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Fish Sound Production and Acoustic Telemetry Reveal Behaviors and Spatial Patterns Associated with Spawning Aggregations of Two Caribbean Groupers

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Fish Sound Production and Acoustic Telemetry Reveal Behaviors and Spatial Patterns Associated with Spawning Aggregations of Two Caribbean Groupers Vol. 518: 239–254, 2015 MARINE ECOLOGY PROGRESS SERIES Published January 7 doi: 10.3354/meps11060 Mar Ecol Prog Ser Fish sound production and acoustic telemetry reveal behaviors and spatial patterns associated with spawning aggregations of two Caribbean groupers Timothy J. Rowell1,3,*, Richard S. Nemeth2, Michelle T. Schärer3, Richard S. Appeldoorn3 1Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive, La Jolla, California 92093, USA 2Center for Marine and Environmental Studies, University of the Virgin Islands, 2 John Brewer’s Bay, St. Thomas, United States Virgin Islands 00802, USA 3Department of Marine Sciences and Caribbean Coral Reef Institute, University of Puerto Rico, Mayagüez, PO Box 9000, Mayagüez, Puerto Rico 00681-9013, USA ABSTRACT: Regional abundances of Nassau grouper Epinephelus striatus and yellowfin grouper Mycteroperca venenosa have declined due to overfishing of their spawning aggregations, prompting permanent and seasonal fisheries closures in the US Virgin Islands (USVI). As both species produce sounds associated with reproductive behaviors (courtship-associated sounds; CAS), passive acoustic and acoustic telemetry methods were used to determine temporal patterns of reproductive activity, site usage, and fish movements in order to assess the effectiveness of cur- rent management strategies at 2 marine protected areas (MPAs) in the USVI: the Grammanik Bank (GB) and Hind Bank Marine Conservation District (MCD). Patterns of sound production and ultrasonic acoustic tag detections showed that both species formed spawning aggregations from January through May at the GB, highlighting the current seasonal regulations (1 February to 30 April) as insufficient for protecting spawning stocks during the entire reproductive season. Acoustic tagging confirmed connectivity between the GB and MCD and exposed the broad extent of habitat used, including non-protected areas, during the spawning season. Spawning did not likely occur within the MCD, but the MPA did support abundances of calling individuals during spawning periods, indicating that both species produce CAS away from their spawning sites. This finding coupled with the detection of routine migrations between spawning and non-spawning sites presents a potential mechanism to lead conspecifics to the aggregation site and thereby increase reproductive fitness and spawning output. KEY WORDS: Nassau grouper · Epinephelus striatus · Yellowfin grouper · Mycteroperca venenosa · Passive acoustics · Ultrasonic acoustic tagging · Fish movement patterns · Marine protected area Resale or republication not permitted without written consent of the publisher INTRODUCTION occur when fish congregate at discrete sites over a short period of time and during specific seasonal A broad diversity of fishes, represented by 20 and lunar periods to release gametes, constituting tropical fish families and nearly 170 species, has an an nual event that often represents their sole been reported to spawn in aggregations (Sadovy de opportunity for reproduction and contribution to Mitcheson & Colin 2012). Spawning aggregations recruitment (Domeier & Colin 1997). Highly pre- *Corresponding author: [email protected] © Inter-Research 2015 · www.int-res.com 240 Mar Ecol Prog Ser 518: 239–254, 2015 dictable in space and time, spawning aggregations review of 17 MPAs implemented to protect FSA sites, are vulnerable to overfishing (Sadovy & Domeier Grüss et al. (2014) reported that only 43% had posi- 2005), which disrupts synchronized spawning, tive conservation effects on target species. One of decreases mean length, repro ductive output, and the major impediments to designing effective MPAs spawning stock biomass and may lead to extirpation for FSA protection is a lack of understanding of the and possible regional species extinction (Beets & complex patterns of behavior and movement asso - Friedlander 1992, Sadovy & Figuerola 1992, Sadovy ciated with spawning aggregations. 