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 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 , Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida

Abstract Monthly sampling across the Straits of Florida (SOF) allowed for a thorough investigation of the feeding ecologies of four taxa of larval tunas (family , tribe Thunnini) and the horizontal and vertical distributions of larvae and their dominant prey. Before piscivory, spp. larvae had a mixed diet of crustaceans and appendicularians, whereas (Katsuwonus pelamis), (Euthynnus alletteratus), and 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 and habitats despite the potentially long distances between such crustacean (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 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 current speeds vary greatly, and the meandering core of the abundance and general temporal and spatial overlap of Florida Current (averaging , 2 ms21) is confined to the Feeding and distribution of tuna larvae 985 western half of the SOF with current speeds declining over canal, prey items were teased out with minutien pins, the Florida shelf break (ca. Sta. 1–4) and more gradually in identified, and enumerated. the eastern half of the SOF to 0–0.4 ms21. Plankton Environmental abundances of zooplankton taxa were was sampled at each station during daylight hours with the estimated from the 1-m2 MOCNESS samples. For general use of two adjoined multiple opening-closing net and temporal and spatial analyses across the SOF, zooplankton environmental sensing systems (MOCNESS; Wiebe et al. samples from the 0–25-m depth interval at even-numbered 1985) of different opening and mesh sizes (4 m2, 1-mm stations from four months (April, June, August, and mesh; 1 m2, 150-mm mesh; Guigand et al. 2005), which October) in 2003 were examined. To investigate vertical allowed for the concurrent collection of a broad size range distributions, samples from all four MOCNESS depth of larval fishes and the available zooplankton prey. intervals collected during three cruises (March, June, and Similarly, adjoined rectangular neuston nets (2 3 1 m, 1- October) at three stations spanning the transect (Stas. 2, 8, mm mesh; 0.5 3 1 m, 150-mm mesh) sampled the sea and 16) were examined. Samples were split with a Folsom surface to a depth of , 0.5 m. The MOCNESS obliquely splitter several times to obtain manageable aliquots from sampled the upper 100 m at all but the shallower western- which zooplankton taxa were identified to varying taxo- most station (to 50 m) with nominal discrete-depth nomic levels. Three aliquots were analyzed, and individuals intervals of 25 m (, 5 min interval21 at a horizontal speed for each taxon were enumerated for each aliquot unless at of , 1.5 m s21). Flow meters in each net system allowed for least 50 individuals were counted in previous aliquots. The calculations of the volume of water sampled. Plankton 150-mm mesh size of the nets precluded accurate abundance samples were fixed in 95% ethanol and later drained and estimates of nauplii. After examination, the three stored in 70% ethanol. Fluorescence data were collected at aliquots were stored separately from the original plankton each station with a conductivity-temperature-depth (CTD) sample, and these aliquots were later examined to obtain profiler at night either before (eastern half of transect) or relative proportions of the appendicularian genera Oiko- after (western half of transect) the daytime plankton pleura and Fritillaria by identifying 30 randomly selected sampling. individuals and applying this ratio to the initial abundance Gut evacuation rates were estimated with additional estimate of appendicularians. Because of a focus on sampling at nighttime (a nonfeeding period) that was appendicularians (the dominant prey of larval tunas), we conducted on two consecutive nights along the Florida report environmental abundances of copepodite-stage shelf break in June 2005 (Llopiz and Cowen 2008). (adult and juveniles together) only at the order MOCNESS tows of 15 min duration to a depth of 15 m level (Boxshall and Halsey 2004). For select samples in were performed at ca. 0.5, 1.5, 2.5, and 3.5 h postsunset. 2003 and 2004 in which prey removal by larval tunas was This sampling allowed for modeling the reduction in gut highest (none of which corresponded to those in the subset content with time. analyzed for general zooplankton distributions), appen- dicularians were similarly enumerated, except subsamples Laboratory procedures—Fish larvae were sorted from the were taken with a Hensen-Stempel pipette (typically 5 mL preserved samples of the 1-mm mesh nets, and larval tunas from 1 liter of plankton sample) until at least 100 were identified by pigment patterns that are retained after individuals were counted or three subsamples had been preservation (Richards 2005). Body lengths (BLs) for all analyzed. This subsampling method has error levels similar tuna larvae were measured as notochord length (preflexion) to using a Folsom splitter (7–9% coefficient of variation vs. or standard length (postflexion) with an ocular micrometer 5–18%, respectively [Postel et al. 2000]). (Leica MZ12). Oceanic tunas (Thunnus spp.) were grouped Although the -level identification of appendicular- at the genus level, although molecular techniques (Richard- ians excised from tuna guts was often not possible, those that son et al. 2007) indicated 95% of collected Thunnus larvae were identifiable were Oikopleura, and if not identifiable, were (Thunnus atlanticus; Richardson et al. in were usually distinctly large. For this reason, and because press). Within the genus Thunnus,noamong-species nearly all Fritillaria appendicularians were very small differences in diets were observed between molecularly relative to Oikopleura (mean dry weight of 0.2 vs. 1.0 mg, identified blackfin tuna and the far less abundant yellowfin respectively, on the basis of trunk-length to weight tuna (Thunnus albacares). Auxis spp. larvae were also conversions in Hopcroft et al. [1998]), we focused on the grouped together due to similarities in diet and distribu- distribution and availability of Oikopleura appendicularians. tions. Molecular analyses showed that (Auxis Even within Oikopleura there was a broad range of sizes, and thazard) and (Auxis rochei) were approximately this variability, along with the inability to measure the size of equally abundant in the SOF (Richardson et al. in press). consumed individuals (because of their soft bodies), has to Subsamples of tuna larvae from 2003 were inspected for be acknowledged as a potential source of error in the gut contents (n 5 788). For the more abundant and widely accuracy of daily rations and prey removal rates. Although it distributed Thunnus spp. and skipjack tuna, only larvae is likely that small Oikopleura are less important prey than from even-numbered months and stations were inspected. large individuals, the use of total Oikopleura abundances in Auxis spp. larvae from even months and all stations and analyses should provide conservative estimates of prey little tunny from all months and stations were inspected. availability and larval