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,

The planktonic organisms of the open ocean occupy
some of the largest and, yet, most poorly understood
ecosystems. Additionally, we know less about plankton
dynamics in the tropical oceans than in higher latitudes. In
the low-latitude open ocean, characteristics of planktonic
organisms such as species distributions and trophic
interactions are often observed, but sampling limitations
often preclude placing such results into a broader
ecosystem context. Thus, the potential influence of any
differences between high- and low-latitude pelagic environ-
ments, including differences in diversity and productivity
patterns, are difficult to understand. Although some large-
scale ecological patterns and processes have been revealed
in the oceanic plankton, especially for phytoplankton and
crustacean zooplankton (McGowan and Walker 1979;
Murphy and Haugen 1985; San Martin et al. 2006), such
work is notably limited for planktonic larval fishes,
especially in lower latitudes.
The planktonic larval stage of most marine teleost fishes
is a characteristic of the reproductive strategy of releasing
thousands to millions of eggs into the planktonic environ-
ment (Elgar 1990; Winemiller and Rose 1993), which leads
* Corresponding author: jllopiz@rsmas.miami.edu
Present addresses:
1 Northeast Fisheries Science Center, National Marine Fisheries
altricial larvae that must survive in potentially food-limited
waters. Although larval and adult fishes have remarkably
different ecological roles, selective forces governing the
survival of larvae operate during both the larval and adult
stages. For example, many larvae possess specific feeding,
swimming, and vertical distribution behaviors (Cowen
2002; Leis and Carson-Ewart 2003; Llopiz and Cowen
2009) that presumably enhance survival, whereas the
spawning behavior of adults, including specific spawning
times and locations (Iles and Sinclair 1982), can place
offspring in an environment optimal for survival. For fishes
such as tunas, the swimming capabilities and highly
migratory nature of the adults have been hypothesized to
allow for the placement of offspring in favorable larval
habitats despite the potentially long distances between such
regions and those best suited for the feeding and growth of
adults during nonspawning periods (Bakun 1996; Block et
al. 2001).
Our current understanding of larval fish ecologies in
lower latitudes, although relatively limited, suggests there
might be substantial differences between the tropics and
higher latitudes, especially regarding larval fish trophody-
namics (Sampey et al. 2007; Llopiz and Cowen 2009).
Larvae of high-latitude fishes often exhibit broad diets that
appear to be regulated more by prey size than prey type,
resulting in little resource partitioning (Economou 1991;
Pepin and Penney 1997, but see Last 1978). This could be

