Intertidal Migration of the Four-Eyed Fish Anableps Anableps in North Brazilian Mangrove Creeks

Vol. 509: 271–287, 2014 MARINE ECOLOGY PROGRESS SERIES Published August 27 doi: 10.3354/meps10863 Mar Ecol Prog Ser Intertidal migration of the four-eyed fish Anableps anableps in North Brazilian mangrove creeks Uwe Krumme1,2,*, Marianna Audfroid Calderón1, Andreas Echterhoff1 1Leibniz Center for Tropical Marine Ecology (ZMT), Fahrenheitstr. 6, 28359 Bremen, Germany 2Thünen Institute of Baltic Sea Fisheries (TI-OF), Alter Hafen Süd 2, 18069 Rostock, Germany ABSTRACT: The movement patterns of mangrove fish during tidal cycles are virtually unknown, yet needed to understand fish habitat use. The intertidal migration of the four-eyed fish Anableps anableps L. (Anablepidae, Cyprinodontiformes), a surface-swimming species, was observed along 2 large mangrove-lined creeks in North Brazil. The number, direction and size of the fish crossing fixed line transects were recorded at 5 min intervals using visual surveys during daylight at spring, mid- and neap tide cycles. Migration took place in a surge and was predictably structured and directly related to water level, current speed and direction, and recurred independent of creek and tide. The fish rode the early flood tide upstream towards the creek heads. After the ebb current peak, they returned in a surge along the same pathways. The intertidal distances travelled ranged from 0.7 to >2 km per tide. Fish density maxima occurred at early flood and late ebb tide, with more fish swimming alone during flood tide and largest group sizes during ebb tides. At neap high tides, fish aggregated in fewer accessible creek heads. When spring tides inundated wider creek areas and made additional creek heads available, maximum fish dispersal occurred. Small fish underwent migrations at shallower water depths than larger fish, thereby optimizing foraging and refuge time. Creek heads were prime feeding grounds, and intertidal creeks were the pathways connecting trophic flows of A. anableps, highlighting that in the management of mangrove ecosystems, complete drainage systems deserve protection. Striking similarities in tidal migrations of resident salt marsh species suggest that equal evolutionary pressures resulted in universal migratory strategies of estuarine resident taxa. KEY WORDS: Anableps anableps · Intertidal fish migration · Movement patterns · Mangrove creek · Microhabitat use · Visual census · Bragança · Pará Resale or republication not permitted without written consent of the publisher INTRODUCTION 1980, Ansell & Gibson 1990), mudflats (e.g. Raffaelli et al. 1990), salt marsh creeks (e.g. Kneib & Wagner Mangroves are widely considered important nurs- 1994, Bretsch & Allen 2006a,b, Kimball & Able ery sites for many nekton species. While it is clear 2007a,b) and rocky shores (e.g. Rangeley & Kramer that numerous species are regularly present in man- 1995, Castellanos-Galindo et al. 2010). However, pat- groves, often with great numbers of individuals, terns in intertidal fish movement vary between information is scarce on how exactly they use the coastal habitats, even within the same region mangrove microhabitats in time and space. Exten- (Castellanos-Galindo et al. 2010, Castellanos- sive knowledge is available on the movement pat- Galindo & Krumme 2013). For instance, fish move- terns of intertidal fish in other intertidal habitats, ments are restricted to flooded waterways in systems such as sandy beaches (e.g. Tyler 1971, Gibson 1973, with dendritic creek systems, whereas movements *Corresponding author: [email protected] © Inter-Research 2014 · www.int-res.com 272 Mar Ecol Prog Ser 509: 271–287, 2014 are wide-ranging on less structured open shorelines. These findings from intertidal mangroves have Complex creek systems, especially those with inter- mainly been inferred from blocking or enclosing tidal vegetation, provide more edge, vertical struc- areas of different mangrove zones or strata. This, ture and a variety of microhabitats for nekton than however, has rarely been completed at different open shorelines, which may be linked to specific times of the tide because netting techniques are adaptations in intertidal habitat use. unable to capture the spatio-temporal simultaneity Knowledge about intertidal microhabitat use is and complexity inherent in the intertidal migrations crucial to be able to understand ecological connec- of animals. Other approaches such as underwater tions, define meaningful sampling designs and pro- video, hydroacoustic observations or hydroacoustic vide robust interpretation of sampling data. Regard- imaging (e.g. DIDSON) have been successfully ing mangroves, understanding the role of different applied to study fish movements in mangroves and microhabitats for fish is of paramount importance for salt marsh habitats (Krumme & Saint-Paul 2003, Ellis conservation and zoning. For instance, aquaculture & Bell 2008, Frias-Torres & Luo 2009, Kimball & Able ponds often invade from the landward side, destroy- 2012), but only captured the temporal patterns at the ing the uppermost sections of the mangrove forests, specific sampling location and were unable to with largely unknown consequences for intertidal account for the larger-scale spatio-temporal simul- animals (Lee 1999). taneity involved in intertidal fish movements. More- Most mangrove forests of the world are subject to over, in tidally influenced mangrove environments, substantial tidal effects and constitute only tempo- these approaches usually have limited capabilities rary habitats for nektonic organisms, being accessi- due to a combination of adverse characteristics, such ble only during times of inundation. In these tidally as high turbidity, strong tidal currents, litter trans- influenced mangroves, fish have to move between port, complex creek and forest structure, and ex - low-water resting sites (LWRS) and high-water feed- treme shallowness. ing sites (HWFS) to avoid stranding, thereby connec - In the present study, we used human observers to ting subtidal and intertidal habitats (Sheaves 2005, visually record the movements of the four-eyed fish Krumme 2009). Anableps anableps (Anablepidae, Cyprinodontifor- Mangroves have often been treated as a uniform mes) moving at different tides in 2 large intertidal habitat unit, regardless of the structural hetero - mangrove creeks in North Brazil. The species always geneity inherent in the large intertidal forests and swims at the water surface except for brief sub - mangrove-lined creek networks that dominate mersions when heavily disturbed (Zahl et al. 1977) extensive tidal coastal areas. Yet, different man- and thus gives us a unique opportunity for complete grove microhabitats exist (e.g. Koch & Wolff 2002, visual observations capturing the spatio-temporal Kon et al. 2011) and likely have different functions simultaneity inherent in fish migrations through for fish and invertebrate species, which may result intertidal vegetated creek systems. A. anableps is a in heterogeneous animal distributions in inundated viviparous, estuarine resident species that uses man- mangroves. For instance, species and size groups of grove creeks throughout its life. Reproduction takes shrimps seemed to use specific microhabitats during place year-round; therefore, females require a con- high tide (Rönnbäck et al. 2002, Vance et al. 2002, stant food supply (Brenner & Krumme 2007, Oliveira Meager et al. 2003), moving considerable distances et al. 2011). The species is distributed from the Gulf into the mangrove (Vance et al. 1996). In the Philip- of Paria (East Venezuela, Trinidad) (Cervigón et al. pines, Rönnbäck et al. (1999) observed differences 1993, Wothke & Greven 1998) to the state of Parnaiba/ in microhabitat use of shrimps and fish, and found Piauí in northern Brazil (U. Krumme pers. obs.). highest fish abundance and biomass in the most Brenner & Krumme (2007) showed that A. anableps inland habitat of the mangrove. In a temperate Aus- in North Brazil rest in the subtidal zone in a linear tralian mangrove, distinct patterns of fish assem- distribution along the banks of sheltered channels blage zonation and strong edge effects were found during the low-water period (LWRS). Virtually all fish (Hindell & Jenkins 2005). Giarrizzo et al. (2010) disappeared into mangrove-lined intertidal creeks revealed a size-structured intertidal migration of early in the flooding tide and returned to the subtidal the banded puffer fish Colomesus psittacus and with the late ebb tide, but the course of the intertidal suggested that the structure was related to ontoge- migration, distribution and microhabitat use in the netic changes in feeding and to the vertical zonation inundated mangrove (HWFS) remained unknown. of hard-shelled prey items in the North Brazilian Stomach content analysis showed that the major food mangrove. sources of A. anableps were epiphytic macroalgae, Krumme et al.: Intertidal migration of Anableps anableps 273 Insecta and Grapsidae (Brenner & Krumme 2007), The tide is semidiurnal and asymmetric; flood tide while stable isotope analysis sugges ted that the lasts 4 h and ebb tide lasts approximately 8 h. Dur- green algae Enteromorpha is the main food source ing the last 4 h, the ebb tide in the subtidal Furo is as similated (Giarrizzo et al. 2011). Brenner & Krumme extremely weak with an almost negligible fall in the (2007) found consistently fuller stomachs in fish re - water level due to sand banks at the mouth of the turning from a creek near the edge of the mangrove Furo. The tidal range is 2 to 3 m at neap tides and 3 peninsula than from a creek

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