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Mangrove-associated fish assemblages off the southern Panama Bight region (tropical eastern Pacific)

ABSTRACT

The Panama Bight ecoregion (PBE) in the eastern Pacific contains probably the best developed mangrove forests in the American continent. Fishes inhabiting the mangrove-estuary mosaic play fundamental ecological roles and sustain the artisanal fishery operating there. Here, using data collected along ~300 km between 2012 and 2017, we examine the spatial dynamics of mangrove fish assemblages that undertake intertidal migrations in the southern part of the PBE (southern Colombian Pacific coast), where the largest and least disturbed mangroves of Colombia are located. Sixty-one fish species used intertidal mangrove habitats in these areas, constituting ~30% of all fishes inhabiting the whole mosaic of mangrove habitats in this ecoregion. Species within Clupeidae, Ariidae, Centropomidae and Tetraodontidae, all common in mangroves of the eastern Pacific, were the most dominant. Half of the fish species found are commercially important to the artisanal fishery. Differences in fish community structure could be related to salinity differences, but other environmental and ecological factors could also play a role in explaining these differences. A better understanding of the ecological role of mangrove fishes in the region could be gained by examining the ichthyofauna of other habitats within the mosaic and their trophic relationships.

Keywords:
Colombia; Community ecology; Estuarine fishes; Macrotidal estuaries; Mangroves fishes

RESUMEN

La ecorregión del Panama Bight (EPB) en el océano Pacifico oriental contiene probablemente los bosques de manglar más desarrollados de America. Los peces que habitan el mosaico estuario-manglar juegan papeles ecológicos fundamentales y sostienen las pesquerías artesanales que operan allí. Usando datos colectados a lo largo de ~300 km entre 2012 y 2017, examinamos la dinámica espacial de ensamblajes de peces de manglar que realizan migraciones intermareales en el EPB sur (costa sur del Pacífico colombiano), donde se encuentran los manglares más grandes y menos intervenidos de Colombia. Sesenta y un especies de peces ingresaron en zonas intermareales de manglar, constituyendo ~30% de todos los peces que pueden ser encontrados en el mosaico de hábitats de manglar de esta ecoregión. Especies de Clupeidae, Ariidae, Centropomidae y Tetraodontidae, todas comunes en manglares del Pacífico oriental, fueron las más dominantes. La mitad de los peces encontrados son importantes comercialmente para la pesquería artesanal. Las diferencias en la estructura de la comunidad pueden estar relacionadas con diferencias en salinidad, pero otros factores ambientales y ecológicos podrían también jugar un rol explicando las diferencias encontradas. Un mejor entendimiento del rol ecológico de los peces de manglar de la región podría alcanzarse examinando la ictiofauna de otros hábitats de este mosaico y sus relaciones tróficas.

Palabras clave:
Colombia; Ecologia de comunidades; Estuarios macro-mareales; Peces de manglar

INTRODUCTION

More than 20% of mangrove areas in the world are located in Latin America and the Caribbean (Bunting et al., 2018Bunting P, Rosenqvist A, Lucas RM, Rebelo LM, Hilarides L, Thomas N et al. The Global Mangrove Watch - A new 2010 global baseline of Mangrove extent. Remote Sens. 2018; 10(10):1669. https://doi.org/10.3390/rs10101669
https://doi.org/10.3390/rs10101669...
). These mangroves belong to the Atlantic-East Pacific mangrove biogeographic region (AEP), which is considered low in species richness if compared with the Indo-Pacific mangrove region (Lee et al., 2017Lee SY, Jones EBG, Diele K, Castellanos-Galindo GA, Nordhaus I. Chapter 3: Biodiversity. In: Rivera-Monroy VH, Lee SY, Kristensen E, Twilley RR, editors. Mangrove ecosystems: A global biogeographic perspective. Structure, function and services. Cham: Springer ; 2017. p.55-86). Nevertheless, mangroves in the AEP are still important habitats for a diverse range of coastal taxa that are threatened by various human-related stressors acting at different scales (e.g., urban expansion; Castellanos-Galindo et al., 2017Castellanos-Galindo GA, Kluger LC, Tompkins P. Panama impotent mangrove laws. Science. 2017; 355(6328):918-19. https://doi.org/10.1126/science.aam6909
https://doi.org/10.1126/science.aam6909...
). A conspicuous part of this biodiversity is represented by fishes that play key ecological roles like transporting energy within mangroves and adjacent shallow-water ecosystems (Nagelkerken et al., 2015Nagelkerken I, Sheaves M, Baker R, Connolly RM. The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish Fish . 2015; 16(2):362-71. https://doi.org/10.1111/faf.12057
https://doi.org/10.1111/faf.12057...
). Many of these fishes are often targeted by coastal small-scale or industrial fisheries providing food for people and income to local and national economies (Aburto-Oropeza et al., 2008Aburto-Oropeza O, Ezcurra E, Danemann G, Valdez V, Murray M, Sala E. Mangroves in the Gulf of California increase fishery yields. Proc Natl Acad Sci USA. 2008; 105(30):10456-59. https://doi.org/10.1073/pnas.0804601105
https://doi.org/10.1073/pnas.0804601105...
, Herrón et al., 2019Herrón P, Castellanos-Galindo GA, Stäbler M, Díaz JM, Wolff M. Towards ecosystem-based assessment and management of small-scale and multi-ear fisheries: Insights from the Tropical Eastern Pacific. Front Mar Sci. 2019; 6(127):1-17. https://doi.org/10.3389/fmars.2019.00127
https://doi.org/10.3389/fmars.2019.00127...
).