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 (, 2 m s21) 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
characterized by low secondary productivity that exhibits
little and less predictable seasonal variability (Longhurst
and Pauly 1987). As such, most fishes in these regions
exhibit frequent spawning over protracted reproductive
seasons, hypothesized to be a bet-hedging strategy for an
unpredictable environment (den Boer 1968; Johannes
1978). Such an environment, coupled with a higher
diversity of both fish larvae and planktonic prey, might
result in highly selective larval feeding behaviors. Spatially,
the vertical distributions of fish larvae and the spawning
locations of the adults (influencing the horizontal dis-
tributions of the larvae) could also contribute to a
reduction in both inter- and intraspecific competition for
resources.
Here, we integrate data on larval diets, prey availability,
prey removal, and vertical and horizontal distributions of
four taxa of larval tunas in the Straits of Florida (SOF)
collected over large temporal and spatial scales. The four
taxa of tuna larvae examined, oceanic tunas (Thunnus spp.),
skipjack tuna (Katsuwonus pelamis), little tunny (Euthynnus
alletteratus), and bullet and frigate tunas (Auxis spp.),
represent all four genera of ‘‘true’’ tunas (family Scom-
bridae, tribe Thunnini) that occur in the tropical and
subtropical open ocean. Within the SOF, they composed
97% of the scombrid larvae and were second only to
lanternfishes (Myctophidae) in larval fish abundance.
These taxa occur together in the SOF from ca. April to
November and are morphologically similar, having preco-
cious development and the capability for piscivory during
the larval stage (Tanaka et al. 1996). Considering the high
abundance and general temporal and spatial overlap of
tuna larvae in the SOF, we address the following questions:
(1) Is feeding by larval tunas selective, resulting in taxon-
specific diets? (2) Do the horizontal and vertical distribu-
tions of larval tunas correspond to the availability of their
prey? (3) Could larval tuna consumption result in limited
prey availability? (4) Do tuna larvae have taxon-specific
horizontal or vertical distributions, or both, that would
reduce the potential for inter- and intraspecific competition
or resource depletion? Answers to these questions will help
us better understand the potential influence of feeding and
prey availability on the distributions and behavior of these
co-occurring taxa.
Methods
Field sampling—The SOF region (Fig. 1A) is a tropical
to subtropical oceanic environment containing the rapidly
flowing Florida Current that, to the north, becomes
approximately one third of the total transport of the Gulf
Stream (Leaman et al. 1989). Upstream of the Florida
Current is the Loop Current of the Gulf of Mexico or,
periodically, when the Loop Current is pinched off, the
direct outflow of the Caribbean Sea via the Yucatan
Channel. For the present study, a transect of 17 stations
(numbered west to east) across the SOF from the Florida
shelf break (south of Miami, Florida) to the Great Bahama
Bank (south of Bimini, Bahamas) was sampled monthly in
2003 and 2004 (Llopiz and Cowen 2008). The three eastern-
and westernmost stations were , 2 km apart, and other
central stations were , 5.5 km apart. Within this region,
current speeds vary greatly, and the meandering core of the
Florida Current (averaging , 2 ms21) is confined to the
 Feeding and distribution of tuna larvae
western half of the SOF with current speeds declining over
the Florida shelf break (ca. Sta. 1–4) and more gradually in
the eastern half of the SOF to 0–0.4 ms21. Plankton
was sampled at each station during daylight hours with the
use of two adjoined multiple opening-closing net and
environmental sensing systems (MOCNESS; Wiebe et al.
1985) of different opening and mesh sizes (4 m2, 1-mm
mesh; 1 m2, 150-mm mesh; Guigand et al. 2005), which
allowed for the concurrent collection of a broad size range
of larval fishes and the available zooplankton prey.
Similarly, adjoined rectangular neuston nets (2 3 1 m, 1-
mm mesh; 0.5 3 1 m, 150-mm mesh) sampled the sea
surface to a depth of , 0.5 m. The MOCNESS obliquely
sampled the upper 100 m at all but the shallower western-
most station (to 50 m) with nominal discrete-depth
intervals of 25 m (, 5 min interval21 at a horizontal speed
of , 1.5 m s21). Flow meters in each net system allowed for
calculations of the volume of water sampled. Plankton
samples were fixed in 95% ethanol and later drained and
stored in 70% ethanol. Fluorescence data were collected at
each station with a conductivity-temperature-depth (CTD)
profiler at night either before (eastern half of transect) or
after (western half of transect) the daytime plankton
sampling.
Gut evacuation rates were estimated with additional
sampling at nighttime (a nonfeeding period) that was
conducted on two consecutive nights along the Florida
shelf break in June 2005 (Llopiz and Cowen 2008).
MOCNESS tows of 15 min duration to a depth of 15 m
were performed at ca. 0.5, 1.5, 2.5, and 3.5 h postsunset.
This sampling allowed for modeling the reduction in gut
content with time.
Laboratory procedures—Fish larvae were sorted from the
preserved samples of the 1-mm mesh nets, and larval tunas
were identified by pigment patterns that are retained after
preservation (Richards 2005). Body lengths (BLs) for all
tuna larvae were measured as notochord length (preflexion)
or standard length (postflexion) with an ocular micrometer
(Leica MZ12). Oceanic tunas (Thunnus spp.) were grouped
