vincent, 2013Caldwell IR, Vincent ACJ. A sedentary fish on the move: effects of displacement on long-snouted seahorse (Hippocampus guttulatus Cuvier) movement and habitat use. Environ Biol Fishes. 2013; 96(1):67–75. https://doi.org/10.1007/s10641-012-0023-4
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). Their limited mobility prevents them from traveling long distances or resisting the drag of water currents, especially in the juvenile stage (Qin et al., 2014Qin G, Zhang Y, Huang L, Lin Q. Effects of water current on swimming performance, ventilation frequency, and feeding behavior of young seahorses (Hippocampus erectus). J Exp Mar Biol Ecol. 2014; 461:337–43. https://doi.org/10.1016/j.jembe.2014.09.001
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). Adults only travel larger distances when exposed to major disturbances (Caldwell, Vincent, 2013Caldwell IR, Vincent ACJ. A sedentary fish on the move: effects of displacement on long-snouted seahorse (Hippocampus guttulatus Cuvier) movement and habitat use. Environ Biol Fishes. 2013; 96(1):67–75. https://doi.org/10.1007/s10641-012-0023-4
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). In other words, seahorses are strongly habitat-dependent. Adverse anthropic impacts on aquatic ecosystems, such as habitat destruction and pollution, greatly increases the vulnerability and risk of extinction of seahorses (Vincent et al., 2011Vincent ACJ, Foster SJ, Koldewey HJ. Conservation and management of seahorses and other Syngnathidae. J Fish Biol. 2011; 78(6):1681–724. https://doi.org/10.1111/j.1095-8649.2011.03003.x
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).

Coastal regions with high concentrations of human settlements are impacted by a wide array of anthropic stressors, including fishing, pollution, navigation, habitat destruction, eutrophication, and the introduction of competitive species. These factors are particularly adverse to vulnerable species like seahorses (Pollom et al., 2021Pollom RA, Ralph GM, Pollock CM, Vincent ACJ. Global extinction risk for seahorses, pipefishes and their near relatives (Syngnathiformes). Oryx. 2021; 55(4):497–506. https://doi.org/10.1017/S0030605320000782
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). Because of their ‘charisma’ (Vincent et al., 2011Vincent ACJ, Foster SJ, Koldewey HJ. Conservation and management of seahorses and other Syngnathidae. J Fish Biol. 2011; 78(6):1681–724. https://doi.org/10.1111/j.1095-8649.2011.03003.x
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), seahorses are also coveted by aquariophiles and are in many locations subject to unsustainable commercial practices (Vincent et al., 2011Vincent ACJ, Foster SJ, Koldewey HJ. Conservation and management of seahorses and other Syngnathidae. J Fish Biol. 2011; 78(6):1681–724. https://doi.org/10.1111/j.1095-8649.2011.03003.x
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; Koning, Hoeksema, 2021Koning S, Hoeksema BW. Diversity of seahorse species (Hippocampus spp.) in the international aquarium trade. Diversity (Basel). 2021; 13(5):187. https://doi.org/10.3390/d13050187
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). In addition, seahorses may be harmed by accidental capture (Vaidyanathan et al., 2021Vaidyanathan T, Zhang X, Balakrishnan R, Vincent A. Catch and trade bans for seahorses can be negated by non-selective fisheries. Aquat Conserv. 2021; 31(1):43–59. https://doi.org/10.1002/AQC.3419
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) and have long been exploited for souvenirs, charms and cult objects (Alves, Rosa, 2006Alves RRN, Rosa IL. From cnidarians to mammals: The use of animals as remedies in fishing communities in NE Brazil. J Ethnopharmacol. 2006; 107(2):259–76. https://doi.org/10.1016/J.JEP.2006.03.007
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; Law, 2021Law S. Dried seahorse in traditional medicine: A narrative review. IDHM. 2021; 2:158. https://doi.org/10.4081/idhm.2021.158
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; Pereira et al., 2021Pereira LF, Silveira RB, Silva AG, Freitas MO, Abilhoa V. Medicinal and mustical-religious uses of seahorse in Southern Brazilian coast. Rev Biodivers. 2021; 20(4):168–76. Available from: https://periodicoscientificos.ufmt.br/ojs/index.php/biodiversidade/article/view/13251
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; Loiola et al., 2022Loiola SC, Pinto LM, Kobayashi RK, Sánchez-Botero JI, Sequeira Garcez D. Conhecimento empírico de pescadores artesanais como base para a conservação do cavalo-marinho Hippocampus reidi (Teleostei: Syngnathidae) no estuário do rio Pacoti (CE). In: Garcez DS, Sánchez-Botero JI, editors. Conhecimento local e o manejo de recursos pesqueiros de uso comum: Experiências nos litorais do Maranhão, Ceará e Pernambuco. Fortaleza: Imprensa Universitária; 2022. p.219–80.).

The international seahorse trade is regulated by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), which provides a list of all the species of the genus Hippocampus in their appendix II (CITES, 2023Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). Appendices I, II and III. Appendices. 2023:1–81. Available from: https://cites.org/eng/app/appendices.php
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). The Convention has been successful at reducing the commercial pressure on natural populations, especially trading of live specimens (Foster et al., 2022Foster SJ, Justason T, Magera AM, Vincent ACJ. CITES makes a measurable difference to the trade in live marine fishes: The pioneering case of seahorses. Biol Conserv. 2022; 272:109653. https://doi.org/10.1016/j.biocon.2022.109653
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), but studies have shown that unregistered and clandestine international trade, especially of dried seahorses, remain common in many countries (Foster et al., 2019Foster SJ, Kuo TC, Wan AKY, Vincent ACJ. Global seahorse trade defies export bans under CITES action and national legislation. Mar Policy. 2019; 103:33–41. https://doi.org/10.1016/J.MARPOL.2019.01.014
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). Specimens exported for aquarium use are still captured in the wild (Koning, Hoeksema, 2021Koning S, Hoeksema BW. Diversity of seahorse species (Hippocampus spp.) in the international aquarium trade. Diversity (Basel). 2021; 13(5):187. https://doi.org/10.3390/d13050187
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), regardless of regulations to the contrary, leading to the depletion of natural stocks (Vaidyanathan, Vincent, 2021Vaidyanathan T, Vincent ACJ. State of seahorse fisheries in India, nearly two decades after they were banned. Biodivers Conserv. 2021; 30:2223–53. https://doi.org/10.1007/s10531-021-02188-6
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).

In Brazil, seahorses have been on the National List of Endangered Species since 2014, pursuant to Ordinance #445 of 17 Dec 2014 issued by the Ministério do Meio Ambiente (MMA, 2014Ministério do Meio Ambiente (MMA). Portaria No 445, de 17 de dezembro de 2014. Brazil: Diário Oficial da União, Seção 1, p.126; 2014.). The ban covers the capture, transportation, storage and sales of specimens from natural populations. More recently, the list of endangered seahorses was updated through Ordinance #148 of 7 June 2022 issued by the Ministério do Meio Ambiente (MMA, 2022Ministério do Meio Ambiente (MMA). Portaria MMA No 148, de 7 de junho de 2022. Brazil: Diário Oficial da União, Seção 1, p.74; 2022.) and now includes three species considered vulnerable: Hippocampus reidi Ginsburg, 1933, H. erectus Perry, 1810, and H. patagonicus Piacentino & Luzzatto, 2004. These species are also listed as vulnerable in the Livro Vermelho da Fauna Brasileira Ameaçada de Extinção (Di Dario et al., 2018Di Dario F, Santos RA, Ramos RTC, Rosa IML, Sampaio CLS, Joyeux J-C et al. Hippocampus reidi Ginsburg, 1933. In: Instituto Chico Mendes de Conservação da Biodiversidade, editor. Livro Vermelho da Fauna Brasileira Ameaçada de Extinção, vol. Volume VI – Peixes. 1st ed. Brasília: MMA/ICMBio; 2018. p.786–91.).