tuna consumption rates. Within each taxon, no more than five larvae were inspected from each combination of station, depth interval, and 2- Data analysis—For examining the horizontal distribu- mm BL size class. After excising the entire alimentary tions of larval tunas, taxon-specific abundances at each 986 Llopiz et al. station (individuals [ind.] m22 of sea surface to maximum %FO is emphasized because it can better illustrate depth sampled, calculated as the sum of the abundances in differences in prey choice and prey exclusion, especially each net, which themselves are the products of the number when prey sizes substantially differ, as observed here for of ind. m23 and the depth range sampled) were summed larval tunas. To obtain numerical percentages of prey types over both years and for all months of general co-occurrence and to establish evacuation rates, estimates were made of of the four tuna taxa (April to November in 2003 and April the number of appendicularians in the gut. Although to October in 2004 because of incomplete sampling of somewhat difficult to distinguish because of their soft stations in November) and expressed as a relative bodies, consumed appendicularians progressed from fully abundance (to the total of all four taxa). The abundances intact and undigested individuals in the stomach of larval of all fish larvae (i.e., the potential prey of piscivorous tuna tunas to increasingly digested but largely distinct appen- larvae) were calculated similarly and for the same periods, dicularian ‘‘packets’’ (enhanced by the different trunk, tail, but only for the upper 50 m to correspond with the and ‘‘house’’ regions) toward the posterior intestine (Llopiz predominant depths of tuna larvae. For other potential and Cowen 2009). zooplankton prey (appendicularians and copepods), which Evacuation rates were estimated for little tunny and were only analyzed for the 0–25-m depth interval, Auxis spp. larvae, which fed nearly exclusively upon abundances were expressed as ind. m23. appendicularians. Fifteen larvae of each taxon (4–8 mm Vertical distributions of tuna larvae were investigated BL) from each of the four postsunset sampling periods with the use of abundance (m22) proportions at depth were inspected (n 5 120). Appendicularians were enumer- calculated for each cruise for the entire larval population ated and expressed as a proportion of gut capacity (yielding across the SOF. Surface layer abundances (from neuston a measure of gut fullness) to standardize for the increase in nets; m22) were added to the 0–25-m MOCNESS net. gut capacity with larval length. Gut capacity at length was Abundances from each depth interval were standardized to established by the linear relationship of the maximum 25 m of depth because not every net sampled exactly 25 m number of appendicularians observed in specimens of 1- (93% were within 3 m of the target interval). Abundances in mm BL intervals from the monthly transect sampling (little each nominal 25-m depth interval over all stations sampled tunny: y 5 2.17BL 2 3.36, p 5 0.002, r2 5 0.92; Auxis spp.: in a cruise were summed and expressed as a proportion of y 5 1.69BL + 1.39, p 5 0.002, r2 5 0.93). Perhaps because the total in all depth intervals. Collections from several of the use of prey numbers (such that ingestion 5 egestion) cruises allowed for differences in taxon-specific proportions rather than remaining prey weight, the decline in gut at depth to be tested with ANOVA and Tukey’s honestly fullness was distinctly linear. As such, weighted least significant difference (HSD) test for pairwise comparisons. squares linear regression (Neter et al. 1996) on raw gut Proportions at depth were arcsine square-root transformed fullness data at time postsunset was used to establish linear (arcsin p1/2). Distribution centers were also calculated for evacuation models for each taxon following Bochdansky each cruise (Ro¨pke 1993), and similar results were and Deibel (2001). In these ‘‘redefined’’ linear models, the obtained. However, they are not reported because of the slope of the linear regression is divided by the initial gut largely confined nature of Thunnus spp. to the upper 25-m fullness (intercept) to obtain an evacuation rate constant depth interval and the resulting narrow error estimates. that can be used in daily ration models. The guts of all 30 Furthermore, distribution centers might not clearly convey larvae at 3.5 h postsunset were empty and thus not included the degree to which taxa actually overlap in their in the regression, and one extreme Auxis spp. outlier distributions. Vertical distribution analyses included the (possibly net or sample contamination) at 2.5 h postsunset months of general co-occurrence (April–November) in was excluded. Mean gut fullness values from the daytime- 2003 and excluded the shallower and thermally constrained collected monthly transect samples (little tunny: 0.50 6 (shoaling thermocline) westernmost station and, for little 0.26 SD; Auxis spp.: 0.47 6 0.22 SD) were used in tunny, three cruises from which #10 ind. were collected. conjunction with the evacuation rate constant to obtain For the vertical distributions of Oikopleura, differences in estimates of daily rations, following Eggers (1979), with the 23 relative abundances (m ) were tested via ANOVA on the equation nine station-month combinations for which all depth intervals were examined. Fluorescence (a proxy for Ct~tSalinz St{S0 chlorophyll concentrations; uncalibrated) distributions ðÞ with depth (1-m intervals) were examined for March, June, where Ct is the consumption (ration) during time t (hours and October (months of Oikopleura vertical distribution of daylight) in units of multiples of gut capacity, S is the data). For each station, fluorescence was converted to mean daytime level of stomach content (gut fullness), alin is values relative to the maximum observed in the upper 100 m the linear evacuation rate constant, St is the stomach to visualize the mean location of the deep chlorophyll content level at sunset (equal to S), and S0 is the level at maximum. sunrise (zero). The Eggers (1979) model was used because Feeding and diets were described with feeding incidence feeding was observed to be continuous and there were no (the proportion of larvae with prey present in the gut), the patterns of diel variability in gut fullness. However, very numerical percentage of prey types (%N), and the similar estimates were obtained with the model of Elliot frequency of occurrence of prey types (%FO; expressed and Persson (1978). The gut capacity with size relationship for each prey type as the percentage of larvae with the prey was then used to calculate size-specific daily rations in type present). Although both %N and %FO are reported, numbers of appendicularians. Because daily ration models Feeding and distribution of tuna larvae 987 combine single (i.e., mean) values of gut content and evacuation rate constants, estimates of daily rations are 892) 5 p generally presented in the literature without any associated FO n error. Here, variability (SE) in the estimates of daily rations % was calculated using Gaussian error propagation (Lo 2005) 162, 5 l