at the genus level, although molecular techniques (Richard-
son et al. 2007) indicated 95% of collected Thunnus larvae
were blackfin tuna (Thunnus atlanticus; Richardson et al. in
press). Within the genus Thunnus, no among-species
differences in diets were observed between molecularly
identified blackfin tuna and the far less abundant yellowfin
tuna (Thunnus albacares). Auxis spp. larvae were also
grouped together due to similarities in diet and distribu-
tions. Molecular analyses showed that frigate tuna (Auxis
thazard) and bullet tuna (Auxis rochei) were approximately
equally abundant in the SOF (Richardson et al. in press).
Subsamples of tuna larvae from 2003 were inspected for
gut contents (n 5 788). For the more abundant and widely
distributed Thunnus spp. and skipjack tuna, only larvae
from even-numbered months and stations were inspected.
Auxis spp. larvae from even months and all stations and
little tunny from all months and stations were inspected.
Within each taxon, no more than five larvae were inspected
from each combination of station, depth interval, and 2-
mm BL size class. After excising the entire alimentary
985
canal, prey items were teased out with minutien pins,
identified, and enumerated.
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 (April, June, August, and
October) in 2003 were examined. To investigate vertical
distributions, samples from all four MOCNESS depth
intervals collected during three cruises (March, June, and
October) at three stations spanning the transect (Stas. 2, 8,
and 16) were examined. Samples were split with a Folsom
splitter several times to obtain manageable aliquots from
which zooplankton taxa were identified to varying taxo-
nomic 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-mm mesh size of the nets precluded accurate abundance
estimates of copepod nauplii. After examination, the three
aliquots were stored separately from the original plankton
sample, and these aliquots were later examined to obtain
relative proportions of the appendicularian genera Oiko-
pleura and Fritillaria by identifying 30 randomly selected
individuals and applying this ratio to the initial abundance
estimate of appendicularians. Because of a focus on
appendicularians (the dominant prey of larval tunas), we
report environmental abundances of copepodite-stage
copepods (adult and juveniles together) only at the order
level (Boxshall and Halsey 2004). For select samples in
2003 and 2004 in which prey removal by larval tunas was
highest (none of which corresponded to those in the subset
analyzed for general zooplankton distributions), appen-
dicularians were similarly enumerated, except subsamples
were taken with a Hensen-Stempel pipette (typically 5 mL
from 1 liter of plankton sample) until at least 100
individuals were counted or three subsamples had been
analyzed. This subsampling method has error levels similar
to using a Folsom splitter (7–9% coefficient of variation vs.
5–18%, respectively [Postel et al. 2000]).
Although the genus-level identification of appendicular-
ians excised from tuna guts was often not possible, those that
were identifiable were Oikopleura, and if not identifiable,
were usually distinctly large. For this reason, and because
nearly all Fritillaria appendicularians were very small
relative to Oikopleura (mean dry weight of 0.2 vs. 1.0 mg,
respectively, on the basis of trunk-length to weight
conversions in Hopcroft et al. [1998]), we focused on the
distribution and availability of Oikopleura appendicularians.
Even within Oikopleura there was a broad range of sizes, and
this variability, along with the inability to measure the size of
consumed individuals (because of their soft bodies), has to
be acknowledged as a potential source of error in the
accuracy of daily rations and prey removal rates. Although it
is likely that small Oikopleura are less important prey than
large individuals, the use of total Oikopleura abundances in
analyses should provide conservative estimates of prey
availability and larval tuna consumption rates.
Data analysis—For examining the horizontal distribu-
tions of larval tunas, taxon-specific abundances at each
986 Llopiz et al.
station (individuals [ind.] m22 of sea surface to maximum
depth sampled, calculated as the sum of the abundances in
each net, which themselves are the products of the number
of ind. m23 and the depth range sampled) were summed
over both years and for all months of general co-occurrence
of the four tuna taxa (April to November in 2003 and April
to October in 2004 because of incomplete sampling of
stations in November) and expressed as a relative
abundance (to the total of all four taxa). The abundances
of all fish larvae (i.e., the potential prey of piscivorous tuna
larvae) were calculated similarly and for the same periods,
but only for the upper 50 m to correspond with the
predominant depths of tuna larvae. For other potential
zooplankton prey (appendicularians and copepods), which
were only analyzed for the 0–25-m depth interval,
abundances were expressed as ind. m23.
Vertical distributions of tuna larvae were investigated
with the use of abundance (m22) proportions at depth
calculated for each cruise for the entire larval population
across the SOF. Surface layer abundances (from neuston
nets; m22) were added to the 0–25-m MOCNESS net.
Abundances from each depth interval were standardized to
25 m of depth because not every net sampled exactly 25 m
(93% were within 3 m of the target interval). Abundances in
each nominal 25-m depth interval over all stations sampled
in a cruise were summed and expressed as a proportion of