Despite these mechanisms of protection, Brazil is a major supplier of live seahorses for the aquarium trade (Rhyne et al., 2012Rhyne AL, Tlusty MF, Schofield PJ, Kaufman L, Morris JA. Revealing the appetite of the marine aquarium fish trade: The volume and biodiversity of fish imported into the United States. PLoS ONE. 2012; 7(5):35808. https://doi.org/10.1371/journal.pone.0035808
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, 2017Rhyne AL, Tlusty MF, Szczebak JT, Holmberg RJ. Expanding our understanding of the trade in marine aquarium animals. PeerJ. 2017; 5:e2949. https://doi.org/10.7717/peerj.2949
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; Gurjão, Lotufo, 2018Gurjão LM, Lotufo TMC. Native species exploited by marine aquarium trade in Brazil. Biota Neotrop. 2018; 18(3):e20170387. https://doi.org/10.1590/1676-0611-bn-2017-0387
https://doi.org/10.1590/1676-0611-bn-201...
; Koning, Hoeksema, 2021Koning S, Hoeksema BW. Diversity of seahorse species (Hippocampus spp.) in the international aquarium trade. Diversity (Basel). 2021; 13(5):187. https://doi.org/10.3390/d13050187
https://doi.org/10.3390/d13050187...
). Currently, exported specimens are claimed to be bred in captivity (Foster et al., 2022Foster SJ, Justason T, Magera AM, Vincent ACJ. CITES makes a measurable difference to the trade in live marine fishes: The pioneering case of seahorses. Biol Conserv. 2022; 272:109653. https://doi.org/10.1016/j.biocon.2022.109653
https://doi.org/10.1016/j.biocon.2022.10...
), but information on the regional and national seahorse trade is scant and unreliable (Koning, Hoeksema, 2021Koning S, Hoeksema BW. Diversity of seahorse species (Hippocampus spp.) in the international aquarium trade. Diversity (Basel). 2021; 13(5):187. https://doi.org/10.3390/d13050187
https://doi.org/10.3390/d13050187...
). Among Brazilian states, Ceará is one of the largest exporters of seahorses for the aquarium trade (Monteiro-Neto et al., 2003Monteiro-Neto C, Cunha FEA, Nottingham MC, Araújo ME, Rosa IL, Barros GML. Analysis of the marine ornamental fish trade at Ceará State, northeast Brazil. Biodivers Conserv. 2003; 12:1287–95. https://doi.org/10.1023/A:1023096023733
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; Gurjão et al., 2018Gurjão LM, Barros GML, Lopes DP, Machado DAN, Lotufo TMC. Illegal trade of aquarium species through the Brazilian postal service in Ceará State. Mar Freshw Res. 2018; 69(1):178–85. https://doi.org/10.1071/MF16257
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). The only seahorse species confirmed to occur in Ceará is H. reidi, one of the most widely traded species in the world (Foster et al., 2016Foster S, Wiswedel S, Vincent A. Opportunities and challenges for analysis of wildlife trade using CITES data - seahorses as a case study. Aquat Conserv. 2016; 26(1):154–72. https://doi.org/10.1002/aqc.2493
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). This scenario alerts us regarding the urgency of carrying out natural history studies to understand better ways to support conservation efforts.

Ceará is inserted in the northeastern coastline of Brazil, in a large semi-arid region extending from Maranhão to Rio Grande do Norte (Soares et al., 2021Soares MO, Campos CC, Carneiro PBM, Barroso HS, Marins RV, Teixeira CEP et al. Challenges and perspectives for the Brazilian semi-arid coast under global environmental changes. Perspect Ecol Conserv. 2021; 19(3):267–78. https://doi.org/10.1016/j.pecon.2021.06.001
https://doi.org/10.1016/j.pecon.2021.06....
). The rainfall pattern in this region is mainly determined by the Intertropical Convergence Zone (ITCZ), resulting in a well-demarcated and often intense rainy season in the first semester. The reduced river flow associated with high temperatures and high rates of evaporation decreases the freshwater flow in estuaries, which tend to be shallow and seasonally hypersaline (Schettini et al., 2017Schettini CAF, Valle-Levinson A, Truccolo EC. Circulation and transport in short, low-inflow estuaries under anthropogenic stresses. Reg Stud Mar Sci. 2017; 10:52–64. https://doi.org/10.1016/j.rsma.2017.01.004
https://doi.org/10.1016/j.rsma.2017.01.0...
). Thus, environmental factors may be expected to vary significantly between the rainy season and the dry season (Montagna et al., 2018Montagna PA, Hu X, Palmer TA, Wetz M. Effect of hydrological variability on the biogeochemistry of estuaries across a regional climatic gradient. Limnol Oceanogr. 2018; 63(6):2465–78. https://doi.org/10.1002/LNO.10953
https://doi.org/10.1002/LNO.10953...
), with higher salinity and greater water transparency in the latter due to the reduced inflow of freshwater and organic matter of continental origin.

