Not to be cited without prior reference to the authors ICES CM 2009/T:14 The successful and selective feeding of larval fishes in the low-latitude open ocean: Is starvation an insignificant source of mortality? Joel K. Llopiz and Robert K. Cowen University of Miami, Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, Miami, FL 33149 USA, [email protected] Abstract Historical interest in understanding the larval stage of high-latitude fishes has provided extensive insight into feeding-related processes that can influence larval fish mortality. However, the feeding dynamics of larvae that occur in lower latitudes, especially those that primarily inhabit oceanic waters, is notably limited. From monthly sampling across the Straits of Florida (SOF) over two years, we acquired data on the feeding ecologies of 21 taxa of fish larvae in order to elucidate levels of feeding success, as well the degree to which this subset of the larval fish community relies upon specific zooplankton prey types. Larval taxa examined included billfishes, tunas, mackerels, and seven families of coral reef fishes. All but one taxon examined for gut contents (total n = 3138) had feeding incidences near 100%. Additionally, gut evacuation was rapid and occurred in ~3 hr, indicating successful and frequent prey consumption. These observations, in conjunction with the fact that larvae withstand a nightly non-feeding period (10- 14 hrs in low-latitudes), point to the possibility that fish larvae in these waters experience low or even negligible levels of starvation mortality, although additional efforts specifically addressing this possibility are needed. Furthermore, diets of larvae were taxon-specific and often extremely narrow, illustrating very selective feeding among a high diversity of available zooplankton prey. Two notable characteristics of the diets of these larvae were high reliance upon appendicularians by several taxa and the prevalence of piscivory, which appears to be exhibited by over 30 species of scombroid larvae that occur in the SOF. Introduction The larval stage of most marine fishes is characterized by a planktonic period during which there is high vulnerability to both starvation and predation. Despite the potential influence of these two processes on total survival to later stages (Houde 1987), our understanding of them is limited, and this is especially so in lower latitudes. The tropical/subtropical ocean is generally oligotrophic and unproductive with fluctuations in productivity that are low in magnitude and temporally inconsistent (Longhurst & Pauly 1987). These conditions, which could represent a nutritionally constraining environment for altricial larvae, differ from those of higher latitudes where there are distinct secondary productivity blooms with which fish spawning periods often coincide (Cushing 1990). Intuitively, low productivity in conjunction with warm temperatures are conditions that should favor high levels of mortality directly due to starvation. However, because of the paucity of data on the feeding success of low-latitude fish larvae, in addition to several other aspects related to their trophic ecologies, there has been little empirical evidence either supporting or refuting this hypothesis. Although there are a few studies on larval fish trophodynamics in lower latitudes, recent work in the Straits of Florida (Llopiz & Cowen 2008, 2009, Sponaugle et al. 2009, Llopiz et al. in review) has taken a large, ecosystem-scale approach in both time and space to better understand the trophic interactions of co-occurring larval fishes in the low-latitude oceanic plankton. This work has thus far examined the trophic ecologies of 21 taxa of larval fishes, highlighting several aspects and behaviors that seem paradoxical when considering the presumed nutritional constraints of this region (i.e. oligotrophic, oceanic, average near-surface temperatures of 28–30°C from late spring to early fall). This contribution brings together many of the interesting results of this work that seem to contradict the potential for high levels of starvation mortality, at least in the Straits of Florida. These results do not show that starvation is not a substantial source of mortality in these waters, but do suggest it is possible—and possibly less so relative to higher latitudes. Future work that directly addresses this possibility is therefore greatly needed. With the recent increased focus on larval fish trophodynamics, we also conducted a meta-analysis to investigate the possibility for any latitudinal differences in several characteristics related to the trophic ecologies of fish larvae. Methods Field sampling The Straits of Florida (SOF) region is a tropical/subtropical oceanic habitat between Florida and both Cuba and the Bahamas (Fig. 1). Within the SOF is the strongly flowing Florida Current that is fed either by the Loop Current of the Gulf of Mexico or, when the Loop Current is occasionally pinched off, directly by the waters exiting the Caribbean Sea through the Yucatan Channel. To the north, the