1994, Aguilar-Perera & Aguilar-Dávila 1996, Cole- Recent application of ultrasonic telemetry and man et al. 1996, Matos-Caraballo 1997, Giménez- passive acoustics has greatly aided our understand- Hurtado et al. 2005, Aguilar-Perera 2006, Sadovy de ing of the behaviors associated with spawning ag - Mitcheson et al. 2012, Sadovy de Mitcheson & Eris- gregations, especially for groupers (Epinephelidae). man 2012). In many cases, reef fish aggregations Acoustic tagging studies, which utilize an array of have disappeared prior to our understanding a spe- acoustic receivers and fish tagged with acoustic trans- cies’ reproductive requirements. mitters, have been used to evaluate MPA design One of the best known examples of a species that (Chap man et al. 2005) and determine home range, has experienced local population collapse due to site fidelity, diel movements, and large and small- overfishing of aggregations is the Nassau grouper scale migration patterns (Heupel et al. 2010, Hitt et Epinephelus striatus (Sadovy 1997, Cornish & Eklund al. 2011). For groupers, acoustic tags have been used 2003, Sadovy & Domeier 2005, Aguilar-Perera 2006, to estimate the timing of aggregation formation, Sadovy de Mitcheson et al. 2012), which is currently spawning frequency, as well as arrival, departure, listed as Endangered by the International Union for and residency times (Zeller 1998, Semmens et al. the Conservation of Nature (IUCN; www.iucnredlist. 2007, Starr et al. 2007, Rhodes & Tupper 2008, Rhodes org), and proposed as threatened under the US En - et al. 2012). Ultrasonic telemetry has also revealed dangered Species Act. In recent decades, the major- accurate patterns of spawning seasonality, use of mi - ity of known Nassau grouper aggregations in the gratory corridors, and other complex behaviors that tropical western Atlantic have disappeared, and the may increase the vulnerability of groupers during the remaining have decreased significantly in number spawning season (Starr et al. 2007, Rhodes et al. of individuals (Sadovy & Eklund 1999, Sala et al. 2012). However, because individual tagged groupers 2001, Aguilar-Perera 2006, Sadovy de Mitcheson et do not participate in all spawning months and can al. 2008). The yellowfin grouper Mycteroperca vene - skip entire spawning seasons (Nemeth 2005), pat- nosa is another large aggregating species that often terns of grouper abundance at spawning aggregation utilizes the same aggregation sites as Nassau grouper sites and use of MPAs over the spawning season (Olsen & LaPlace 1979, Whaylen et al. 2004, Nemeth have not been fully documented. et al. 2006b, Heyman & Kjerfve 2008) and is currently The use of passive acoustics, which can record listed as Near Threatened by the IUCN due to heavy court ship-associated sounds (CAS) produced by some fishing pressure and habitat destruction, although grouper species at spawning aggregations, such as there is limited information on the status of the spe- Nassau and yellowfin groupers (Schärer et al. cies and aggregations throughout its range (Brule & 2012a,b), is a promising technology to monitor aggre- Garcia-Moliner 2004). gation dynamics and has certain advantages over Protection of spawning aggregations has typically ultrasonic telemetry. Passive acoustic methods gen- focused on seasonal or area closures, which target erate large datasets with minimal effort (Myrberg the most common spawning times and locations 1997, Luczkovich & Sprague 2002, Rountree et al. known to fishers. Many fish spawning aggregation 2006, Luczkovich et al. 2008a, Mann et al. 2008) that (FSA) sites are used by multiple species either can be used to locate spawning aggregation sites simultaneously or sequentially (Whaylen et al. 2004, (Luczkovich et al. 1999, 2008b, Walters et al. 2009, Nemeth et al. 2006b, Heyman & Kjerfve 2008). While Rowell et al. 2011) and monitor site usage, repro - some marine protected areas (MPAs) have produced ductive behavior, and aggregation presence and res- population recovery (Beets & Friedlander 1999, Ne - idency duration (Locascio & Mann 2008, Mann et al. meth 2005), others have been ineffective, resulting in 2009, 2010, Nelson et al. 2011, Schärer et al. 2012a,b, continued population decline for target species, pos- 2014). When calibrated, passive acoustics can also sibly due to inadequate design or lack of enforce- assess relative and absolute changes in spawning ment (Eklund et al. 2000, Nemeth et al. 2006a, 2007, stock abundance at high temporal resolution (Rowell Rhodes & Tupper 2008, Rhodes et al. 2014). In a et al. 2012, Marques et al. 2013). In groupers, sound Rowell et al.: Grouper sound production and acoustic telemetry 241 production levels and rates have been observed to re- and yellowfin grouper FSA site (Federal Register flect relative fish abundance, aggregation formation, 2005). This closure has resulted in initial recovery courtship behaviors, and spawning activity through of spawning stocks of both species (Nemeth et al. comparisons to underwater visual surveys and pas- 2006b, Kadison et al. 2010, 2011). The MCD was sive video recordings (Rowell et al. 2012, Schärer et declared a year-round no-take area in December al. 2012a,b, 2014). 1999 through a cooperative effort between the In this study, passive acoustic recordings were inte- Caribbean Fishery Management Council and local grated with results of ultrasonic acoustic tagging fishermen to protect deep coral reefs and improve of Nassau and yellowfin groupers to examine the fishery resources (Federal Register
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