Salinity is considered the second-most important determinant of marine life (Tyberghein et al., 2012Tyberghein L, Verbruggen H, Pauly K, Troupin C, Mineur F, Clerck O. Bio-ORACLE: A global environmental dataset for marine species distribution modelling. Glob Ecol Biogeogr. 2012; 21(2):272–81. https://doi.org/10.1111/j.1466-8238.2011.00656.x
https://doi.org/10.1111/j.1466-8238.2011...
) as it regulates the distribution of organisms according to osmotic pressure. It is particularly important in estuaries where it is the main regulator of biological population density (Schettini et al., 2017Schettini CAF, Valle-Levinson A, Truccolo EC. Circulation and transport in short, low-inflow estuaries under anthropogenic stresses. Reg Stud Mar Sci. 2017; 10:52–64. https://doi.org/10.1016/j.rsma.2017.01.004
https://doi.org/10.1016/j.rsma.2017.01.0...
). Seahorses are euryhaline animals with glomerular kidneys (Martinez, 2017Martinez CBR. The Kidney. Reference module in life sciences. Elsevier; 2017. p.1–7. https://doi.org/10.1016/B978-0-12-809633-8.03171-X
https://doi.org/10.1016/B978-0-12-809633...
) allowing them to tolerate salinities between nine and 37 (Jiaxin et al., 1990Jiaxin C, Bueno P, Lovatelli A. Brief introduction to mariculture of five selected species in China. Bangkok: 1990.), although adult specimens of H. reidi have been observed at salinities around five (Silveira, 2005Silveira RB. Dinâmica Populacional do Cavalo-marinho Hippocampus reidi no manguezal de Maracaípe, Ipojuca, Pernambuco, Brasil. [PhD Thesis]. Porto Alegre: Pontifícia Universidade Católica do Rio Grande do Sul; 2005. Available from: https://hdl.handle.net/10923/5335
https://hdl.handle.net/10923/5335...
). Seahorses tolerate slow changes in salinity well (Tseng et al., 2020Tseng C-C, Chien JH, Chu T-W, Cheng A-C, Shiu Y-L, Han T-W et al. Effects of food type, temperature and salinity on the growth performance and antioxidant status of the longsnout seahorse, Hippocampus reidi. Aquac Res. 2020; 51(11):4793–804. https://doi.org/10.1111/ARE.14826
https://doi.org/10.1111/ARE.14826...
), but abrupt changes in salinity following the sudden discharge of masses of freshwater into the estuary can lead to a spike in mortality (Hora et al., 2016Hora MSC, Joyeux J-C, Rodrigues RV, Sousa-Santos LP, Gomes LC, Tsuzuki MY. Tolerance and growth of the longsnout seahorse Hippocampus reidi at different salinities. Aquaculture. 2016; 463:1–06. https://doi.org/10.1016/J.AQUACULTURE.2016.05.003
https://doi.org/10.1016/J.AQUACULTURE.20...
) and upset the temporal distribution of seahorses throughout the ecosystem. In addition, juveniles have a smaller osmotic regulation capacity and so are more likely to be affected by osmotic stress (Hora et al., 2016Hora MSC, Joyeux J-C, Rodrigues RV, Sousa-Santos LP, Gomes LC, Tsuzuki MY. Tolerance and growth of the longsnout seahorse Hippocampus reidi at different salinities. Aquaculture. 2016; 463:1–06. https://doi.org/10.1016/J.AQUACULTURE.2016.05.003
https://doi.org/10.1016/J.AQUACULTURE.20...
; Tseng et al., 2020Tseng C-C, Chien JH, Chu T-W, Cheng A-C, Shiu Y-L, Han T-W et al. Effects of food type, temperature and salinity on the growth performance and antioxidant status of the longsnout seahorse, Hippocampus reidi. Aquac Res. 2020; 51(11):4793–804. https://doi.org/10.1111/ARE.14826
https://doi.org/10.1111/ARE.14826...
). Although seahorses thrive best at salinities near their isosmotic point (Hora et al., 2016Hora MSC, Joyeux J-C, Rodrigues RV, Sousa-Santos LP, Gomes LC, Tsuzuki MY. Tolerance and growth of the longsnout seahorse Hippocampus reidi at different salinities. Aquaculture. 2016; 463:1–06. https://doi.org/10.1016/J.AQUACULTURE.2016.05.003
https://doi.org/10.1016/J.AQUACULTURE.20...
) of 11.68 (well below the average estuarine environment), reproduction peaks when the salinity is most stable, and the osmotic stress is smallest (usually during the dry season).

Seahorses are predators that ambush small crustaceans and larvae floating in the water column. To do so, they bring their long snout within striking range and suck in the prey (Foster, Vincent, 2004Foster SJ, Vincent ACJ. Life history and ecology of seahorses: implications for conservation and management. J Fish Biol. 2004; 65(1):1–61. https://doi.org/10.1111/j.0022-1112.2004.00429.x
https://doi.org/10.1111/j.0022-1112.2004...
). Turbidity would therefore seem to compromise foraging and, in fact, the relationship between foraging and luminosity has been evaluated in ex situ studies on H. reidi (Felício et al., 2006Felício AKC, Rosa IL, Souto A, Freitas RHA. Feeding behavior of the longsnout seahorse Hippocampus reidi Ginsburg, 1933. J Ethol. 2006; 24(3):219–25. https://doi.org/10.1007/s10164-005-0189-8
https://doi.org/10.1007/s10164-005-0189-...
) and other species (e.g., Hippocampus trimaculatus Leach, 1814 by Sheng et al., 2006Sheng J, Lin Q, Chen Q, Gao Y, Shen L, Lu J. Effects of food, temperature and light intensity on the feeding behavior of three-spot juvenile seahorses, Hippocampus trimaculatus Leach. Aquaculture. 2006; 256(1–4):596–607. https://doi.org/10.1016/j.aquaculture.2006.02.026
https://doi.org/10.1016/j.aquaculture.20...
; H. barbouri Jordan & Richardson, 1908 by Er et al., 2020Er VWC, Christianus A, Harah ZM, Chong CM, Ismail MS. Foraging dependency of Barbour’s seahorse Hippocampus barbouri (Jordan and Richardson 1908) juveniles on photoperiod and light intensity. J Environ Biol. 2020; 41:1281–88. https://doi.org/10.22438/jeb/41/5(SI)/MS_21
https://doi.org/10.22438/jeb/41/5(SI)/MS...
). On the other hand, few studies have evaluated the influence of turbidity in situ. One example is a study by Claassens, Hodgson (2018)Claassens L, Hodgson AN. Monthly population density and structure patterns of an endangered seahorse Hippocampus capensis: a comparison between natural and artificial habitats. J Fish Biol. 2018; 92(6):2000–15. https://doi.org/10.1111/jfb.13639
https://doi.org/10.1111/jfb.13639...
which failed to detect a significant effect of turbidity on the distribution of Hippocampus capensis Boulenger, 1900, in coastal waters, including estuaries. A more systematic evaluation of the influence of water transparency on population structure would help clarify the ecology of seahorses in tropical semi-arid estuaries.

Research on how H. reidi populations along the semi-arid coast of Brazil are temporally affected by changes in environmental factors (e.g., prolonged dry or rainy seasons altering salinity and water transparency) can shed light on seahorse population structure and thus help manage populations in tropical estuaries. The main purpose of this study was to evaluate the patterns of H. reidi population structure in a Brazilian semi-arid estuary, with emphasis on temporal variations, contrasting the impact of the abiotic variables associated with the dry season and the rainy season. We expected temporal variations in environmental factors to influence population structure (higher salinity and greater water transparency associated with higher densities of H. reidi) and we expected reproduction to occur throughout the year, with a peak in the dry season (greater proportion of pregnant males).

MATERIAL AND METHODS

Study area. The study was carried out in the Pacoti River estuary on the coast of Ceará, a semi-arid region in Northeastern Brazil. The mean salinity of the estuary was 37.7 (range: 37.3–38.7), the mean temperature was 29.2ºC (range: 28.1–31.3) (Schettini et al., 2017Schettini CAF, Valle-Levinson A, Truccolo EC. Circulation and transport in short, low-inflow estuaries under anthropogenic stresses. Reg Stud Mar Sci. 2017; 10:52–64. https://doi.org/10.1016/j.rsma.2017.01.004
https://doi.org/10.1016/j.rsma.2017.01.0...
) and the mean annual rainfall in the region was 1584 mm (INMET, 2023Instituto Nacional de Meteorologia (INMET). Normais climatológicas do Brasil 1991-2020. 2023a. Available from: https://portal.inmet.gov.br/normais#
https://portal.inmet.gov.br/normais#...
). The estuary receives a large inflow of freshwater during the rainy season, from January to June, whereas very little rain falls in the dry season, between July and December (Molisani et al., 2006Molisani MM, Cruz ALV, Maia LP. Estimation of the freshwater river discharge to estuaries in Ceará State, Brazil. Arq Ciênc Mar. 2006; 39:53–60.). With an average depth of ~3 m, the estuary is characterized as shallow, with well-mixed waters (Schettini et al., 2017Schettini CAF, Valle-Levinson A, Truccolo EC. Circulation and transport in short, low-inflow estuaries under anthropogenic stresses. Reg Stud Mar Sci. 2017; 10:52–64. https://doi.org/10.1016/j.rsma.2017.01.004
https://doi.org/10.1016/j.rsma.2017.01.0...
).