In the Latin American and Caribbean region, Colombia ranks 4th in mangrove areal extent after Brazil, Mexico, and Venezuela (Hamilton, Casey, 2016Hamilton SE, Casey D. Creation of a high spatio-temporal resolution global database of continuous mangrove forest cover for the 21st century (CGMFC- 21). Global Ecol Biogeogr. 2016; 25(6):729-38. https://doi.org/10.1111/geb.12449
https://doi.org/10.1111/geb.12449...
; Mejía-Rentería et al., 2018Mejía-Renteria JC, Castellanos-Galindo GA, Cantera-Kintz JR, Hamilton SE. A comparison of Colombian Pacific mangrove extent estimations: implications for the conservation of a unique Neotropical tidal forest. Estuar Coast Shelf Sci . 2018; 212:233-40. https://doi.org/10.1016/j.ecss.2018.07.020
https://doi.org/10.1016/j.ecss.2018.07.0...
). Having coasts in both Caribbean and Pacific coasts, the country harbors different mangrove ecosystem types, being the ones in the Pacific the most extensive. These mangroves are undisturbed compared to the ones located close to the few large cities in this coast, and at the same time they poorly studied due to their difficult accessibility (i.e., no coastal road connecting them to the rest of the country; Castellanos-Galindo et al., 2015Castellanos-Galindo GA, Cantera JR, Saint-Paul U, Ferrol-Schulte D. Threats to mangrove social-ecological systems in the most luxuriant coastal forests of the Neotropics. Biodivers Conserv. 2015; 24:701-04. https://doi.org/10.1007/s10531-014-0827-y
https://doi.org/10.1007/s10531-014-0827-...
, 2021Castellanos-Galindo GA, Kluger LC, Camargo MA, Cantera J, Pineda JEM, Blanco-Libreros JF et al. Mangrove research in Colombia: temporal trends, geographical coverage and research gaps. Estuar Coast Shelf Sci. 2021; 248:106799. https://doi.org/10.1016/j.ecss.2020.106799
https://doi.org/10.1016/j.ecss.2020.1067...
). Mangroves in the Pacific coast of Colombia are predominately distributed in the southern 2/3 of the extremely rainy (~3000 mm annual rainfall) macro and mesotidal coastline where extensive alluvial plains and two major deltas occur, i.e., The Patía and Mira River deltas (Correa, Morton, 2010Correa I, Morton R. Pacific coast of Colombia. In: Bird ECF, editor. Encyclopedia of the world’s coastal landforms. Dordrecht: Springer ; 2010. p.193-97.). It is in this ~500 km coastal stretch where the tallest mangroves of the American continent are located with tree heights reaching almost 60 m (Simard et al., 2019Simard M, Fatoyinbo L, Smetanka C, Rivera-Monroy VH, Castañeda-Moya E, Thomas N et al. Mangrove canopy height globally related to precipitation, temperature and cyclone frequency. Nat Geosci. 2019a; 12:40-45. https://doi.org/10.1038/s41561-018-0279-1
https://doi.org/10.1038/s41561-018-0279-...
; Castellanos-Galindo et al., 2021Castellanos-Galindo GA, Casella E, Tavera H, Zapata Padilla LA, Simard M. Structural characteristics of the tallest mangrove forests of the American Continent: A comparison of ground-based, drone and radar measurements. Front For Glob Change. 2021; 4:732468. https://doi.org/10.3389/ffgc.2021.732468
https://doi.org/10.3389/ffgc.2021.732468...
).