the total in all depth intervals. Collections from several
cruises allowed for differences in taxon-specific proportions
at depth to be tested with ANOVA and Tukey’s honestly
significant difference (HSD) test for pairwise comparisons.
Proportions at depth were arcsine square-root transformed
(arcsin p1/2). Distribution centers were also calculated for
each cruise (Röpke 1993), and similar results were
obtained. However, they are not reported because of the
largely confined nature of Thunnus spp. to the upper 25-m
depth interval and the resulting narrow error estimates.
Furthermore, distribution centers might not clearly convey
the degree to which taxa actually overlap in their
distributions. Vertical distribution analyses included the
months of general co-occurrence (April–November) in
2003 and excluded the shallower and thermally constrained
(shoaling thermocline) westernmost station and, for little
tunny, three cruises from which #10 ind. were collected.
For the vertical distributions of Oikopleura, differences in
relative abundances (m23) were tested via ANOVA on the
nine station-month combinations for which all depth
intervals were examined. Fluorescence (a proxy for
chlorophyll concentrations; uncalibrated) distributions
with depth (1-m intervals) were examined for March, June,
and October (months of Oikopleura vertical distribution
data). For each station, fluorescence was converted to
values relative to the maximum observed in the upper 100 m
to visualize the mean location of the deep chlorophyll
maximum.
Feeding and diets were described with feeding incidence
(the proportion of larvae with prey present in the gut), the
numerical percentage of prey types (%N), and the
frequency of occurrence of prey types (%FO; expressed
for each prey type as the percentage of larvae with the prey
type present). Although both %N and %FO are reported,
%FO is emphasized because it can better illustrate
differences in prey choice and prey exclusion, especially
when prey sizes substantially differ, as observed here for
larval tunas. To obtain numerical percentages of prey types
and to establish evacuation rates, estimates were made of
the number of appendicularians in the gut. Although
somewhat difficult to distinguish because of their soft
bodies, consumed appendicularians progressed from fully
intact and undigested individuals in the stomach of larval
tunas to increasingly digested but largely distinct appen-
dicularian ‘‘packets’’ (enhanced by the different trunk, tail,
and ‘‘house’’ regions) toward the posterior intestine (Llopiz
and Cowen 2009).
Evacuation rates were estimated for little tunny and
Auxis spp. larvae, which fed nearly exclusively upon
appendicularians. Fifteen larvae of each taxon (4–8 mm
BL) from each of the four postsunset sampling periods
were inspected (n 5 120). Appendicularians were enumer-
ated and expressed as a proportion of gut capacity (yielding
a measure of gut fullness) to standardize for the increase in
gut capacity with larval length. Gut capacity at length was
established by the linear relationship of the maximum
number of appendicularians observed in specimens of 1-
mm BL intervals from the monthly transect sampling (little
tunny: y 5 2.17BL 2 3.36, p 5 0.002, r2 5 0.92; Auxis spp.:
y 5 1.69BL + 1.39, p 5 0.002, r2 5 0.93). Perhaps because
of the use of prey numbers (such that ingestion 5 egestion)
rather than remaining prey weight, the decline in gut
fullness was distinctly linear. As such, weighted least
squares linear regression (Neter et al. 1996) on raw gut
fullness data at time postsunset was used to establish linear
evacuation models for each taxon following Bochdansky
and Deibel (2001). In these ‘‘redefined’’ linear models, the
slope of the linear regression is divided by the initial gut
fullness (intercept) to obtain an evacuation rate constant
that can be used in daily ration models. The guts of all 30
larvae at 3.5 h postsunset were empty and thus not included
in the regression, and one extreme Auxis spp. outlier
(possibly net or sample contamination) at 2.5 h postsunset
was excluded. Mean gut fullness values from the daytime-
collected monthly transect samples (little tunny: 0.50 6
0.26 SD; Auxis spp.: 0.47 6 0.22 SD) were used in
conjunction with the evacuation rate constant to obtain
estimates of daily rations, following Eggers (1979), with the
equation
! alin zðSt {S0 Þ
Ct ~tS
where Ct is the consumption (ration) during time t (hours
of daylight) in units of multiples of gut capacity, S ! is the
mean daytime level of stomach content (gut fullness), alin is
the linear evacuation rate constant, St is the stomach
content level at sunset (equal to S! ), and S0 is the level at
sunrise (zero). The Eggers (1979) model was used because
feeding was observed to be continuous and there were no
patterns of diel variability in gut fullness. However, very
similar estimates were obtained with the model of Elliot
and Persson (1978). The gut capacity with size relationship
was then used to calculate size-specific daily rations in
numbers of appendicularians. Because daily ration models
 Feeding and distribution of tuna larvae 987
percentage of larvae containing at least one prey item, and the diet is described with both numerical percentages of prey types (%N) and the frequencies of occurrence of prey
types (%FO), defined as the percentage of feeding larvae with the prey type present. nl, number of larvae inspected; np, number of prey excised; BL, body length; crust.,
Table 1. Summary feeding data for larvae of Thunnus spp., skipjack tuna, little tunny, and Auxis spp. collected in the Straits of Florida. Feeding incidence is the