The mangrove forest along the Pacoti River includes the species Rhizophora mangle L. (red mangrove), Avicennia germinans L. and Avicennia schaueriana Stapf & Leechm. ex Moldenke (black mangrove), Laguncularia racemosa (L.) C. F. Gaertn. (white mangrove), and Conocarpus erectus L. (button mangrove) (Gorayeb et al., 2004Gorayeb A, Silva EV, Meireles AJA. Meio ambiente e condições de sustentabilidade da planície flúvio-marinha do rio Pacoti - Ceará - Brasil. Geoambiente On-Line. 2004; 2:1–17. https://doi.org/10.5216/rev.%20geoambie.v0i2.25861
https://doi.org/10.5216/rev.%20geoambie....
). In the zone affected by the tides, about 158 ha is covered by mangrove (SEMACE, 2010Superintendência Estadual do Meio Ambiente (SEMACE). Área de Proteção Ambiental do Rio Pacoti. SemaceCeGovBr. 2010. Available from: https://www.semace.ce.gov.br/2010/12/08/area-de-protecao-ambiental-do-rio-pacoti/
https://www.semace.ce.gov.br/2010/12/08...
). The species L. racemosa and R. mangle are predominant in the lower part of the estuary where the present study was conducted.

The first kilometer upstream from the river mouth was divided into 11 sampling areas (Fig. 1), consisting on non-linear transects of variable length (range: 65–611 m) and 1 m width. The area of potential occupation by H. reidi in the Pacoti River estuary was defined based on the availability of habitats and knowledge of the local ecology (Loiola et al., 2022Loiola SC, Pinto LM, Kobayashi RK, Sánchez-Botero JI, Sequeira Garcez D. Conhecimento empírico de pescadores artesanais como base para a conservação do cavalo-marinho Hippocampus reidi (Teleostei: Syngnathidae) no estuário do rio Pacoti (CE). In: Garcez DS, Sánchez-Botero JI, editors. Conhecimento local e o manejo de recursos pesqueiros de uso comum: Experiências nos litorais do Maranhão, Ceará e Pernambuco. Fortaleza: Imprensa Universitária; 2022. p.219–80.). Earlier studies (Rosa et al., 2007Rosa IL, Oliveira TPR, Castro ALC, Moraes LES, Xavier JHA, Nottingham MC et al. Population characteristics, space use and habitat associations of the seahorse Hippocampus reidi (Teleostei: Syngnathidae). Neotrop Ichthyol. 2007; 5(3):405–14. https://doi.org/10.1590/S1679-62252007000300020
https://doi.org/10.1590/S1679-6225200700...
; Osório, 2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.; Silva, 2018Silva VMM. Caracterização da população de Hippocampus reidi no estuário do rio Pacoti, Ceará. [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2018. Available from: http://www.repositorio.ufc.br/handle/riufc/36777
http://www.repositorio.ufc.br/handle/riu...
) sampled seahorses further upstream, but hydromorphological changes appear to have reduced the occurrence of H. reidi in the upper zone, as reported by Silva (2018Silva VMM. Caracterização da população de Hippocampus reidi no estuário do rio Pacoti, Ceará. [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2018. Available from: http://www.repositorio.ufc.br/handle/riufc/36777
http://www.repositorio.ufc.br/handle/riu...
) who attributed the low seahorse density upstream to silting. Large dams have been built in the Pacoti River, reducing the flow of freshwater which would otherwise have expelled sediments more effectively, thereby altering silting rates and estuarine morphology (Lacerda et al., 2007Lacerda LD, Menezes MOT, Molisani MM. Changes in mangrove extension at the Pacoti River estuary, CE, NE Brazil due to regional environmental changes between 1958 and 2004. Biota Neotrop. 2007; 7(3):67–72. https://doi.org/10.1590/S1676-06032007000300007
https://doi.org/10.1590/S1676-0603200700...
). Based on these reports and the experience of local fishermen, we focused our sampling efforts on the lower zone of the estuary, where the population of seahorses was concentrated.

The location and extension of the transects were based on the availability of habitats with anchoring structures: we selected areas with at least two microhabitats, mostly mangrove roots and sand, along with other bottoms (e.g., seaweed, seagrass, rocks), avoiding areas with highly homogenous microhabitats (e.g., large uninterrupted tracts of sand). Priority was given to the availability of habitats rather than to transect size (as in many previous studies), taking into account that the expected association between biological diversity and area may be an artifact of the number of locally available habitats (Rabelo et al., 2017Rabelo RM, Bicca-Marques JC, Aragón S, Nelson BW. Are fluvial islands “real” islands for arboreal mammals? Uncovering the effect of patch size under the species–area relationship. J Biogeogr. 2017; 44(8):1802–12. https://doi.org/10.1111/jbi.13034
https://doi.org/10.1111/jbi.13034...
).

Sampling. Seahorse specimens were registered and abiotic data was collected during low tide (0.3–0.6 m) once a month between December 2017 and November 2018. Each month, the sampling sites were chosen at random and the greatest possible number of sites were covered within the time window allowed by the low tide (Tab. S1). Specimens of H. reidi were located visually from above or, if the water was deep enough, by skin diving, as proposed by Sabino (1999Sabino J. Comportamento de peixes em riachos: métodos de estudo para uma abordagem naturalística. In: Caramaschi EP, Mazzoni R, Peres-Neto PR, editors. Ecologia de peixes de riachos, vol. 6. Rio de Janeiro: PPGE-UFR; 1999. p.183–208.).

Predictors of population structure. Salinity and water transparency (cm) were measured with a refractometer and a Secchi disk, respectively, for each sampling site and at each sampling event. The rainy season and dry season were considered to extend from January to June, and from July to December, respectively, based on monthly rainfall indices retrieved from the National Institute of Meteorology, covering the period 1991–2020 (INMET, 2023bInstituto Nacional de Meteorologia (INMET). Banco de dados meteorológicos do INMET. 2023b. Available from: https://bdmep.inmet.gov.br/
https://bdmep.inmet.gov.br/...
).

Descriptors of population structure. We determined the sex of each individual based on the presence of a brood pouch (present = male; absent = female) (Lourie et al., 2004Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ. A guide to the identification of seahorses. Washington D.C.: University of British Columbia and World Wildlife Fund; 2004.). Males with swollen brood pouch were considered pregnant. In addition, the height of the smallest individual with a brood pouch was used as cut-off to segregate adults from juveniles (Baum, Vincent, 2005Baum JK, Vincent ACJ. Magnitude and inferred impacts of the seahorse trade in Latin America. Environ Conserv. 2005; 32(4):305–19. https://doi.org/10.1017/S0376892905002481
https://doi.org/10.1017/S037689290500248...
).