to incorporate the observed variability in daytime gut n fullness and the parameters (intercept and slope) of the gut spp. ( evacuation regression. N

Estimates of prey removal by larval tuna consumption % was estimated by daily ration at length relationships Auxis together with data on larval abundances and the individual lengths of all larvae collected (n 5 8897). This allowed for calculating a removal rate of appendicularians (m23 d21) 720) 5 p n

that was related to environmental Oikopleura abundances. FO

Daily rations at size for skipjack tuna were assumed to be % N) and the frequencies of occurrence of prey 133, the midpoints of the relationships for little tunny and Auxis % 5 l spp. because of our observation that development of little n , number of prey excised; BL, body length; crust., tunny is the most precocious of the three taxa and Auxis p n spp. the least. Prey removal rate estimates only included larvae at lengths before low reliance on piscivory (, 8 mm N % for skipjack tuna and little tunny and , 15 mm for Auxis spp.). The consumption by Thunnus spp. was not included in estimates because of their mixed diets of appendicular- spp. collected in the Straits of Florida. Feeding incidence is the ians and crustaceans. Although daily rations, and thus prey 740) Little tunny ( 5 p Auxis

removal rates, are potentially a function of prey abun- n dance, only the mean daily ration estimates were used to FO % calculate prey removal rates. 170, 5 l n ,numberoflarvaeinspected; Results l n

Feeding variability—Of the 788 tuna larvae subsampled N

for feeding analyses, more than 98% had prey present in the % gut (Table 1). Feeding incidences by taxa were 98% for Thunnus spp. and 99% for skipjack tuna, little tunny, and Auxis spp. Despite phylogenetic and morphological simi-

larities (Fig. 1B), the diets of Thunnus spp. were distinctly 2979) Skipjack tuna ( 5 different from the other three taxa of larval tunas (Table 1; p n FO % Fig. 2). Thunnus spp. diets were mixed throughout larval spp., skipjack tuna, little tunny, and

ontogeny, consisting of copepod nauplii and copepodites 323, 5 (calanoids and the cyclopoid genus Farranula), appendicu- l larians, Evadne spp. cladocerans, and larval fish. Similar to n Thunnus spp., all other taxa exhibited piscivory, although Thunnus spp. (

to varying degrees and beginning at different lengths. N

Before piscivory, however, skipjack tuna, little tunny, and % Auxis spp. larvae relied nearly exclusively on appendicular- ians (Fig. 2B–D). Consumption of appendicularians by Thunnus Thunnus spp. increased with larval length to a maximum when nearly 80% of the larvae 7–11 mm BL had appendicularians present (Fig. 2A).

Predator and prey distributions—The horizontal distri- butions of tuna larvae across the SOF showed the highest total abundances and the occurrence of all four taxa in the sp. 10.5 31.9 0.0 0.0 0.0 0.0 0.1 0.6 western region (Fig. 3A). In the central and eastern SOF, Summary feeding data for larvae of total tuna abundances were lower, and little tunny and sp. 2.9 13.9 0.0 0.0 0.0 0.0 0.0 0.0 Evadne Auxis spp. were nearly absent, with only skipjack tuna and Feeding incidence 0.98 0.99 0.99 0.99 Size range (mm BL) 2.4–10.6 3.2–10.6 3.2–14.5 3.3–9.8 FO), defined as the percentage of feeding larvae with the prey type present. % Thunnus spp. occurring. Illustrating their co-occurrence Prey type within each region, taxa were also present during the same Table 1. time periods (Fig. 3B,C). NaupliusCalanoidaFarranula 60.9 6.7 83.9 36.0 3.2 0.0 6.0 0.0 2.2 0.0 7.6 0.0 2.0 0.8 7.5 3.1 percentage of larvae containing attypes least ( one prey item, and the diet is described with both numerical percentages of prey types ( crustacean; rem., remains. AppendiculariaLarval fishOtherUnknown crust. rem.Unknown soft rem. 11.3 5.1 1.2 1.0 36.0 0.4 32.5 8.2 6.0 89.7 3.2 0.7 1.5 4.2 94.6 0.7 2.4 10.1 6.0 90.1 3.0 0.6 93.9 5.6 1.3 0.3 3.0 21.2 94.7 6.1 1.5 0.3 99.4 0.2 0.9 1.9 0.9 1.3 4.4 3.8 Cladocera, Copepoda 988 Llopiz et al.