combine single (i.e., mean) values of gut content and

Thunnus spp. (nl5323, np52979) Skipjack tuna (nl5170, np5740) Little tunny (nl5133, np5720) Auxis spp. (nl5162, np5892)

evacuation rate constants, estimates of daily rations are

%FO

0.6

7.5
3.1
0.0

1.3
3.8
1.9
4.4
99.4

generally presented in the literature without any associated

error. Here, variability (SE) in the estimates of daily rations
3.3–9.8

was calculated using Gaussian error propagation (Lo 2005)

0.99

to incorporate the observed variability in daytime gut

fullness and the parameters (intercept and slope) of the gut
evacuation regression.
0.1

2.0
0.8
0.0
94.7
0.2
0.9
0.3
0.9
%N

Estimates of prey removal by larval tuna consumption

was estimated by daily ration at length relationships
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)
%FO

0.0

7.6
0.0
0.0
93.9
21.2
1.5
3.0
6.1
that was related to environmental Oikopleura abundances.
Daily rations at size for skipjack tuna were assumed to be
3.2–14.5

the midpoints of the relationships for little tunny and Auxis

0.99

spp. because of our observation that development of little

tunny is the most precocious of the three taxa and Auxis
spp. the least. Prey removal rate estimates only included
0.0

2.2
0.0
0.0
90.1
5.6
0.3
0.6
1.3
%N

larvae at lengths before low reliance on piscivory (, 8 mm

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-
ians and crustaceans. Although daily rations, and thus prey
removal rates, are potentially a function of prey abun-
%FO

0.0

6.0
0.0
0.0
94.6
10.1
3.0
2.4
6.0
dance, only the mean daily ration estimates were used to
calculate prey removal rates.
3.2–10.6
0.99
Results
Feeding variability—Of the 788 tuna larvae subsampled

0.0

3.2
0.0
0.0
89.7
4.2
0.7
0.7
1.5
%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

%FO
different from the other three taxa of larval tunas (Table 1;

31.9

83.9
36.0
13.9
36.0
6.0
3.2
32.5
8.2
Fig. 2). Thunnus spp. diets were mixed throughout larval

2.4–10.6
ontogeny, consisting of copepod nauplii and copepodites

0.98
(calanoids and the cyclopoid genus Farranula), appendicu-
larians, Evadne spp. cladocerans, and larval fish. Similar to
Thunnus spp., all other taxa exhibited piscivory, although
to varying degrees and beginning at different lengths.

10.5

60.9
6.7
2.9
11.3
1.0
0.4
5.1
1.2
%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 spp. increased with larval length to a maximum
when nearly 80% of the larvae 7–11 mm BL had
appendicularians present (Fig. 2A).

Size range (mm BL)

Feeding incidence
crustacean; rem., remains.
Predator and prey distributions—The horizontal distri-
butions of tuna larvae across the SOF showed the highest

Cladocera, Evadne sp.