The species were identified based on external morphology, using the guide of Project Seahorse (Lourie et al., 2004Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ. A guide to the identification of seahorses. Washington D.C.: University of British Columbia and World Wildlife Fund; 2004.). The individuals were photographed and measured as proposed by Lourie et al. (2004Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ. A guide to the identification of seahorses. Washington D.C.: University of British Columbia and World Wildlife Fund; 2004.), with the height corresponding to the distance between the tip of the coronet to the tip of the uncurled tail. The predominant color of each individual was registered without taking into account stripes, blotches, and spots commonly displayed by individuals (Lourie et al., 2004Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ. A guide to the identification of seahorses. Washington D.C.: University of British Columbia and World Wildlife Fund; 2004.). The holdfast (e.g., mangrove roots, seagrass, sand, etc.) employed at the moment of sampling was registered.

Statistical analyses. The collected data were analyzed with the R programming language (R Development Core Team, 2023R Development Core Team. R: A language and environment for statistical computing, version 4.2.2. Vienna, Austria: R Foundation for Statistical Computing; 2023. Available from: https://www.r-project.org/
https://www.r-project.org/ ...
). Population density was estimated for each event (e.g., sample month) and expressed as the ratio between the number of individuals observed in each transect and the area of that transect. We initially verified the existence of significant differences in density, water transparency, and salinity between the dry season and the rainy season using the generalized least squares (GLS) test (Zuur et al., 2009Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York, NY: Springer New York; 2009. https://doi.org/10.1007/978-0-387-87458-6
https://doi.org/10.1007/978-0-387-87458...
).

FIGURE 1 |
Geographic location of the Pacoti River estuary, Ceará, Brazil (A, B), indicating Hippocampus reidi sampling locations (A to K) (C).

The sex ratio was determined by comparing proportions and analyzing the difference between the expected and actual frequency for males and females, using the chi-squared test (χ²) (R Development Core Team, 2023R Development Core Team. R: A language and environment for statistical computing, version 4.2.2. Vienna, Austria: R Foundation for Statistical Computing; 2023. Available from: https://www.r-project.org/
https://www.r-project.org/ ...
). The proportion of pregnant males each month was expressed as the ratio between pregnant males and the total number of males.

We then evaluated the effect of the sampling month, salinity, and water transparency on population density and mean body height using a linear mixed model (LMM) and the lme4 package (Bates et al., 2015Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw. 2015; 67(1):1–48. https://doi.org/10.18637/jss.v067.i01
https://doi.org/10.18637/jss.v067.i01...
). The effect of the sampling month, salinity, and water transparency on the proportion of pregnant males was analyzed with generalized linear mixed models (GLMM), again using the lme4 package. In our models, the sampling area was considered a random variable in view of the varying size of the transects in order to control for the effect of spatial autocorrelation. To select the models, we started out by creating a null model which was then contrasted with models fitted with predictors using the function anova() (Zuur et al., 2009Zuur AF, Ieno EN, Walker N, Saveliev AA, Smith GM. Mixed effects models and extensions in ecology with R. New York, NY: Springer New York; 2009. https://doi.org/10.1007/978-0-387-87458-6
https://doi.org/10.1007/978-0-387-87458...
). Marginal and conditional R² values were calculated using the performance package (Lüdecke et al., 2021Lüdecke D, Ben-Shachar M, Patil I, Waggoner P, Makowski D. performance: An R package for assessment, comparison and testing of statistical models. J Open Source Softw. 2021; 6(60):3139. https://doi.org/10.21105/joss.03139
https://doi.org/10.21105/joss.03139...
).

Categorized as ‘bright’ or ‘dull’, coloring was expressed in relative frequencies. Orange, yellow, and red colors were considered ‘bright’ and were easily spotted in the environment. Brown, black, green, white, and grey were considered ‘dull’ and provided better camouflage. Using the chi-squared test (χ²) (R Development Core Team, 2023R Development Core Team. R: A language and environment for statistical computing, version 4.2.2. Vienna, Austria: R Foundation for Statistical Computing; 2023. Available from: https://www.r-project.org/
https://www.r-project.org/ ...
), we tested for possible correlations between coloring and season. Finally, the relative frequency of holdfast use was determined.

RESULTS

Predictors of population structure. At the sampling locations, the mean salinity was 25.9 (SD = 5.62) (Fig. 2A) while the mean water transparency was 0.62 m (SD = 0.24 m) (Fig. 2B). These two parameters varied significantly between the dry season and the rainy season (salinity: χ2 = 2686.70, df = 1; p <0.01; water transparency: χ2 = 1.84, df = 1; p<0.01). Salinity was higher during the former, and water transparency was greater during the latter (Tab. 1).

TABLE 1 |
Study variables potentially predictive of Hippocampus reidi population structure (salinity and water transparency) in the lower zone of the Pacoti River estuary (mean ± standard deviation, and range). Comparison of the dry season and the rainy season. Significant differences were determined with the generalized least squares (GLS) method.

Descriptors of population structure. In total, 248 specimens of H. reidi were registered in the 11 transects. Population density varied throughout the year, from 0.004 to 0.104 ind.m-2, with a mean density of 0.044 ind.m-2 (SD = 0.026). Density values varied significantly between the dry season and the rainy season (L.ratio = 7.206; p< 0.01).

Contrary to our expectations, seahorse population density was not correlated with sampling month, salinity, or water transparency in the lower zone of the Pacoti River estuary (χ2 = 21.112, df = 13, p= 0.07; conditional R2 = 0.062, marginal R2 = 0.000) (Fig. 2C; S2).

Our sample included 114 males and 116 females, indicating a sex ratio of 1:1 for the population (χ2 = 0.017, df = 1, p= 0.89) (Tab. 2), and 67 of the males were classified as pregnant. The proportion of pregnant males each month varied from 0% to 100% (Tab. 2), but pregnant males were more likely to be observed in the dry season and at sites with higher salinity (χ2 = 33.673, df = 11, p< 0.01; conditional R2 < 0.01, marginal R2 = 0.929) (Fig. 2D; Fig. 3).

The mean height of the observed specimens was 12.7 cm (SD = 2.02 cm; range: 5.5-17 cm). The smallest seahorse with a brood pouch measured 10 cm. Using this size as cut-off between adults and juveniles, 18 of the specimens observed during the complete study period were classified as juveniles. A strong correlation was seen between sampling month and body height (χ2 = 42.749; df = 11; p< 0.01; conditional R2 = 0.168; marginal R2 = 0.154) since the captured specimens were slightly larger in the dry season (13.2 cm, SD = 2.05) than in the rainy season (12.1 cm, SD = 1.84) (Fig. 2E).

TABLE 2 |
Number of males, females and juveniles of Hippocampus reidi registered in the lower zone of the Pacoti River estuary, along with sex ratios and the proportion of pregnant males. X2, dfand p are parameters of the chi-squared test (χ²).
FIGURE 2 |
Temporal variation of environmental variables: (A) salinity and (B) water transparency (cm), and Hippocampus reidi population variables: (C) population density (ind.m-2), (D) proportion of pregnant males (Y = pregnant male record, N = non-pregnant male record) and (E) individual height (cm), in the Pacoti River estuary, Ceará, Brazil, between December 2017 and November 2018. The months of the rainy season are highlighted in blue.

Eight color patterns were observed in the seahorse population of the Pacoti River estuary. Bright colors were predominant (Fig. 4A), with orange as the most common (44%), followed by brown, yellow, and red. Black, green, white, and grey were less common. The proportion of bright-colored specimens varied between the seasons (χ2 = 3.931, df = 1; p= 0.04), with bright colors being slightly more common in the rainy season (Fig. S3).