A long-standing paradigm, but one with poor scientific support, has claimed that 75 % of all commercially caught fish depend directly on mangrove ecosystems (Sheaves, 2017Sheaves M. How many fish use mangroves? The 75% rule an ill-defined and poorly validated concept. Fish Fish . 2017; 18(4):778-89. https://doi.org/10.1111/faf.12213
https://doi.org/10.1111/faf.12213...
). This has driven the conservation agenda and has helped to make the case for mangrove protection worldwide in recent years. However, more careful examinations of the dependence of fish on mangroves and specially those fish targeted by fisheries restrict the number of mangrove-associated fish well below the 75 % number (e.g., Aburto-Oropeza et al., 2008Aburto-Oropeza O, Ezcurra E, Danemann G, Valdez V, Murray M, Sala E. Mangroves in the Gulf of California increase fishery yields. Proc Natl Acad Sci USA. 2008; 105(30):10456-59. https://doi.org/10.1073/pnas.0804601105
https://doi.org/10.1073/pnas.0804601105...
). This confusion is partly due to the difficulties in differentiating what constitutes a mangrove-dependent fish (see Zu Ermgassen et al., 2020Zu Ermgassen PSE, Grove T, Nagelkerken I. Global affiliation of juvenile fishes and invertebrates with mangrove habitats. Bull Mar Sci. 2020; 96(3):403-14. https://doi.org/10.5343/bms.2019.0044
https://doi.org/10.5343/bms.2019.0044...
). Coastal fishes occupy a mosaic of habitats that could be defined as a seascape nursery (Nagelkerken et al., 2015Nagelkerken I, Sheaves M, Baker R, Connolly RM. The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish Fish . 2015; 16(2):362-71. https://doi.org/10.1111/faf.12057
https://doi.org/10.1111/faf.12057...
). In this seascape, mangroves may play an important role for certain fish species whereas for others not. Differentiating and understanding how different habitats within a certain seascape nursery benefit fishes can bring valuable insights for habitat conservation or even for fisheries management in mangrove areas (Brown et al., 2018Brown CJ, Broadley A, Adame MF, Branch TA, Turschwell MP, Connolly RM. The assessment of fishery status depends on fish habitats. Fish Fish. 2018; 20(1):1-14. https://doi.org/10.1111/faf.12318
https://doi.org/10.1111/faf.12318...
).

The study of the relationship between mangroves and fish has significantly increased in the last two decades. A couple of reviews in the last ~15 years ago summarized our understanding of this relationship at the global level (see Faunce, Serafy, 2006Faunce CH, Serafy JE. Mangroves as fish habitat: 50 years of field studies. Mar Ecol Prog Ser . 2006; 318:1-18. http://doi.org/10.3354/meps318001
http://doi.org/10.3354/meps318001...
; Nagelkerken et al., 2008Nagelkerken I, Blaber SJM, Bouillon S, Green P, Haywood M, Kirton LG et al. The habitat function of mangroves for terrestrial and marine fauna: A review. Aquat Bot. 2008; 89(2):155-85. https://doi.org/10.1016/j.aquabot.2007.12.007
https://doi.org/10.1016/j.aquabot.2007.1...
). At local scales, salinity has been frequently identified as a major driver of fish community organization in mangroves (Ley et al., 1999Ley J, McIvor CC, Montague CL. Fishes in mangrove prop-root habitats of northeastern Florida Bay: distinct assemblages across an estuarine gradient. Estuar Coast Shelf Sci . 1999; 48(6):701-23. https://doi.org/10.1006/ecss.1998.0459
https://doi.org/10.1006/ecss.1998.0459...
). Salinity can also interact with physical and seascape characteristics of mangroves settings explaining much of the variability observed at the community level (Castellanos-Galindo, Krumme, 2015Castellanos-Galindo GA, Krumme U. Tides, salinity, and biogeography affect fish assemblage structure and function in macrotidal mangroves of the neotropics. Ecosystems . 2015; 18:1165-78. https://doi.org/10.1007/s10021-015-9887-4
https://doi.org/10.1007/s10021-015-9887-...
; Bradley et al., 2021Bradley M, Nagelkerken I, Baker R, Travers M, Sheaves M. Local environmental context structures Animal-Habitat Associations across Biogeographic Regions. Ecosystems. 2021; 1-15. https://doi.org/10.1007/s10021-021-00651-7
https://doi.org/10.1007/s10021-021-00651...
) Considering larger scales, Sheaves (2012Sheaves M. Ecosystem equivalence and the ability to generalise: insights from global consistencies in mangrove fish assemblages. Mar Ecol Prog Ser . 2012; 461:137-49. https://doi.org/10.3354/meps09774
https://doi.org/10.3354/meps09774...
) compiled 76 studies from around the world to understand the functional characteristics of mangrove fishes. These overviews have helped to identify geographical data gaps and also to motivate research in those areas less well studied (e.g., Eastern Pacific - Castellanos-Galindo, Krumme, 2013aCastellanos-Galindo GA, Krumme U. Mangrove fish assemblages from data-sparse regions and the measurement of ecological equivalence: Comment on Sheaves (2012). Mar Ecol Prog Ser. 2013a; 474:299-302. https://doi.org/10.3354/meps10242
https://doi.org/10.3354/meps10242...
; Castellanos-Galindo et al., 2013Castellanos-Galindo GA, Krumme U, Rubio EA, Saint-Paul U. Spatial variability of mangrove fish assemblage composition in the tropical eastern Pacific Ocean. Rev Fish Biol Fish. 2013; 23:69-86. https://doi.org/10.1007/s11160-012-9276-4
https://doi.org/10.1007/s11160-012-9276-...
; Western Atlantic - Vilar et al., 2013Vilar CC, Joyeux JC, Giarrizzo T, Spach HL, Vieira JP, Vaske-Junior T. Local and regional ecological drivers of fish assemblages in Brazilian estuaries. Mar Ecol Prog Ser . 2013; 485:181-97. https://doi.org/10.3354/meps10343
https://doi.org/10.3354/meps10343...
). Nevertheless, several gaps in the understanding of regional ecological patterns persist in areas of the Eastern Pacific like Central America and the southern portion of Panama Bight mangroves including Colombia, Ecuador and Peru.