Vertically in the water column, all taxa of tuna larvae were primarily limited to the upper 50 m (Fig. 4A). Thunnus spp. larvae were found at significantly shallower depths than the other three taxa. Relative abundances of Thunnus spp. in the 0–25-m interval were 92% and significantly higher than skipjack tuna, little tunny, and Auxis spp. (ANOVA, Tukey’s HSD, all p , 0.001). Correspondingly, within the intervals of 25–50 and 50– 75 m, Thunnus spp. larvae were significantly less abundant than the three other taxa, with the exception of little tunny in the 50–75-m interval (ANOVA, Tukey’s HSD, p 5 0.04– 0.001). Vertical separation was most pronounced between Thunnus spp. and skipjack tuna (Fig. 4A). The extent of this separation is likely masked by the large depth intervals because Thunnus spp. larvae were abundant in the upper 0.5 m of the water column, whereas no skipjack tuna larvae were collected at the sea surface. These vertical distribu- tions are presumed to be a reflection of differences in larval behavior, in that tuna eggs are buoyant and found at the sea surface (Richards 2005; Richardson et al. 2009). The greatest levels of available Oikopleura appendicular- ians were also found in the upper 50 m of the water column (Fig. 4B), coincident with the highest abundances of tuna larvae. Relative Oikopleura abundance was lowest in the 75–100-m interval and significantly lower than both the intervals 0–25 and 25–50 m (ANOVA, Tukey’s HSD, p 5 0.002 and 0.012). The vertical distribution of Oikopleura was opposite that of fluorescence with the minimum of Oikopleura abundance, observed in the 75–100-m interval, coinciding with the mean depth of the across the SOF (Fig. 4B). Horizontally, mean abundances of Oikopleura in the upper 25 m declined significantly from the west (where all four taxa of tuna larvae co-occurred) with distance from 2 the Florida shelf (Fig. 5A; linear regression, F1,6 5 7.83, r 5 0.57, p 5 0.03). The westernmost station examined (Sta. 2) had the highest mean Oikopleura abundance (102 ind. m23), and from there, means declined to a minimum of 36 ind. m23 in the eastern SOF (Sta. 12). Despite clear patterns in station means, Oikopleura abundances were highly variable both temporally among months and spatially within the same months (Fig. 5A; this variability and a limited number of cruises analyzed precluded detecting significant differences among the means). Abun- dances in June were generally low across the entire transect (mean of 30 ind. m23). In October, which also had the highest mean abundance (110 ind. m23), the maximum abundance of 323 ind. m23 occurred relatively near (, 20 km) the observed minimum of 35 ind. m23. Abundances of all fish larvae (the potential prey of piscivorous tuna larvae) differed across the SOF (Fig. 5B; ANOVA, F1,16 5 5.73, p , 0.001), with higher abundances occurring in the western SOF. The average abundance in the west (Stas. 1–5) was nearly twice that of the central and eastern SOF, with a 2.5-fold difference between the stations with the highest and lowest abundances (Stas. 1, 12). Fig. 2. Frequency of occurrence of prey types (percentage of larvae with prey type present) by length class for (A) Thunnus Prey selectivity and prey switching—Appendicularians spp., (B) skipjack tuna, (C) little tunny, and (D) Auxis spp. larvae. constituted a small percentage of the prey field available to larval tunas when considering the environmental abun- Feeding and distribution of tuna larvae 989