Seahorses were recorded using nine different substrates as holdfasts (Fig. 4B), the most common being white mangrove roots (L. racemosa; 39.9%), followed by sand (22.6%) and red mangrove roots (R. mangle; 17.3%). Less commonly used for anchoring were fallen trunks and branches, seagrass (Halodule wrightii Asch.), seaweeds, a native oyster species (Crassostrea sp. Sacco, 1897) and rocks. A few specimens were seen employing artificial holdfasts, such as abandoned fishing nets and ropes, and a few were observed while swimming in the water column.

FIGURE 3 |
Spatial variation in the proportion of pregnant males of Hippocampus reidi along the salinity gradient in the Pacoti River estuary, Ceará, Brazil, between December 2017 and November 2018. Y = pregnant male record, N = non-pregnant male record.
FIGURE 4 |
Proportion of color patterns (A) and holdfast use (B) of Hippocampus reidi in the Pacoti River estuary, Ceará, Brazil, between December 2017 and November 2018.

DISCUSSION

Our results show that the seahorse population density in the lower zone of the Pacoti River estuary was not influenced by salinity or water transparency. The significant variations observed in these parameters throughout the 1-year study period could not explain the density variation, suggesting the population structure of H. reidi over time is independent of the evaluated abiotic factors. On the other hand, the reproductive behavior was influenced by seasonal variation.

The mean population density was higher in this study than in earlier surveys of the Pacoti River estuary by Osório (2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.; 0.012 ind.m-2) and Silva (2018Silva VMM. Caracterização da população de Hippocampus reidi no estuário do rio Pacoti, Ceará. [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2018. Available from: http://www.repositorio.ufc.br/handle/riufc/36777
http://www.repositorio.ufc.br/handle/riu...
; 0.005 ind.m-2), possibly due to (i) differences in sampling methodology and/or (ii) differences in the location of the transects. Osório (2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.) and Silva (2018Silva VMM. Caracterização da população de Hippocampus reidi no estuário do rio Pacoti, Ceará. [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2018. Available from: http://www.repositorio.ufc.br/handle/riufc/36777
http://www.repositorio.ufc.br/handle/riu...
) used fixed 100 m2 transects to survey the population of H. reidi but, as pointed out by Foster, Vincent (2004Foster SJ, Vincent ACJ. Life history and ecology of seahorses: implications for conservation and management. J Fish Biol. 2004; 65(1):1–61. https://doi.org/10.1111/j.0022-1112.2004.00429.x
https://doi.org/10.1111/j.0022-1112.2004...
), fixed transects tend to yield lower densities than focal grids. Considering our methodology of selecting areas based on the potential occupation of H. reidi, we expected to find higher densities compared to surveys based on fixed transects. As for the location of the transects along the estuary, Silva (2018Silva VMM. Caracterização da população de Hippocampus reidi no estuário do rio Pacoti, Ceará. [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2018. Available from: http://www.repositorio.ufc.br/handle/riufc/36777
http://www.repositorio.ufc.br/handle/riu...
) reported that no specimens were observed at the sampling sites farthest from the river mouth, and that the low overall density of H. reidi may be explained by the absence of substrates for anchoring, such as mangrove roots, seaweeds and seagrass, due to the growing silting of some of the sampling sites. This silting and destruction of habitats and anchoring structures was also reported by local fishermen during pilot samplings (GAV, 2018, pers. obs.), indicating that some of the areas evaluated by Osório (2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.) may be devoid of seahorses today.

Despite considerable fluctuations between the dry season and the rainy season, salinity was not an explanatory factor of seahorse population density in the lower zone of the Pacoti River estuary. This rather unexpected finding may be due to the high tolerance to salinity of H. reidi, but it should be pointed out that current knowledge of the relationship between seahorse population density and salinity is based mainly on experimental studies, which have generally failed to investigate the tolerance of seahorses to temporal variations in salinity. As for water transparency, our results are supported by Claassens, Hodgson (2018Claassens L, Hodgson AN. Monthly population density and structure patterns of an endangered seahorse Hippocampus capensis: a comparison between natural and artificial habitats. J Fish Biol. 2018; 92(6):2000–15. https://doi.org/10.1111/jfb.13639
https://doi.org/10.1111/jfb.13639...
) who found turbidity to have no measurable influence on the distribution of H. capensis in South African estuaries. Thus, while luminosity plays an important role in prey visualization and therefore in seahorse foraging behavior (Felício et al., 2006Felício AKC, Rosa IL, Souto A, Freitas RHA. Feeding behavior of the longsnout seahorse Hippocampus reidi Ginsburg, 1933. J Ethol. 2006; 24(3):219–25. https://doi.org/10.1007/s10164-005-0189-8
https://doi.org/10.1007/s10164-005-0189-...
), in the lower zone of estuaries, where the water column is relatively transparent, it seems to have no impact on population structure.

Some other studies conducted in Brazilian semi-arid estuaries have identified environmental variables influencing the population density of seahorses, most especially the availability of habitats (Rosa et al., 2007Rosa IL, Oliveira TPR, Castro ALC, Moraes LES, Xavier JHA, Nottingham MC et al. Population characteristics, space use and habitat associations of the seahorse Hippocampus reidi (Teleostei: Syngnathidae). Neotrop Ichthyol. 2007; 5(3):405–14. https://doi.org/10.1590/S1679-62252007000300020
https://doi.org/10.1590/S1679-6225200700...
; Aylesworth et al., 2015Aylesworth LA, Xavier JH, Oliveira TPR, Tenorio GD, Diniz AF, Rosa IL. Regional-scale patterns of habitat preference for the seahorse Hippocampus reidi in the tropical estuarine environment. Aquat Ecol. 2015; 49(4):499–512. https://doi.org/10.1007/s10452-015-9542-3
https://doi.org/10.1007/s10452-015-9542-...
). Aylesworth et al. (2015Aylesworth LA, Xavier JH, Oliveira TPR, Tenorio GD, Diniz AF, Rosa IL. Regional-scale patterns of habitat preference for the seahorse Hippocampus reidi in the tropical estuarine environment. Aquat Ecol. 2015; 49(4):499–512. https://doi.org/10.1007/s10452-015-9542-3
https://doi.org/10.1007/s10452-015-9542-...
) also found smaller depth and higher temperature to be associated with greater density in a northeast Brazilian estuary. In a shallow estuary like Pacoti, especially in the lower zone, depth and temperature are not expected to vary throughout the year enough to impact seahorse population density, matching the pattern of other estuaries in the semi-arid region (Pinto, 2023Pinto LM. Padrões de diversidade espaço-temporal da assembleia de peixes estuarinos da costa semiárida brasileira: Efeitos da influência marinha em diferentes escalas. [PhD Thesis]. Fortaleza: Universidade Federal do Ceará; 2023. Available from: http://www.repositorio.ufc.br/handle/riufc/71492
http://www.repositorio.ufc.br/handle/riu...
). It should be kept in mind that much of our knowledge of the natural history and ecology of seahorses is based on spatial distribution data, not temporal variation, something that may explain the discrepancy between our findings and the literature. Studies evaluating temporal variations of these parameters and their possible correlations with seahorse populations in such ecosystems should therefore be encouraged.

