Limnol. Oceanogr., 55(3), 2010, 983–996 E 2010, by the American Society of Limnology and Oceanography, Inc. doi:10.4319/lo.2010.55.3.0983 Distinctions in the diets and distributions of larval tunas and the important role of appendicularians Joel K. Llopiz,* David E. Richardson,1 Akihiro Shiroza,2 Sharon L. Smith, and Robert K. Cowen Division of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida Abstract Monthly plankton sampling across the Straits of Florida (SOF) allowed for a thorough investigation of the feeding ecologies of four taxa of larval tunas (family Scombridae, tribe Thunnini) and the horizontal and vertical distributions of tuna larvae and their dominant prey. Before piscivory, Thunnus spp. larvae had a mixed diet of crustaceans and appendicularians, whereas skipjack tuna (Katsuwonus pelamis), little tunny (Euthynnus alletteratus), and Auxis spp. displayed highly selective and nearly exclusive feeding on appendicularians. The availability of both appendicularians and larval fish prey declined from west to east across the SOF, and appendicularians were notably patchy. In the western SOF where prey was more abundant, all taxa of tuna larvae co-occurred, indicating the sharing of resources by the larvae, in addition to the adults of these taxa using similar spawning habitat upstream in the Florida Current. In the central and eastern SOF, where prey was less abundant, only Thunnus spp. and skipjack tuna co-occurred, and these two taxa exhibited significantly different vertical distributions. Prey removal rates (estimated from gut evacuation rates and daily rations) occurring in the western SOF where tuna taxa co-occurred are likely to be sustainable by appendicularian levels within this region but would potentially not be by levels in the east. The spatial and trophic characteristics of these four abundant larval taxa highlight the potential influence of feeding-related processes on larval and adult behavior, while also illustrating a critical trophic link to the microbial food web provided by appendicularians in this oligotrophic environment. Introduction to extremely high mortality rates of the planktotrophic, altricial larvae that must survive in potentially food-limited The planktonic organisms of the open ocean occupy waters. Although larval and adult fishes have remarkably some of the largest and, yet, most poorly understood different ecological roles, selective forces governing the ecosystems. Additionally, we know less about plankton survival of larvae operate during both the larval and adult dynamics in the tropical oceans than in higher latitudes. In stages. For example, many larvae possess specific feeding, the low-latitude open ocean, characteristics of planktonic swimming, and vertical distribution behaviors (Cowen organisms such as species distributions and trophic 2002; Leis and Carson-Ewart 2003; Llopiz and Cowen interactions are often observed, but sampling limitations 2009) that presumably enhance survival, whereas the often preclude placing such results into a broader spawning behavior of adults, including specific spawning ecosystem context. Thus, the potential influence of any times and locations (Iles and Sinclair 1982), can place differences between high- and low-latitude pelagic environ- offspring in an environment optimal for survival. For fishes ments, including differences in diversity and productivity such as tunas, the swimming capabilities and highly patterns, are difficult to understand. Although some large- migratory nature of the adults have been hypothesized to scale ecological patterns and processes have been revealed allow for the placement of offspring in favorable larval in the oceanic plankton, especially for phytoplankton and habitats despite the potentially long distances between such crustacean zooplankton (McGowan and Walker 1979; regions and those best suited for the feeding and growth of Murphy and Haugen 1985; San Martin et al. 2006), such adults during nonspawning periods (Bakun 1996; Block et work is notably limited for planktonic larval fishes, al. 2001). especially in lower latitudes. Our current understanding of larval fish ecologies in The planktonic larval stage of most marine teleost fishes lower latitudes, although relatively limited, suggests there is a characteristic of the reproductive strategy of releasing might be substantial differences between the tropics and thousands to millions of eggs into the planktonic environ- higher latitudes, especially regarding larval fish trophody- ment (Elgar 1990; Winemiller and Rose 1993), which leads namics (Sampey et al. 2007; Llopiz and Cowen 2009). Larvae of high-latitude fishes often exhibit broad diets that * Corresponding author: [email