Fig. 3. Relative abundances of tuna larvae (A) spatially at each of the 17 stations (numbered west to east) sampled across the Straits of Florida during periods of co-occurrence in 2003 (April to November) and 2004 (April to October) and (B, C) monthly during these periods within the western Straits of Florida, where all taxa generally co-occur (Stas. 1–5) and in the central and eastern regions (Stas. 6– 17) where mostly only Thunnus spp. and skipjack tuna co-occur (total n 5 8156). Relative abundance is the percentage of the total catch standardized by sea surface area to a depth of 100 m. dances of copepodite-stage copepods (Fig. 6). Mean tions (to total prey). However, differences in prey type percentages of Oikopleura in the environment (by month percentages for skipjack tuna, little tunny, and Auxis spp. and region in the SOF) ranged from 4% to 15% of the total were not significant among larvae collected over a range of of appendicularians and copepods combined. Despite these environmental Oikopleura abundances (50 ind. m23 inter- low proportions, of the nonpiscivorous skipjack tuna, little vals, range of 14–323 ind. m23; Kruskal–Wallis, p 5 0.08– tunny, and Auxis spp. larvae, 89% exclusively had 0.85; not shown) or over a range of Oikopleura to total prey appendicularians present in the gut (n 5 446). Formal ratios (total prey 5 sum of Oikopleura and copepods, 4% prey selectivity analyses (Chesson 1978) for these taxa were intervals, range of 2–26%; Kruskal–Wallis, p 5 0.16–0.82; unnecessary because, from a subset of samples with not shown). To provide a more sensitive indication if prey environmental zooplankton data, larvae (n 5 78) consumed switching is occurring, we also examined the occurrence 333 appendicularians, no copepodite-stage copepods, and (presence–absence) of non-appendicularian prey in the guts only 7 copepod nauplii (not shown; ambient abundances of of larvae collected at variable environmental abundances nauplii were unavailable, which also prevented selectivity and proportions of Oikopleura.Influenceofambient analyses for Thunnus spp.). Within these samples, percent- Oikopleura abundance and proportions on the occurrence ages of all appendicularians in the environment relative to of at least one non-appendicularian prey was marginally the sum of copepodites and appendicularians ranged from significant only within skipjack tuna (logistic regression; vs. 8% to 20%, with a mean of 13%. abundances: x2 5 3.848, df 5 1, p 5 0.050; vs. proportions: To investigate the possibility for prey switching, the x2 5 3.880, df 5 1, p 5 0.049). Thus, larvae generally percentages within each larva of all prey in the gut that remained nearly exclusive consumers of appendicularians were appendicularians were examined over a range of both (Fig. 7), even at low Oikopleura abundances (e.g., 14–50 environmental Oikopleura abundances and relative propor- ind. m23) and levels of relative availability (2–8%). 990 Llopiz et al.

Fig. 4. Vertical distributions of larval tunas, appendicularians, and fluorescence. (A) Mean (+ SE, back-transformed from arcsine-transformed values) larval tuna relative abundances by taxa in 25-m depth intervals calculated from monthly values of the entire larval population across the Straits of Florida. (B) Mean (+ SE) relative environmental abundances of Oikopleura appendicularians at depth interval calculated from three stations (west, central, and east) in the SOF in March, June, and October. Also plotted is the mean relative fluorescence (proxy for chlorophyll) for the same months. Fluorescence was converted to values relative to the maximum at each station to standardize for cross-straits variability in magnitude. For panel A, differences between taxa combinations within each interval (because intertaxa differences were of interest) are indicated by unshared letters, whereas in panel B, they indicate differences in Oikopleura abundance among depth intervals (Tukey’s HSD; p , 0.05, ** p , 0.01, or *** p , 0.001).

Daily rations and prey removal—Gut evacuation of minimum Oikopleura abundance (Fig. 5A) of 31 ind. m23, appendicularian prey by little tunny and Auxis spp. took the observed maximum values of prey consumption could less than 3.5 h (Fig. 8A). Mean size-specific daily ration have hypothetically removed up to 15.9% d21 (Table 2). estimates for little tunny and Auxis spp. larvae (Fig. 8B) increased with size from 10–18 appendicularians d21 for Discussion larvae of 3 mm BL up to 50–57 appendicularians d21 for larvae of 10 mm BL. These estimates are for 14 h of feeding We have taken a large-scale approach by incorporating during the longest daylight lengths (June–July), which is data on the abundances and distributions of fish larvae and near the center of temporal overlap and peak spawning for zooplankton prey in conjunction with diet analyses and all four taxa of tuna larvae. Estimates for November (11 h estimates of prey removal to illustrate several unique of daylight) are 82% of 14-h values. characteristics of co-occurring larval tunas. Our results Observed monthly maximum estimates of potential prey are consistent with the hypothesis that both larval tunas removal rates by tuna larvae (Table 2) ranged from 0.4 to and adult tunas (via locations of spawning habitat) are 4.9 appendicularians m23 d21 during the months of highest adapted to larval resource availability, thereby maximizing larval tuna abundance (June–September). All maxima for survival during the larval stage. Oikopleura appendicular- these months occurred in the western SOF, with four of ians were the nearly exclusive prey of three taxa of larvae eight at the westernmost station. Environmental abun- before piscivory, with piscivory exhibited by all four taxa. dances of Oikopleura appendicularians where these maxima Both Oikopleura and total fish larvae were more abundant occurred were variable, ranging from 29 to 268 ind. m23, in the western SOF, which is where larval tuna abundances yielding percent removal estimates ranging from 0.3% to were also greatest and where all four taxa of tuna larvae co- 3.5% Oikopleura d21. If related to the average observed occurred. Although differential mortality of the four taxa Feeding and distribution of tuna larvae 991

Fig. 6. Environmental abundances (geometric mean) of appendicularians and copepod copepodites (juvenile and adult) from 4 months and two regions of the Straits of Florida in 2003 (west: Stas. 2, 4, and 6, where all taxa of larval tunas generally co- occurred; central (cen.) and east: Stas. 8–16 (even stations only), where mostly only skipjack tuna and Thunnus spp. co-occur).