This manuscript presents data on mangrove fish assemblages of the Panama Bight mangrove eco-region collected between 2012 and 2017 that help to fill in a gap in the knowledge of mangrove-associated fish communities in the Eastern Pacific region (West coast of the American continent). We specifically examined the small-scale variability (10s of km) in fish community structure and its relation to salinity in an area dominated by highly developed mangrove forests (southern Colombian Pacific coast).

MATERIAL AND METHODS

Study area. The Panama Bight mangrove eco-region includes the coasts of Panama, Colombia, and Ecuador in the western coast of the Americas and is part of the larger tropical eastern Pacific region that spans the continental shores of Mexico to Peru plus five oceanic islands (Robertson, Cramer, 2009Robertson DR, Cramer KL. Shore-fishes and biogeographic subdivisions of the Tropical Eastern Pacific. Mar Ecol Prog Ser . 2009; 380:1-17. https://doi.org/10.3354/meps07925
https://doi.org/10.3354/meps07925...
). The Colombian Pacific is inserted in these two regions and extends for ca. 1400 km between Panama and Ecuador. The southern 2/3 of the coast are dominated by mangrove forests that thrive within a matrix of alluvial plains and barrier islands (Martinez et al., 1995Martinez JO, Gonzalez JL, Pilkey OH, Neal WJ. Tropical barrier islands of Colombia’s Pacific coast. J Coast Res. 1995; 11(2):432-53. Available from: https://www.jstor.org/stable/4298350
https://www.jstor.org/stable/4298350...
). Mangrove extent in this part of the coast ranges between 110000 and 130000 ha (Mejía-Rentería et al., 2018Mejía-Renteria JC, Castellanos-Galindo GA, Cantera-Kintz JR, Hamilton SE. A comparison of Colombian Pacific mangrove extent estimations: implications for the conservation of a unique Neotropical tidal forest. Estuar Coast Shelf Sci . 2018; 212:233-40. https://doi.org/10.1016/j.ecss.2018.07.020
https://doi.org/10.1016/j.ecss.2018.07.0...
) and represent more than 70% of all mangrove area in the whole country. Rhizophora spp. mangrove trees of up to 55 m heights (Simard et al., 2019Simard M, Fatoyinbo L, Smetanka C, Rivera-Monroy VH, Castañeda-Moya E, Thomas N et al. Mangrove canopy height globally related to precipitation, temperature and cyclone frequency. Nat Geosci. 2019a; 12:40-45. https://doi.org/10.1038/s41561-018-0279-1
https://doi.org/10.1038/s41561-018-0279-...
) are the dominant species but at least five more mangrove tree species can be found in this coast. Most artisanal fisheries in the Colombian Pacific coast operate in these mangrove-dominated areas and target several resources that can live in close proximity to mangrove areas (Castellanos-Galindo, Zapata, 2019Castellanos-Galindo GA, Zapata LA. Small-Scale fisheries on the Pacific Coast of Colombia: Historical context, current situation, and future challenges In: Salas S, Barragán-Paladine M, Chuenpagdee R, editors. Viability and sustainability of Small-Scale Fisheries in Latin America and the Caribbean. Cham: Springer; 2019. p.79-100. https://doi.org/10.1007/978-3-319-76078-0_4
https://doi.org/10.1007/978-3-319-76078-...
; Herrón et al., 2019Herrón P, Castellanos-Galindo GA, Stäbler M, Díaz JM, Wolff M. Towards ecosystem-based assessment and management of small-scale and multi-ear fisheries: Insights from the Tropical Eastern Pacific. Front Mar Sci. 2019; 6(127):1-17. https://doi.org/10.3389/fmars.2019.00127
https://doi.org/10.3389/fmars.2019.00127...
). Salinities in this meso and macrotidal coast are typically < 30 psu and precipitation is extremely high with annual rainfall ranging from ca. 8 m in the central coast to 3 m in the southern coast close to the border with Ecuador. Primary data for this manuscript were collected in the southernmost province of the Colombian Pacific (Nariño) bordering the Ecuadorian coast (Fig. 1).

FIGURE 1
| Southern Colombian Pacific (Nariño province) coast with the seven mangrove sampling sites of this study. Mangrove tree height estimates were derived from Simard et al. (2019bSimard M, Fatoyinbo T, Smetanka C, Rivera-Monroy VH, Castaneda E, Thomas N et al. Global mangrove distribution, aboveground biomass, and canopy height [Internet]. Tennessee; 2019b. https://doi.org/10.3334/ORNLDAAC/1665
https://doi.org/10.3334/ORNLDAAC/1665...
). The five southernmost localities lie within the Tumaco-Cabo Manglares area.