protected] appear to be regulated more by prey size than prey type, resulting in little resource partitioning (Economou 1991; Present addresses: Pepin and Penney 1997, but see Last 1978). This could be 1 Northeast Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, because of a lower diversity of both fish larvae and their Narragansett, Rhode Island prey or to an abundance of food (and associated reduction 2 Cooperative Institute for Marine and Atmospheric Studies, in competition) since spawning seasons in higher latitudes Rosenstiel School of Marine and Atmospheric Science, University are often temporally contracted to correspond to brief of Miami, Miami, Florida periods of high secondary productivity (Cushing 1990). In 983 984 Llopiz et al. Fig. 1. (A) Map of the Gulf of Mexico and Straits of Florida region, including the transect (black bar) of 17 stations that was sampled monthly in 2003 and 2004 between the Florida shelf break and the Great Bahama Bank. The dominant physical feature of this region is the rapid (, 2ms21) Florida Current, which is the upstream outflow either from the Gulf of Mexico or the Caribbean Sea directly via the Yucatan Channel. (B) The morphologically similar four taxa of ‘‘true’’ tunas (tribe Thunnini) that occur in the Straits of Florida. Body lengths are ca. 6 mm for all taxa except Auxis spp., which is ca. 5 mm. Drawings are from Collette et al. (1984); used with permission from the American Society of Ichthyologists and Herpetologists. contrast, most regions of the low-latitude open ocean are tuna larvae in the SOF, we address the following questions: characterized by low secondary productivity that exhibits (1) Is feeding by larval tunas selective, resulting in taxon- little and less predictable seasonal variability (Longhurst specific diets? (2) Do the horizontal and vertical distribu- and Pauly 1987). As such, most fishes in these regions tions of larval tunas correspond to the availability of their exhibit frequent spawning over protracted reproductive prey? (3) Could larval tuna consumption result in limited seasons, hypothesized to be a bet-hedging strategy for an prey availability? (4) Do tuna larvae have taxon-specific unpredictable environment (den Boer 1968; Johannes horizontal or vertical distributions, or both, that would 1978). Such an environment, coupled with a higher reduce the potential for inter- and intraspecific competition diversity of both fish larvae and planktonic prey, might or resource depletion? Answers to these questions will help result in highly selective larval feeding behaviors. Spatially, us better understand the potential influence of feeding and the vertical distributions of fish larvae and the spawning prey availability on the distributions and behavior of these locations of the adults (influencing the horizontal dis- co-occurring taxa. tributions of the larvae) could also contribute to a reduction in both inter- and intraspecific competition for Methods resources. Here, we integrate data on larval diets, prey availability, Field sampling—The SOF region (Fig. 1A) is a tropical prey removal, and vertical and horizontal distributions of to subtropical oceanic environment containing the rapidly four taxa of larval tunas in the Straits of Florida (SOF) flowing Florida Current that, to the north, becomes collected over large temporal and spatial scales. The four approximately one third of the total transport of the Gulf taxa of tuna larvae examined, oceanic tunas (Thunnus spp.), Stream (Leaman et al. 1989). Upstream of the Florida skipjack tuna (Katsuwonus pelamis), little tunny (Euthynnus Current is the Loop Current of the Gulf of Mexico or, alletteratus), and bullet and frigate tunas (Auxis spp.), periodically, when the Loop Current is pinched off, the represent all four genera of ‘‘true’’ tunas (family Scom- direct outflow of the Caribbean Sea via the Yucatan bridae, tribe Thunnini) that occur in the tropical and Channel. For the present study, a transect of 17 stations subtropical open ocean. Within the SOF, they composed (numbered west to east) across the SOF from the Florida 97% of the scombrid larvae and were second only to shelf break (south of Miami, Florida) to the Great Bahama lanternfishes (Myctophidae) in larval fish abundance. Bank (south of Bimini, Bahamas) was sampled monthly in These taxa occur together in the SOF from ca. April to 2003 and 2004 (Llopiz and Cowen 2008). The three eastern- November and are morphologically similar, having preco- and westernmost stations were , 2 km apart, and other cious development and the capability for piscivory during central stations were , 5.5 km apart. Within this region, the larval stage (Tanaka et al. 1996). Considering the high