The sex ratio observed in this study (1:1) is common for seahorse populations, most likely due to their monogamous behavior in each reproductive season (Foster, Vincent, 2004Foster SJ, Vincent ACJ. Life history and ecology of seahorses: implications for conservation and management. J Fish Biol. 2004; 65(1):1–61. https://doi.org/10.1111/j.0022-1112.2004.00429.x
https://doi.org/10.1111/j.0022-1112.2004...
). Monogamy tends to increase reproductive success rates in fishes that, like seahorses, occur in low density and have low mobility (Vincent, Sadler, 1995Vincent ACJ, Sadler LM. Faithful pair bonds in wild seahorses, Hippocampus whitei. Anim Behav. 1995; 50(6):1557–69. https://doi.org/10.1016/0003-3472(95)80011-5
https://doi.org/10.1016/0003-3472(95)800...
). An equitable sex ratio is suggestive of a healthy population not affected by sex-specific impacts or pressure.

The presence of pregnant males in almost all the sampling months (exceptions were January and March) indicates that reproduction occurs throughout the whole year, as reported by Silveira (2005Silveira RB. Dinâmica Populacional do Cavalo-marinho Hippocampus reidi no manguezal de Maracaípe, Ipojuca, Pernambuco, Brasil. [PhD Thesis]. Porto Alegre: Pontifícia Universidade Católica do Rio Grande do Sul; 2005. Available from: https://hdl.handle.net/10923/5335
https://hdl.handle.net/10923/5335...
), and corroborates the claim that seahorses have longer productive periods in the tropics than in temperate regions (Foster, Vincent, 2004Foster SJ, Vincent ACJ. Life history and ecology of seahorses: implications for conservation and management. J Fish Biol. 2004; 65(1):1–61. https://doi.org/10.1111/j.0022-1112.2004.00429.x
https://doi.org/10.1111/j.0022-1112.2004...
).

Pregnant males were more frequent in June and July, as salinity increased and stabilized around 30, meaning the newborn were exposed to less osmotic stress. In contrast, Osório (2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.) observed more pregnant males in the first semester, coinciding with the rainy season. The timing and duration of the reproductive season are influenced by the availability of food and environmental variables affecting the development and growth of the fry (Vincent, Giles, 2003Vincent ACJ, Giles BG. Correlates of reproductive success in a wild population of Hippocampus whitei. J Fish Biol. 2003; 63(2):344–55. https://doi.org/10.1046/J.1095-8649.2003.00154.X
https://doi.org/10.1046/J.1095-8649.2003...
). On average, salinities were higher in Osório (2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.) than in the present study, suggesting that seahorse populations were exposed to less osmotic stress that year, despite the rainy season. In Ceará, the dry season coincides with windier weather (INMET, 2023aInstituto Nacional de Meteorologia (INMET). Normais climatológicas do Brasil 1991-2020. 2023a. Available from: https://portal.inmet.gov.br/normais#
https://portal.inmet.gov.br/normais#...
), a factor pointed out by Mai, Velasco (2012Mai ACG, Velasco G. Population dynamics and reproduction of wild longsnout seahorse Hippocampus reidi. J Mar Biol Assoc U K. 2012; 92(2):421–27. https://doi.org/10.1017/S0025315411001494
https://doi.org/10.1017/S002531541100149...
), increasing the potential for dispersal of the planktonic fry of H. reidi.

The registered seahorses were on average larger in the dry season than in the rainy season, contradicting Osório (2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.) who registered no seasonal difference in size for the same estuary. Adult seahorses have a greater capacity for osmoregulation; thus, the increased frequency of large seahorses in the dry season may not be related to fluctuations in salinity but to other environmental factors not evaluated in this study.

The specimens of H. reidi observed for this study in the Pacoti River estuary were on average larger than the seahorses previously observed in Ceará (Rosa et al., 2007Rosa IL, Oliveira TPR, Castro ALC, Moraes LES, Xavier JHA, Nottingham MC et al. Population characteristics, space use and habitat associations of the seahorse Hippocampus reidi (Teleostei: Syngnathidae). Neotrop Ichthyol. 2007; 5(3):405–14. https://doi.org/10.1590/S1679-62252007000300020
https://doi.org/10.1590/S1679-6225200700...
; Osório, 2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.; Silva, 2018Silva VMM. Caracterização da população de Hippocampus reidi no estuário do rio Pacoti, Ceará. [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2018. Available from: http://www.repositorio.ufc.br/handle/riufc/36777
http://www.repositorio.ufc.br/handle/riu...
). In fact, the seahorses observed in Ceará by Osório (2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.) and Rosa et al. (2007Rosa IL, Oliveira TPR, Castro ALC, Moraes LES, Xavier JHA, Nottingham MC et al. Population characteristics, space use and habitat associations of the seahorse Hippocampus reidi (Teleostei: Syngnathidae). Neotrop Ichthyol. 2007; 5(3):405–14. https://doi.org/10.1590/S1679-62252007000300020
https://doi.org/10.1590/S1679-6225200700...
) are on average smaller than the seahorses observed in other Brazilian states (Rosa et al., 2007Rosa IL, Oliveira TPR, Castro ALC, Moraes LES, Xavier JHA, Nottingham MC et al. Population characteristics, space use and habitat associations of the seahorse Hippocampus reidi (Teleostei: Syngnathidae). Neotrop Ichthyol. 2007; 5(3):405–14. https://doi.org/10.1590/S1679-62252007000300020
https://doi.org/10.1590/S1679-6225200700...
; Carmo et al., 2022Carmo TF, Santos LN, Bertoncini AA, Freret-Meurer NV. Population structure of the seahorse Hippocampus reidi in two Brazilian estuaries. Ocean Coast Res. 2022; 70:e22009. https://doi.org/10.1590/2675-2824070.21016tfdc
https://doi.org/10.1590/2675-2824070.210...
). The mean height of the seahorses registered in Pacoti for our study is closer to the mean height found in other states and is also compatible with the findings of Silva (2018Silva VMM. Caracterização da população de Hippocampus reidi no estuário do rio Pacoti, Ceará. [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2018. Available from: http://www.repositorio.ufc.br/handle/riufc/36777
http://www.repositorio.ufc.br/handle/riu...
) for the same estuary, indicating an improvement in the condition of the local seahorse population, possibly as a consequence of the ban on seahorse fisheries and trade in Brazil through MMA directive #445 of 17 Dec 2014 (MMA, 2014Ministério do Meio Ambiente (MMA). Portaria No 445, de 17 de dezembro de 2014. Brazil: Diário Oficial da União, Seção 1, p.126; 2014.). Since large specimens are the most marketable (Vincent et al., 2011Vincent ACJ, Foster SJ, Koldewey HJ. Conservation and management of seahorses and other Syngnathidae. J Fish Biol. 2011; 78(6):1681–724. https://doi.org/10.1111/j.1095-8649.2011.03003.x
https://doi.org/10.1111/j.1095-8649.2011...
), the increase in mean body height of the registered specimens would seem to reflect a reduction in fishing pressure.