Data collection. Fish sampling in intertidal mangrove creeks was carried out between 2012 and 2017 at seven different localities in the southern Colombian Pacific coast (Fig. 1). Sampling in all locations followed the methodology described in Castellanos-Galindo, Krumme (2013bCastellanos-Galindo GA, Krumme U. Tidal, diel and seasonal effects on intertidal mangrove fish in a high-rainfall area of the Tropical Eastern Pacific. Mar Ecol Prog Ser . 2013b; 494:249-65. https://doi.org/10.3354/meps10512
https://doi.org/10.3354/meps10512...
), where small intertidal mangrove creeks (mouths ~10 m, internal lengths ~100 m) were blocked with nets (20 m x 4 m, stretch mesh size 12 mm) at high tide. After blocking the small creeks at high tide with the nets, fishes that enter with the rising tide into the mangroves are captured on the next low tide after ~6 h. This methodology allows effectively sampling the part of the fish community that exploits intertidal mangrove habitats in meso and macro-tidal regimes. During each sampling, surface salinity at high tide was measured at the entrance of each mangrove creek. Mulatos and Iscuande localities were more intensely sampled than the rest of the other localities (total n = 18 block net samplings from 2012 to 2015), whereas due to logistical constraints the other five localities were only sampled in 2017 (n = 2 per sampling locality) (see Tab. S1 ). These seven localities cover almost the whole southern mangrove-dominated coast of the Colombian Pacific where the tallest mangrove forests of the Americas are located (Fig. 1). For data analyses, these localities were grouped into high salinity (> 20 psu: Boca Grande, Chontal, Mulatos, and Teheran), medium salinity (15-20 psu: Curay and Trujillo) and low salinity (< 15 psu: Iscuandé) sites (Fig. 1).

After capture, fishes were identified, measured (total length, TL), and weighed wet (g ± 0.1). Each fish species was also assigned to one spatial and trophic guild group according to collected stomach content information or derived from Elliott et al. (2007Elliot M, Whitfield AK, Potter IC, Blaber SJM, Cyrus DP, Nordlie FG et al. The guild approach to categorizing estuarine fish assemblages: a global review. Fish Fish . 2007; 8(3):241-68. https://doi.org/10.1111/j.1467-2679.2007.00253.x
https://doi.org/10.1111/j.1467-2679.2007...
), Froese, Pauly (2021Froese R, Pauly D. FishBase [Internet]; 2021. Available from: https://www.fishbase.org
https://www.fishbase.org...
) and Robertson, Allen (2015Robertson DR, Allen GR. Shorefishes of the Tropical Eastern Pacific online information system [Internet]. Balboa; 2015. Available from: http://www.stri.org/sftep
http://www.stri.org/sftep...
).

Data analyses. Rank abundance plots (RADs) for each individual sampled locality were used to visualize species abundance distributions. Multivariate statistic techniques were employed to analyze data related to fish assemblage organization. A PERMANOVA test (permutational multivariate analysis of variance, Anderson, 2001Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001; 26(1):32-46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
https://doi.org/10.1111/j.1442-9993.2001...
) was used to evaluate differences in fish assemblages between localities and salinity zones (fixed factor with 3 levels: low, medium and high). To visualize multivariate patterns revealed by PERMANOVA, constrained (canonical analysis of principal coordinates, CAP) ordination techniques were used (Anderson, Willis, 2003Anderson MJ, Willis TJ. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology. 2003; 84(2):511-25. https://doi.org/10.1890/0012-9658(2003)084[0511:CAOPCA]2.0.CO;2). All multivariate analyses were based on Bray-Curtis distances calculated from square root transformed abundance data and conducted using the Vegan and BiodiversityR packages of the R statistical environment (Oksanen et al., 2017Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al. Vegan: Community ecology package. R package version 2.4-4; 2017. Available at: https://CRAN.R-project.org/package=vegan
https://CRAN.R-project.org/package=vegan...
).

RESULTS

A total number of 61 (+10) morphotypes and 10987 individuals were sampled at the seven localities examined (Tab. 1; Tab. S2 ). These corresponded to 30 fish families. Sixty three percent of the total abundance was composed by species within the Clupeidae (sardines) and Ariidae (sea catfishes). Lile stolifera (Jordan, Gilbert, 1882) (Pacific piquitinga) and Ariopsis simonsi (Starks, 1906) (Tete sea catfish) constituted 99% of this 63%. Other families that were also abundant were Centropomidae (9 %), Tetraodontidae (4 %), Sciaenidae (3 %), Gerreidae (3 %), Atherinopsidae (3 %), Haemulidae (2 %), Serranidae (2 %), Mugilidae (2 %), Engraulidae (2 %), and Lutjanidae (2 %). All these families accounted for 32% of the total abundance. However, the dominance of each family and species varied in each assemblage according to the locality (Fig. 2). For example, rank-abundance plots showed the sea catfish A. simonsi as the most dominant species in four of the seven localities. Centropomus armatus Gill, 1863 (Centropomidae) was present in all localities within the top five species. Similarly, L. stolifera was among the most abundant species in five of the seven localities, and Sphoeroides rosenblatti Bussing, 1996 (Tetraodontidae) was among the most abundant in four of the seven localities Despite the differences in sampling intensity, species richness at each locality was generally between 20 and 40 (Fig. 2). In terms of the trophic and spatial guilds that were represented in these intertidal mangrove fish communities, zoobenthivores and benthopelagic - demersal fish were clearly dominant in number of species and abundance (Tab. 1).