Unknown crust. rem.

total abundances and the occurrence of all four taxa in the

Unknown soft rem.

western region (Fig. 3A). In the central and eastern SOF,

Prey type

Farranula sp.
Appendicularia
total tuna abundances were lower, and little tunny and

Calanoida
Auxis spp. were nearly absent, with only skipjack tuna and

Nauplius

Larval fish
Copepoda
Thunnus spp. occurring. Illustrating their co-occurrence
within each region, taxa were also present during the same

Other
time periods (Fig. 3B,C).
988
Fig. 2. Frequency of occurrence of prey types (percentage of
larvae with prey type present) by length class for (A) Thunnus
spp., (B) skipjack tuna, (C) little tunny, and (D) Auxis spp. larvae.
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 deep chlorophyll
maximum 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
the Florida shelf (Fig. 5A; linear regression, F1,6 5 7.83, r2
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).
Prey selectivity and prey switching—Appendicularians
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
percentages of Oikopleura in the environment (by month
and region in the SOF) ranged from 4% to 15% of the total
of appendicularians and copepods combined. Despite these
low proportions, of the nonpiscivorous skipjack tuna, little
tunny, and Auxis spp. larvae, 89% exclusively had
appendicularians present in the gut (n 5 446). Formal
prey selectivity analyses (Chesson 1978) for these taxa were
unnecessary because, from a subset of samples with
environmental zooplankton data, larvae (n 5 78) consumed
333 appendicularians, no copepodite-stage copepods, and
only 7 copepod nauplii (not shown; ambient abundances of
nauplii were unavailable, which also prevented selectivity
analyses for Thunnus spp.). Within these samples, percent-
ages of all appendicularians in the environment relative to
the sum of copepodites and appendicularians ranged from
8% to 20%, with a mean of 13%.
To investigate the possibility for prey switching, the
percentages within each larva of all prey in the gut that
were appendicularians were examined over a range of both
environmental Oikopleura abundances and relative propor-
tions (to total prey). However, differences in prey type
percentages for skipjack tuna, little tunny, and Auxis spp.
were not significant among larvae collected over a range of
environmental Oikopleura abundances (50 ind. m23 inter-
vals, range of 14–323 ind. m23; Kruskal–Wallis, p 5 0.08–
0.85; not shown) or over a range of Oikopleura to total prey
ratios (total prey 5 sum of Oikopleura and copepods, 4%
intervals, range of 2–26%; Kruskal–Wallis, p 5 0.16–0.82;
not shown). To provide a more sensitive indication if prey
switching is occurring, we also examined the occurrence
(presence–absence) of non-appendicularian prey in the guts
of larvae collected at variable environmental abundances
and proportions of Oikopleura. Influence of ambient
Oikopleura abundance and proportions on the occurrence
of at least one non-appendicularian prey was marginally
significant only within skipjack tuna (logistic regression; vs.
abundances: x2 5 3.848, df 5 1, p 5 0.050; vs. proportions:
x2 5 3.880, df 5 1, p 5 0.049). Thus, larvae generally
remained nearly exclusive consumers of appendicularians
(Fig. 7), even at low Oikopleura abundances (e.g., 14–50
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
appendicularian prey by little tunny and Auxis spp. took
less than 3.5 h (Fig. 8A). Mean size-specific daily ration
estimates for little tunny and Auxis spp. larvae (Fig. 8B)
increased with size from 10–18 appendicularians d21 for
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
during the longest daylight lengths (June–July), which is
near the center of temporal overlap and peak spawning for
all four taxa of tuna larvae. Estimates for November (11 h
of daylight) are 82% of 14-h values.
Observed monthly maximum estimates of potential prey
removal rates by tuna larvae (Table 2) ranged from 0.4 to
4.9 appendicularians m23 d21 during the months of highest
larval tuna abundance (June–September). All maxima for
these months occurred in the western SOF, with four of
eight at the westernmost station. Environmental abun-
dances of Oikopleura appendicularians where these maxima
occurred were variable, ranging from 29 to 268 ind. m23,
yielding percent removal estimates ranging from 0.3% to
3.5% Oikopleura d21. If related to the average observed
minimum Oikopleura abundance (Fig. 5A) of 31 ind. m23,
the observed maximum values of prey consumption could
have hypothetically removed up to 15.9% d21 (Table 2).
Discussion
We have taken a large-scale approach by incorporating