The population of seahorses in the Pacoti River estuary currently displays a predominantly orange coloring, contrasting with the black and brown coloring reported in earlier studies (Osório, 2008Osório FM. Estudo populacional do cavalo-marinho Hippocampus reidi Ginsburg, 1933 (Teleostei: Syngnathidae) em dois estuários cearenses [Master Dissertation]. Fortaleza: Universidade Federal do Ceará; 2008.). Bright-colored specimens are better priced in the aquarium trade (Rosa et al., 2005Rosa IML, Alves RRN, Bonifácio KM, Mourão JS, Osório FM, Oliveira TPR et al. Fishers’ knowledge and seahorse conservation in Brazil. J Ethnobiol Ethnomed. 2005; 1:12. https://doi.org/10.1186/1746-4269-1-12
https://doi.org/10.1186/1746-4269-1-12...
, 2011Rosa IL, Oliveira TPR, Osório FM, Moraes LE, Castro ALC, Barros GML et al. Fisheries and trade of seahorses in Brazil: Historical perspective, current trends, and future directions. Biodivers Conserv. 2011; 20(9):1951–71. https://doi.org/10.1007/s10531-011-0068-2
https://doi.org/10.1007/s10531-011-0068-...
; Loiola et al., 2022Loiola SC, Pinto LM, Kobayashi RK, Sánchez-Botero JI, Sequeira Garcez D. Conhecimento empírico de pescadores artesanais como base para a conservação do cavalo-marinho Hippocampus reidi (Teleostei: Syngnathidae) no estuário do rio Pacoti (CE). In: Garcez DS, Sánchez-Botero JI, editors. Conhecimento local e o manejo de recursos pesqueiros de uso comum: Experiências nos litorais do Maranhão, Ceará e Pernambuco. Fortaleza: Imprensa Universitária; 2022. p.219–80.;) and would seem to be poorly camouflaged in the sandy or muddy environments near the river mouth. It is reasonable to assume that the reduced fishing pressure has allowed more bright-colored specimens to remain in the environment; on the other hand, seahorses are known for their crypsis (Lourie et al., 2004Lourie SA, Foster SJ, Cooper EWT, Vincent ACJ. A guide to the identification of seahorses. Washington D.C.: University of British Columbia and World Wildlife Fund; 2004.). Some have argued that a bright, disruptive coloring with blotches and spots might confound predators by obscuring the body outline, but the bright-colored specimens of H. reidi observed by Duarte et al. (2019Duarte M, Gawryszewski FM, Ramineli S, Bessa E. Disruptive coloration and habitat use by seahorses. Neotrop Ichthyol. 2019; 17(4):190064. https://doi.org/10.1590/1982-0224-20190064
https://doi.org/10.1590/1982-0224-201900...
) made no perceptible effort to blend in with the background. In any case, the color patterns observed in our study suggest that the fishing pressure on H. reidi in the lower zone of the Pacoti River estuary has decreased.

The seahorses in our study area displayed a preference for white mangrove roots (L. racemosa). Being poor swimmers, seahorses rely heavily on holdfasts like roots and trunks to which they anchor using their prehensile tail. The population density of H. reidi has been shown to be directly associated with habitat complexity (Aylesworth et al., 2015Aylesworth LA, Xavier JH, Oliveira TPR, Tenorio GD, Diniz AF, Rosa IL. Regional-scale patterns of habitat preference for the seahorse Hippocampus reidi in the tropical estuarine environment. Aquat Ecol. 2015; 49(4):499–512. https://doi.org/10.1007/s10452-015-9542-3
https://doi.org/10.1007/s10452-015-9542-...
), which translates into ample availability of protective holdfasts, and a microhabitat with mangrove roots and seagrass is considered more complex than a sand bottom (Whitfield, 2017Whitfield AK. The role of seagrass meadows, mangrove forests, salt marshes and reed beds as nursery areas and food sources for fishes in estuaries. Rev Fish Biol Fish. 2017; 27:75–110. https://doi.org/10.1007/s11160-016-9454-x
https://doi.org/10.1007/s11160-016-9454-...
). Over half the seahorses observed in our study (57.2%) used the roots of L. racemosa and R. mangle as holdfast, matching the findings of other studies from Northeastern Brazil (Aylesworth et al., 2015Aylesworth LA, Xavier JH, Oliveira TPR, Tenorio GD, Diniz AF, Rosa IL. Regional-scale patterns of habitat preference for the seahorse Hippocampus reidi in the tropical estuarine environment. Aquat Ecol. 2015; 49(4):499–512. https://doi.org/10.1007/s10452-015-9542-3
https://doi.org/10.1007/s10452-015-9542-...
). In short, the seahorses observed in our study displayed a preference forcomplex holdfasts, and seahorse occurrence appeared to be associated with mangrove vegetation. Therefore, the preservation of the local mangrove forest is essential for the maintenance of H. reidi populations in this ecosystem (Ternes et al., 2023Ternes MLF, Freret-Meurer NV, Nascimento RL, Vidal MD, Giarrizzo T. Local ecological knowledge provides important conservation guidelines for a threatened seahorse species in mangrove ecosystems. Front Mar Sci. 2023; 10.1139368. https://doi.org/10.3389/fmars.2023.1139368
https://doi.org/10.3389/fmars.2023.11393...
, 2016Ternes MLF, Gerhardinger LC, Schiavetti A. Seahorses in focus: Local ecological knowledge of seahorse-watching operators in a tropical estuary. J Ethnobiol Ethnomed. 2016; 12:52. https://doi.org/10.1186/s13002-016-0125-8
https://doi.org/10.1186/s13002-016-0125-...
).

Our results show that the population density of H. reidi in the lower zone of Brazilian semi-arid estuaries can fluctuate over time independently of annual variations in salinity and water transparency, likely due to environmental factors not evaluated in this study. The registered seahorses reproduced throughout the year, peaking in the dry season, and pregnant males were more likely to be observed under higher salinity, possibly as an adaptive strategy to protect juveniles from osmotic stress. The occurrence of H. reidi in local estuaries is positively associated with the presence of mangrove vegetation, highlighting the vulnerability of seahorses to mangrove degradation. Thus, to conserve local seahorse populations, mangrove forests should be protected, the existing ban on fishing and trade should be maintained, and the ecosystem should be safeguarded against water pollution.

ACKNOWLEDGEMENTS

The authors would like to thank the Universidade Federal do Ceará (UFC), especially the Laboratório de Ecologia Aquática e Conservação (LEAC). We are grateful to Maria and Tasso (fishers in the Pacoti River community) and to Wallace A. Sousa and Felipe B. Pereira for their assistance with field data collection. Also, thanks to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Programa Institucional de Bolsas de Iniciação Científica (PIBIC scholarship) and for financial support through the MCTI/CNPq Program (Grant #28/2018, file #423628/2018–6, and Grant #63/2022, file #409354/2022–8). CASRF would like to thank CNPq for the postdoctoral scholarship (Grant #153021/2022–5).

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Valentim GA, Pinto LM, Gurgel-Lourenço RC, Rodrigues-Filho CAS, Sánchez-Botero JI. Population structure of the seahorse Hippocampus reidi (Syngnathiformes: Syngnathidae) in a Brazilian semi-arid estuary. Neotrop Ichthyol. 2023; 21(4):e230004. https://doi.org/10.1590/1982-0224-2023-0004

Edited-by

Osmar Luiz

Publication Dates

  • Publication in this collection
    04 Dec 2023
  • Date of issue
    2023

History

  • Received
    10 Jan 2023
  • Accepted
    18 Sept 2023
Sociedade Brasileira de Ictiologia Neotropical Ichthyology, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Universidade Estadual de Maringá., Av. Colombo, 5790, 87020-900, Phone number: +55 44-3011-4632 - Maringá - PR - Brazil
E-mail: neoichth@nupelia.uem.br