FIGURE 2
| Rank-abundance plots of the intertidal fish communities sampled at different localities in the southern Colombian Pacific between 2012 and 2017. Locality names in purple correspond to the Iscuande-Mulatos region and in green to the Tumaco-Cabo Manglares region.

TABLE 1
| Mangrove fish species captured in intertidal creeks at seven localities of the Colombian Pacific coast during the 2012-2017 period (The Tumaco - Cabo Manglares area includes the five southernmost sampled localities shown in Fig. 1). Spatial guilds (SG): pelagic (P), benthopelagic (BP), demersal (D), reef associated (RA) and freshwater (F) according to Froese, Pauly (2021Froese R, Pauly D. FishBase [Internet]; 2021. Available from: https://www.fishbase.org
https://www.fishbase.org...
); and trophic guilds (TG): zooplanktivore (ZP), detritivore (DV), herbivore-phytoplankton (HVP), piscivore (PV), zoobenthivore (ZB), omnivore (OV). Commercially important species for the artisanal fishery are marked with an asterisk.

The PERMANOVA test showed significant effects for the factor salinity and locality (Tab. 2). The multivariate representation (CAPs) showed clear separation of communities between some localities (Fig. 3A) and across salinity ranges (Fig. 3B). Specially samples from the Iscuandé locality were clearly differentiated from the rest of the samples. Samples from Trujillo, Curay, Bocagrande and Teheran tend to aggregate whereas samples from Mulatos and Chontal grouped together (Fig. 3A). Similarly, samples from low salinity areas (i.e., Iscuandé) were highly dissimilar from samples from medium and high salinity areas. The separation between medium and high salinities was less evident but observable along the CAP axis LD2 (Fig. 3B).

FIGURE 3
| (A) Canonical analysis of principal coordinates (CAP) of intertidal mangrove creek fish assemblages taken at different localities and (B) Canonical analysis of principal coordinates (CAP) of intertidal mangrove creek fish assemblages taken at different localities with different salinities of the southern Colombian Pacific coast, Panama Bight mangrove eco-region. Symbols represent individual block net catches.

TABLE 2
| Results of a PERMANOVA model testing the effects of salinity and locality on mangrove creek fish assemblages collected between 2012 and 2017 in the southern Colombian Pacific coast. Df = degrees of freedom; Sum of Sqs = sum of squares; Pseudo-F = F value by permutation. Boldface indicates statistical significance. P-values based on 999 permutations.

Overall fish mean size (TL) at all localities was 16.7 cm (SD ± 6.7). However, fish size in Iscuandé, the locality with the lowest salinities, tended to be lower (mean = 14.9 cm ± 5.0) than in the rest of localities where mean values were > 17.0 cm. Large fish sizes were observed in the Chontal locality probably due to the dominance of the needlefish Strongylura scapularis (Jordan, Gilbert 1882) in the samples there (Fig. 4).

FIGURE 4
| Size distribution of intertidal mangrove fishes captured in the southern Colombian Pacific coast (Panama Bight eco-region) at seven localities between 2012 and 2017.

DISCUSSION

Our results indicate a fairly similar species composition of fish assemblages in intertidal mangroves in the seven localities examined in the southern Colombian Pacific coast. The species composition is also very similar to that sampled in the same habitats 200 km north of this coast (Bahía Málaga, Castellanos-Galindo, Krumme, 2013bCastellanos-Galindo GA, Krumme U. Tidal, diel and seasonal effects on intertidal mangrove fish in a high-rainfall area of the Tropical Eastern Pacific. Mar Ecol Prog Ser . 2013b; 494:249-65. https://doi.org/10.3354/meps10512
https://doi.org/10.3354/meps10512...
). Likewise, similar fish species composition, with dominance of snooks, marine mojarras (Gerreidae) and croakers (Sciaenidae), has been found in intertidal mangroves of the Gulf of Montijo, Panama (~500 km north) (Castellanos-Galindo et al., unpublished data). This indicates that a specific relatively uniform subset of coastal estuarine fishes (~70 species) is adapted to intertidal migrations throughout the macrotidal Panama Bight eco-region. In northern Brazil (Western Atlantic) and in a similar mangrove-dominated coast (650 km) with a macrotidal regime, Giarrizzo, Krumme (2008Giarrizzo T, Krumme U. Heterogeneity in intertidal fish fauna assemblages along the world’s longest mangrove area in northern Brazil. J Fish Biol. 2008; 72(3):773-79. https://doi.org/10.1111/j.1095-8649.2007.01728.x
https://doi.org/10.1111/j.1095-8649.2007...
), compared studies that used a similar methodology as in the present study and documented a total of 115 fish species inhabiting intertidal mangroves. The similarity in family composition between these two regions is striking, being families like Tetraodontidae and Ariidae common and dominant among the intertidal migrant species in both regions.