Florida Current becomes a large portion of the Gulf Stream, contributing ca. one-third of the total transport off of Figure 1. Map of the Straits of Florida and upstream regions of the Gulf of Cape Hatteras (Leaman et al. 1989). Mexico and northern Caribbean Sea. In 2003 and 2004, a transect of 17 In 2003 and 2004, a transect stations between the Florida shelf break and Great Bahama Bank was sampled monthly for larval fishes, other zooplankton and several physical of 17 stations (numbered west to parameters. Upstream of the Straits of Florida, the Loop Current in the east) across the SOF between the Gulf of Mexico is most often the source for the Florida Current, but can Florida shelf break south of Miami pinch off resulting in Caribbean waters flowing directly into the Straits of Florida (indicated by gray arrows). and Great Bahama Bank (25.5°N; Fig. 1) was sampled monthly for larval fishes, zooplankton, and several other biological and physical parameters (Llopiz & Cowen 2008). We utilized a coupled, asymmetrical multiple opening closing net and environmental sampling system (MOCNESS; Wiebe et al. 1985, Guigand et al. 2005) consisting of 4 m2 (1 mm mesh) and 1 m2 (150 μm mesh) openings. Discrete-depth sampling occurred in 25 m intervals from a depth of 100 m (50 m at the shallower, westernmost station). A paired neuston net (2x1 m, 1-mm mesh and 0.5x1 m, 150-μm mesh) sampled the sea surface to a depth of ca. 0.5 m. All nets were equipped with flowmeters for calculations of volume filtered, and plankton sampling was conducted during daylight hours except during sampling to estimate gut evacuation rates. Plankton samples were fixed in 95% ethanol and later drained and refilled with 70% ethanol. Larval fishes were sorted from all neuston, all 4-m2 MOCNESS, and the 0 to 25 m 1-m2 MOCNESS samples, and were identified to varying levels of taxonomic resolution (at least family) following Richards (2005). To estimate evacuation rates of billfish and tuna larvae, sampling occurred during two consecutive evenings near the Florida shelf in June 2005, beginning at sunset with a neuston net tow and following with MOCNESS tows (one net, double oblique to 15 m, ~15 min in length) at the approximate times of 0.5, 1.5, 2.5 and 3.5 hours post-sunset. The observation of empty guts in the early morning and the decline of contents after sunset indicated that larval billfishes and tunas, similar to many other taxa, only feed during daylight. Laboratory procedures Larvae were sorted from plankton samples and larval body length (BL; notochord/standard length before/after flexion of the urostyle) and lower jaw length (LJL; mandible) were measured with the ocular micrometer of a stereomicroscope (Leica MZ15). Larvae were dissected with a microscalpel and minutien pins, and the contents of the entire alimentary canal were teased out and identified. At least 5 of the most anterior (least digested) prey items were measured for length (prosome length for copepod copepodite stages except of harpacticoids, carapace length for other relevant crustaceans, and the longest dimension in all other prey, including harpacticoid copepods but excluding the caudal rami). Appendicularians were not measured due to their soft bodies. Appendicularian enumeration became more difficult with the degree of digestion (posteriorly in the intestine), but was estimated by the distinctiveness of the trunk, tail and house regions of the organism and the repeatedly observed anterior to posterior gradient of digestion state. Reference to copepod orders follows Boxshall and Halsey (2004). If identified, only copepod genera are referenced, and no distinction was made between juvenile and adult copepodite stages. Environmental abundances of zooplankton taxa were estimated from the 1 m2 MOCNESS samples. For general temporal and spatial analyses across the SOF, zooplankton samples from the 0-25 m depth interval at even-numbered stations from four months (Apr, Jun, Aug and Oct) in 2003 were examined. Samples were split with a Folsum splitter several times to obtain manageable aliquots from which zooplankton taxa were identified to varying taxonomic levels. Three aliquots were analyzed and individuals for each taxon were enumerated for each aliquot unless at least 50 individuals were counted in previous aliquots. The 150-µm mesh size of the nets precluded accurate abundance estimates of copepod nauplii. To investigate the relationships of individual zooplankton taxa to total zooplankton, we used samples collected off the Florida Keys in 2007. Five pairs of nearshore-to-offshore transects were sampled and the 1 m-2 MOCNESS samples were used. To estimate the abundances of individual taxa, plankton subsamples were from taken with a Hensen-Stempel pipette (typically 5 mL from 1 L of plankton sample) for enumerating the common copepod prey of larval fishes. Subsampling occurred until at least 100 individuals were counted or three subsamples had been analyzed. The displacement volume of the entire plankton sample was used as a measure of total zooplankton.