that of Thunnus spp. and skipjack tuna, which is consistent with previous claims that adult little tunny and Auxis spp. prefer habitats nearer continental shelves (Uchida 1981; de Sylva et al. 1987). Therefore, the more restricted spawning distribution of little tunny and Auxis spp. also results in the larvae of these taxa being restricted to the region’s most optimal feeding environment. The higher prey availability in the western SOF should result in a reduced chance for starvation, cannibalism, competition (both inter- and intraspecific), and food-limited growth, and thus an increased chance for maximal growth and survival. In the central and eastern SOF, the vertical distributions and diets of the remaining Thunnus spp. and skipjack tuna Fig. 5. Environmental abundances of the dominant prey of further support an influence of prey availability on the larval tunas by station (numbered west to east) across the Straits ecologies of larval tunas. Thunnus spp. and skipjack tuna of Florida. (A) Oikopleura appendicularians by month (lines) in larvae exhibited significantly different vertical distributions 2003 with geometric means (bars; + SE, back-transformed). The and thus remained spatially separated despite overlapping abundance for Sta. 7 in June was included in the calculation of the horizontally across the SOF. Additionally, prepiscivorous Sta. 6 mean (Sta. 6 sample was unavailable). (B) Geometric mean Thunnus spp. larvae fed on multiple crustacean taxa and (+ SE, back-transformed) abundance of all fish larvae collected in increased their reliance on appendicularians with size. The 2003 and 2004 (n 5 90,246). more diverse diet of Thunnus spp. is a distinctly different, but presumably adaptive, strategy from that of the other could influence observed horizontal distributions, it is taxa. Intuitively, a more diverse diet would assure unlikely that little tunny and Auxis spp. larvae would starve successful feeding in environments with low prey availabil- or be predated upon at such higher rates than the other two ity or variability in available types of prey. Interestingly taxa to result in their consistent absence from the central however, skipjack tuna (in addition to little tunny and and eastern SOF. Additionally, the rapid velocities of the Auxis spp.) continued to selectively and nearly exclusively Florida Current should minimize the chance for much consume appendicularians with no significant evidence for cross-straits mixing. Thus, the co-occurrence of all four prey switching—either at low abundances of available taxa in the western SOF suggests that the adults likely appendicularians or at low relative proportions. Although occupy similar spawning habitat upstream off the Florida consumption of appendicularians by fish larvae has been Keys and on the shoreward side of the core of the Florida observed in higher latitudes, especially in pleuronectiform Current. More conclusive, however, is that little tunny and larvae (Last 1978; Gadomski and Boehlert 1984), our study Auxis spp. spawning does not extend across the SOF like and others (Young and Davis 1990; Sampey et al. 2007; 992 Llopiz et al.

Fig. 8. (A) Mean (6 SE) gut fullness, expressed as a Fig. 7. Proportions of inspected Auxis spp., little tunny, proportion of maximum capacity, of little tunny and Auxis spp. skipjack tuna, and Thunnus spp. larvae exclusively containing larvae collected during periodic postsunset sampling to estimate appendicularians at (A) environmental (available) Oikopleura gut evacuation rates. Total n 5 119, including 30 empty larvae at abundance intervals (50 ind. m23 each) and (B) intervals of 3.5 h postsunset excluded from the weighted least squares linear environmental proportions of Oikopleura (0.04 each) relative to regression. Means are offset for clarity. (B) Size-specific relation- the total of copepod copepodites and Oikopleura. The two lowest ship of daily consumption estimates, in numbers of appendicular- Oikopleura abundances in the 0–50 ind. m23 interval of panel A ians for little tunny and Auxis spp. larvae. Black lines represent are 14 and 19 ind. m23 (one skipjack larva each), with the rest model estimates with shaded areas the SE calculated from being . 25 ind. m23. Sample sizes for the top three taxa in each Gaussian error propagation of evacuation rate and daytime gut plot are indicated above each set of points in the order of both the fullness SE. Estimates are for 14 h of feeding (i.e., summer, also legend and the points (offset for clarity), with Thunnus spp. sample the approximate period of maximum larval abundance). sizes directly above data points. the west had occurred at the average minimum environ- Llopiz and Cowen 2009) suggest this behavior might be mental abundance of appendicularians (which was in the more common in lower latitudes. eastern SOF), percent removal rates would be substantially The dynamics of appendicularian removal by larval higher, including values for July and August 2004 that tunas also support a link between larval distributions and would have been near 16% d21 and 11% d21, respectively. prey availability. For each month during the period of peak Knowledge of appendicularian population growth is larval tuna abundance (June–September), the maximum necessary for placing removal rates into a context of what observed removal of Oikopleura appendicularians occurred is sustainable; however, work in this area is limited, in the western SOF (most often at the westernmost station), especially in warm, oligotrophic waters and on the a result of high total abundances of tuna larvae and the abundant Oikopleura longicauda. Some estimates of gener- occurrence of all four taxa. Percentages of appendicular- ation times for Oikopleura dioica are 3–5 d at temperatures ians removed at these stations had a range of 0.3–3.5% d21, of 20–22uC (Fenaux 1976; Troedsson et al. 2002) and a very averaged 1.5% d21, and were clearly dependent on the rapid 1–2 d in Jamaica at 29uC (Hopcroft and Roff 1995), highly variable abundances of both tuna larvae and which is a temperature similar to the observed surface appendicularians. If the observed maxima of removal in water average in the SOF during the summer. A report Feeding and distribution of tuna larvae 993

Table 2. Removal rates of appendicularians from predation by larval tunas. For each month during the period of peak larval abundance (June–September), the maximum observed prey removal rate by larval tunas (calculated from larval abundances and size- specific daily rations) was related to ambient appendicularian abundances to estimate a daily percentage of appendicularians removed. Maxima of prey removal rates were also related to the average monthly minimum abundance of appendicularians observed in 2003 (31 ind. m23), which always occurred in the eastern Straits of Florida (Fig. 5). This yielded estimates of hypothetical percentages of appendicularians consumed if the maxima of prey removal occurred in this region. All values are corrected for seasonal (photoperiod) differences in estimated daily consumption. Sta., station; abund., abundance; env., environmental.