Fishes in tropical and subtropical coasts use mosaics of habitats including mangroves (Nagelkerken et al., 2015Nagelkerken I, Sheaves M, Baker R, Connolly RM. The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish Fish . 2015; 16(2):362-71. https://doi.org/10.1111/faf.12057
https://doi.org/10.1111/faf.12057...
). These mosaics can include seagrasses and coral reefs in areas of the Caribbean Sea and the Indo-Pacific region, but they include in most of the major mangrove areas of the world, mudflats or other kind of soft-bottom habitats in estuarine and deltaic settings (Twilley et al., 2018Twilley RR, Rovai AS, Riul P. Coastal morphology explains global blue carbon distributions. Front Ecol Environ. 2018; 16(9):503-08. https://doi.org/10.1002/fee.1937
https://doi.org/10.1002/fee.1937...
) This is the case for most of Panama Bight ecoregion. Of the ~230 fish species that inhabit mangroves and associated mosaic of habitats in this region (see review in Castellanos-Galindo et al., 2013Castellanos-Galindo GA, Krumme U, Rubio EA, Saint-Paul U. Spatial variability of mangrove fish assemblage composition in the tropical eastern Pacific Ocean. Rev Fish Biol Fish. 2013; 23:69-86. https://doi.org/10.1007/s11160-012-9276-4
https://doi.org/10.1007/s11160-012-9276-...
) almost one third undertakes intertidal migrations inside mangroves (Fig. 5). The remaining two thirds of these species rarely enter the intertidal mangrove area and stays in subtidal habitats such as creeks and submerged sand or mud-flats. This habitat partition by fishes does not necessarily implies that those fishes not entering mangroves do not benefit from the energy and food produced in this ecosystem. Instead, these fishes could benefit via trophic transfers from the presence of mangroves (see Fig. 5). A deeper understanding of these trophic links needs to be gained examining other habitats within the mangrove habitat mosaic that were not sampled with our methods.

FIGURE 5
| Different ways how coastal fishes may depend on mangrove areas in the Panama Bight ecoregion (adapted from Sheaves, 2017Sheaves M. How many fish use mangroves? The 75% rule an ill-defined and poorly validated concept. Fish Fish . 2017; 18(4):778-89. https://doi.org/10.1111/faf.12213
https://doi.org/10.1111/faf.12213...
). Species numbers are taken from the compilation of mangrove intertidal samplings and from studies performed in mosaics of estuarine mangrove areas.

Comparing our results with the national fishery statistics (SEPEC, 2013Sistema del Servicio Estadístico Pesquero Colombiano (SEPEC). Boletín Estadístico. Magdalena: Autoridad Nacional de Acuicultura y Pesca (AUNAP), Universidad del Magdalena; 2013.), we found that more than half of the total species captured in intertidal mangrove creeks of the southern Colombian Pacific coast are of commercial importance to the artisanal fishery (see Tab. 1). Especially important are the snooks (Centropomidae) and catfishes (Ariidae) that are dominant in the catches of all seven localities examined here (see Fig. 3). In other localities like Bahía Málaga in the central Colombian Pacific coast, snappers are a significant component of the mangrove fish assemblage (in biomass and individual abundance; Castellanos-Galindo, Krumme, 2013bAburto-Oropeza O, Ezcurra E, Danemann G, Valdez V, Murray M, Sala E. Mangroves in the Gulf of California increase fishery yields. Proc Natl Acad Sci USA. 2008; 105(30):10456-59. https://doi.org/10.1073/pnas.0804601105
https://doi.org/10.1073/pnas.0804601105...
) and are an important part of the artisanal fishery. Other species that do not migrate to intertidal mangrove areas, but that live in close proximity to this habitat are also very important for the artisanal fishery in the central and southern Colombian Pacific coast. Among this group, species of Lobotidae (Lobotes pacificus Gilbert, 1898), Scombridae (Scomberomorus sierra Jordan & Starks, 1895), Ariidae (Bagre spp.), and Centropomidae (Centropomus spp.) contribute greatly to the overall fish landings (SEPEC, 2013Sistema del Servicio Estadístico Pesquero Colombiano (SEPEC). Boletín Estadístico. Magdalena: Autoridad Nacional de Acuicultura y Pesca (AUNAP), Universidad del Magdalena; 2013.; Herrón et al., 2019Herrón P, Castellanos-Galindo GA, Stäbler M, Díaz JM, Wolff M. Towards ecosystem-based assessment and management of small-scale and multi-ear fisheries: Insights from the Tropical Eastern Pacific. Front Mar Sci. 2019; 6(127):1-17. https://doi.org/10.3389/fmars.2019.00127
https://doi.org/10.3389/fmars.2019.00127...
) and likely derive some of their food through the trophic mangrove pathway (Fig. 5). Despite it is commonly recognized that this mangrove-dominated coast is crucial in providing habitat for many of the species targeted by the artisanal fishing fleets that operate there, a lack of quantitative knowledge on the relationship between mangrove characteristics and fisheries yields or productivity is lacking. Our results provide initial quantitative information on the fish community that directly use mangroves during tidal inundations.