Max. prey removal Env. append. abund. % consumed Potential % consumed of Cruise (append. m23 d21) Sta. (m23) (d21) mean append abund. minima (d21) Jun 2003 0.5 1 64 0.8 1.7 Jul 2003 0.5 1 38 1.4 1.7 Aug 2003 0.6 1 220 0.3 1.9 Sep 2003 0.4 6 62 0.4 1.1 Jun 2004 1.3 2 70 1.9 4.2 Jul 2004 4.9 3 142 3.5 15.9 Aug 2004 3.3 4 268 1.2 10.7 Sep 2004 0.7 1 29 2.4 2.2 related to the latter study (Hopcroft et al. 1998) also has systems, to underestimate appendicularian abundance estimates of daily specific growth rates of that were (Remsen et al. 2004). Our use of a small mesh size as high as 26 d21 for O. dioica (mean of 14.4 d21) and (150 mm) should reduce the chance of underestimates, 17 d21 for O. longicauda (mean of 7.5 d21). However, these however, especially for Oikopleura. measurements were made in relatively productive coastal Although an understanding of the average state of the waters that also had substantially higher abundances of prey environment is important, the variability of prey appendicularians (location means of 440 and 3607 ind. resources could also have implications. If a threshold level m23) than we observed in the SOF. Such rapid growth of of appendicularian abundance exists below which tuna appendicularians, which is notably greater than that of larvae feed suboptimally or can substantially deplete the crustacean zooplankton, would allow for high levels of resource, the frequency with which larvae experience such predation and, thus, the high reliance on appendicularians levels might influence total larval survival. If so, it is likely by abundant larval tunas. Without knowledge of the that the western SOF will exhibit constraining prey levels consumption rates of the many other appendicularian less frequently. In the context of a bet-hedging strategy of predators (Purcell et al. 2005), including several larval reef frequent spawning over a long season, the western SOF fish taxa in this region (Llopiz and Cowen 2009), the would be a better bet for experiencing larval prey levels proportional contribution by larval tunas to appendicular- above any potential prey threshold. However, resources are ian predation mortality is unknown. Yet it appears that available in the central and eastern SOF, and skipjack tuna larval tunas are unlikely to exert enough predation pressure and Thunnus spp. might occupy these niches to their own on appendicularians to result in a substantial depletion of benefit and to the exclusion of other taxa. Adult skipjack resources, and this is ensured by their horizontal distribu- tuna and Thunnus spp. populations also appear to tions across the SOF because the occurrence of high larval distribute their reproductive output more consistently abundances and all four taxa is where prey availability is compared with the potentially periodic high spawning greatest. output of little tunny (as observed in July and August There are limitations to our estimates of prey removal. 2004), which might only be supported by the higher prey However, we have used a direct approach that eliminates availability in the western SOF. Yet, even in the western several broad assumptions that are necessary when SOF, Oikopleura abundance was observed to vary consid- empirical data are not highly resolved or daily rations erably between months at the same location and between and concurrent distributions of prey and predator are nearby locations in the same month. This variability unavailable. The linear evacuation model used here for highlights the possibility for mismatches between larval tuna larvae yields daily ration estimates lower than those of fish predators and their zooplankton prey, though on most models (Bochdansky and Deibel 2001; Llopiz and distinctly smaller spatial and temporal scales than those Cowen 2008), and estimates of gut evacuation during a exhibited in higher latitudes, which are driven by the nonfeeding period (after sunset) could be slower than those seasonality of primary and secondary productivity peaks from periods of continuous feeding (Canino and Bailey (Cushing 1990). The possibility for such mismatches in 1995). Additionally, only the taxa that fed nearly exclu- lower latitudes has been largely unaddressed despite the sively on appendicularians were used in the analyses. long-standing hypothesis that frequent spawning over Therefore, our estimates of prey removal are conservative, broad temporal and spatial scales by many fish species in with the observed pattern and potential implications low latitudes is a bet-hedging strategy for an unpredictable remaining valid. Still, further investigation is merited environment (Johannes 1978). regarding the influence of predator and prey patchiness A common descriptor of larval fish feeding success is (Lough and Broughton 2007; Young et al. 2009) or the feeding incidence, or the proportion of larvae with food potential for nets, compared with plankton imaging present in the gut. In combination with the rapid digestion 994 Llopiz et al. observed in larval tunas, the daytime feeding incidence of Deibel and Lee 1992) and, thereby, exploit the microbial nearly 99% indicates that feeding is frequent for larval food web to fuel their extremely high population growth tunas in the SOF. These are the first data for larval tunas in rates. Larval tunas, in turn, obtain relatively large, energy- the western North Atlantic Ocean, but much lower daytime rich prey items (Purcell et al. 2005) that are generally feeding incidences have been reported elsewhere. In the abundant and reliably available in an otherwise oligotro- eastern Indian Ocean, 55% of Thunnus spp. and 42% of phic environment. Notably, despite these characteristics of skipjack tuna larvae contained food (Young and Davis appendicularians, skipjack tuna, little tunny, and Auxis 1990), and feeding incidences were ca. 60% for both black spp. do not consume a large proportion of available food skipjack (, a congener of little tunny) and that co-occurring taxa, including Thunnus spp., are feeding Auxis spp. in the Gulf of California (Sanchez-Velasco et al. on (Llopiz and Cowen 2009). As such, the exclusive 1999)—although in the Mediterranean Sea, feeding inci- consumption of appendicularians among several types of dences of A. rochei and Thunnus alalunga were 88% and available prey is an interesting behavior in what has been 98%, respectively (Catalan et al. 2007; Morote et al. 2008). assumed to be a food-limited environment, wherein Additionally, it has been inferred that larval tunas in the starvation is often implicated as a large source of mortality. eastern Pacific Ocean might experience high levels of Evolutionarily, however, specific trophic niches are consis- starvation mortality (Margulies 1993). Without knowledge tent with the occurrence of limited prey availability, but of spawning output or larval feeding success by tunas in further work on a much greater suite of co-occurring other Atlantic Ocean regions, the relative advantage predators and prey is needed to reconcile the paradoxical conferred by the SOF ecosystem to larval survival is results of feeding success, specific diets, and the potential unknown. However, the high abundances and successful for competitive exclusion. feeding of tuna larvae in the SOF indicate that this region is The characteristics of the spatial and trophic niches of likely to be an important spawning ground for these species. larval tunas are a function of the behavior of the individual Spawning within oligotrophic oceanic waters by tunas, larvae, as well as the spawning of the adults. Clear often after long migrations, has been hypothesized to distinctions in diets and vertical distributions of larvae minimize predation on larvae with the potential trade-off of are evident, highlighting the potential influence of food experiencing poor larval feeding conditions (Bakun and acquisition on larval behavioral evolution. Moreover, adult Broad 2003). This theory is largely supported by evidence spawning habitat use yields a horizontal distribution of that many regions can often be nutritionally limiting larvae across the SOF that is consistent with patterns of (Young and Davis 1990; Margulies 1993; Sanchez-Velasco larval resource availability, presumably enhancing larval et al. 1999), even potentially yielding density-dependent survival. An alternative to this is that spawning occurs in feeding and growth (Jenkins et al. 1991). However, the SOF locations that are more related to the survival and feeding appear to provide a relatively favorable feeding environ- of the adults, but this might be less likely for highly mobile ment, possibly because of appendicularian abundances. and migratory tunas. Although the spatial and temporal This is supported not only by higher feeding incidences, but scales involved in such processes are extensive, there is clear also by higher reliance on appendicularians. For example, support that the evolved larval distributions and feeding two species of Thunnus in the eastern Indian Ocean did not behaviors optimize the feeding success and survival of consume appendicularians during any period of develop- larval tunas in the oceanic plankton. ment (Young and Davis 1990), nor did T. alalunga in the Mediterranean Sea (Catalan et al. 2007); A. rochei larvae in Acknowledgments the Mediterranean Sea had %FO for appendicularians of This project was made possible by the great efforts of Cedric only ca. 15% (Morote et al. 2008); and in the Gulf of Guigand, Amy Exum, Lisa Gundlach, Peter Lane, Elizabeth California, Auxis larvae consumed no appendicularians, Crompton, Kevin Leaman, Peter Vertes, Su Sponaugle, and many whereas E. lineatus did rely heavily on appendicularians but others that assisted on cruises, sorted samples, and provided other also had %FOs for copepod nauplii and copepodites of logistical and intellectual support. Special thanks to the captain and crew of the R/V F.G. Walton Smith. Manuscript drafts were 75% and 24%, respectively (Sanchez-Velasco et al. 1999). greatly improved by the suggestions of Martha Hauff, Su One example consistent with our results in the SOF was Sponaugle, Don DeAngelis, and two anonymous reviewers. that of skipjack tuna in the eastern Indian Ocean, which Funding was provided by grants from the National Science also almost exclusively consume appendicularians before Foundation (Ocean Sciences-0136132) and from the Gulf States piscivory (Young and Davis 1990). Marine Fisheries Commission (Billfish-2005-017). Additional For larval tunas, the energy demands of fast growth and support came from a gift from Arthur B. Choate to the University warm temperatures (25–30uC in the SOF) add to the of Miami’s Billfish Research Program, the Harding Michel challenge of feeding in an unproductive habitat. The Memorial Fellowship, the National Oceanographic and Atmo- reliance on appendicularians might be a nutritional spheric Administration’s Living Marine Resources Cooperative ‘‘loophole’’ (Bakun and Broad 2003) that helps larvae Science Center, the Capt. Bob Lewis Billfish Challenge Scholar- ship, and the Capt. Harry Vernon, Jr., Scholarship. overcome these constraints, similar to the benefit that piscivory provides at later stages (Govoni et al. 2003). Appendicularians are able to filter and ingest much smaller References particles than most zooplankton, allowing them to ALLDREDGE, A. L. 1981. The impact of appendicularian grazing on assimilate nano- and picoplankton that dominate low- natural food concentrations in situ. Limnol. Oceanogr. 26: latitude oceanic waters (King et al. 1980; Alldredge 1981; 247–257. Feeding and distribution of tuna larvae 995

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