Data gaps in knowledge of eastern Pacific mangrove fishes. For other ecosystems like coral reefs, small cryptic fishes have been increasingly recognized as significantly important for ecosystem functioning (Brandl et al., 2018Brandl SJ, Goatley CHR, Bellwood DR, Tornabene L. The hidden half: ecology and evolution of cryptobenthic fishes on coral reefs. Biol Rev. 2018; 93(4):1846-73. https://doi.org/10.1111/brv.12423
https://doi.org/10.1111/brv.12423...
, 2019Brandl SJ, Tornabene L, Goatley CH, Casey JM, Morais RA, Cote IM et al. Demographic dynamics of the smallest marine vertebrates fuel coral reef ecosystem functioning. Science. 2019; 364(6446):1189-92. https://doi.org/10.1126/science.aav3384
https://doi.org/10.1126/science.aav3384...
). In mangrove ecosystems the biomass and abundances of these fishes is normally underestimated due to the prevailing sampling methodologies used. This is clearly evident in our study, where only a few species of Gobiidae and Eleotridae were sampled with our sampling method. Apart from a few studies in mangroves in northern Brazil (Barletta et al., 2000Barletta M, Saint-Paul U, Barletta-Bergan A, Ekau W, Schories D. Spatial and temporal distribution of Myrophis punctatus (Ophichthidae) and associated fish fauna in a northern Brazilian intertidal mangrove forest. In: Liebezeit G, Dittmann S, Kröncke I, editors. Life at interfaces and under extreme conditions. Developments in Hydrobiology. Dordrecht: Springer; 2000. p.65-74.), there is an absence of cryptobenthic fish community studies in mangroves. Preliminary observations of these fauna in the mangroves of the central Colombian Pacific show that they can be abundant and relatively diverse (~20 species of mainly gobids and labrisomids; Castellanos-Galindo et al., 2020Castellanos-Galindo GA, Medina-Contreras D, Lazarus JF, Cantera JR. Peces criptobentónicos en el Parque Nacional Natural Uramba Bahía Málaga (Colombia) Pacífico Oriental Tropical. Bol Invest Mar Cost. 2020; 49 (SuplEsp):119-36. https://doi.org/10.25268/bimc.invemar.2020.49.SuplEsp.1090
https://doi.org/10.25268/bimc.invemar.20...
). They therefore may play an important ecological role transforming energy from within the mangrove systems and being prey for more mobile fishes that move between habitats in the coastal zone.

Some areas in the Panama Bight mangrove eco-region and the rest of the tropical eastern Pacific remain under-studied. These areas contain significant parts of mangrove forests that have been historically inaccessible or of difficult access. These areas include The Gulf of San Miguel in the Darien province of Panama, the Baudó region and the San Juan Delta in the central Colombian Pacific coast and the extensive mangrove area of Esmeraldas in northern Ecuador.

Our study provides for the first time, quantitative information on a portion (the one migrating with the tides to intertidal areas) of the fish community inhabiting the largest and more developed mangrove forest in the Colombian Pacific coast, southern part of the Panama Bight ecoregion. Our results show that this intertidal fish community represents ~1/3 of the whole fish fauna in the mangrove mosaic of this region. Juveniles of many commercially important species for the local fishery are found in these intertidal mangroves and clearly show the importance of this habitat for fishes. Our understanding of the larger role that mangroves play for the other components of the coastal fish fauna of the region continues to be limited and we have delineated here a few themes that could help to fill in those knowledge gaps.

ACKNOWLEDGMENTS

Several consultants from the Marine Programme of WWF Colombia have helped during fish sampling campaigns in the last years. Thanks are due to Natalia Uribe, Lina Prieto and Stella Gomez. The expertise and fishing experience of David Satizabal (Armonia) and Chalo in Iscuandé, Don Evelio in Mulatos, among others, is greatly appreciated. Research activities during these years have been possible by the funding from Rufford Foundation, the Conservation Leadership Program, WWF Colombia and the Alexander von Humboldt Foundation. We thank the constructive comments made by three reviewers that helped us improve a first version of this manuscript.

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ADDITIONAL NOTES

  • HOW TO CITE THIS ARTICLE

    Castellanos-Galindo GA, Baos RA, Zapata LA. Mangrove-associated fish assemblages off the southern Panama Bight region (tropical eastern Pacific). Neotrop Ichthyol. 2021; 19(4):e210025. https://doi.org/10.1590/1982-0224-2021-0025

Edited by

Gerson Araújo

Data availability

Data citations

Froese R, Pauly D. FishBase [Internet]; 2021. Available from: https://www.fishbase.org

Publication Dates

  • Publication in this collection
    30 Nov 2021
  • Date of issue
    2021

History

  • Received
    20 Jan 2021
  • Accepted
    10 Sept 2021
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