data on the abundances and distributions of fish larvae and
zooplankton prey in conjunction with diet analyses and
estimates of prey removal to illustrate several unique
characteristics of co-occurring larval tunas. Our results
are consistent with the hypothesis that both larval tunas
and adult tunas (via locations of spawning habitat) are
adapted to larval resource availability, thereby maximizing
survival during the larval stage. Oikopleura appendicular-
ians were the nearly exclusive prey of three taxa of larvae
before piscivory, with piscivory exhibited by all four taxa.
Both Oikopleura and total fish larvae were more abundant
in the western SOF, which is where larval tuna abundances
were also greatest and where all four taxa of tuna larvae co-
occurred. Although differential mortality of the four taxa
 Feeding and distribution of tuna larvae
Fig. 5. Environmental abundances of the dominant prey of
larval tunas by station (numbered west to east) across the Straits
of Florida. (A) Oikopleura appendicularians by month (lines) in
2003 with geometric means (bars; + SE, back-transformed). The
abundance for Sta. 7 in June was included in the calculation of the
Sta. 6 mean (Sta. 6 sample was unavailable). (B) Geometric mean
(+ SE, back-transformed) abundance of all fish larvae collected in
2003 and 2004 (n 5 90,246).
could influence observed horizontal distributions, it is
unlikely that little tunny and Auxis spp. larvae would starve
or be predated upon at such higher rates than the other two
taxa to result in their consistent absence from the central
and eastern SOF. Additionally, the rapid velocities of the
Florida Current should minimize the chance for much
cross-straits mixing. Thus, the co-occurrence of all four
taxa in the western SOF suggests that the adults likely
occupy similar spawning habitat upstream off the Florida
Keys and on the shoreward side of the core of the Florida
Current. More conclusive, however, is that little tunny and
Auxis spp. spawning does not extend across the SOF like
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
further support an influence of prey availability on the
ecologies of larval tunas. Thunnus spp. and skipjack tuna
larvae exhibited significantly different vertical distributions
and thus remained spatially separated despite overlapping
horizontally across the SOF. Additionally, prepiscivorous
Thunnus spp. larvae fed on multiple crustacean taxa and
increased their reliance on appendicularians with size. The
more diverse diet of Thunnus spp. is a distinctly different,
but presumably adaptive, strategy from that of the other
taxa. Intuitively, a more diverse diet would assure
successful feeding in environments with low prey availabil-
ity or variability in available types of prey. Interestingly
however, skipjack tuna (in addition to little tunny and
Auxis spp.) continued to selectively and nearly exclusively
consume appendicularians with no significant evidence for
prey switching—either at low abundances of available
appendicularians or at low relative proportions. Although
consumption of appendicularians by fish larvae has been
observed in higher latitudes, especially in pleuronectiform
larvae (Last 1978; Gadomski and Boehlert 1984), our study
and others (Young and Davis 1990; Sampey et al. 2007;
992 Llopiz et al.
Fig. 7. Proportions of inspected Auxis spp., little tunny,
skipjack tuna, and Thunnus spp. larvae exclusively containing
appendicularians at (A) environmental (available) Oikopleura
abundance intervals (50 ind. m23 each) and (B) intervals of
environmental proportions of Oikopleura (0.04 each) relative to
the total of copepod copepodites and Oikopleura. The two lowest
Oikopleura abundances in the 0–50 ind. m23 interval of panel A
are 14 and 19 ind. m23 (one skipjack larva each), with the rest
being . 25 ind. m23. Sample sizes for the top three taxa in each
plot are indicated above each set of points in the order of both the
legend and the points (offset for clarity), with Thunnus spp. sample
sizes directly above data points.
Llopiz and Cowen 2009) suggest this behavior might be
more common in lower latitudes.
The dynamics of appendicularian removal by larval
tunas also support a link between larval distributions and
prey availability. For each month during the period of peak
larval tuna abundance (June–September), the maximum
observed removal of Oikopleura appendicularians occurred
in the western SOF (most often at the westernmost station),
a result of high total abundances of tuna larvae and the
occurrence of all four taxa. Percentages of appendicular-
ians removed at these stations had a range of 0.3–3.5% d21,
averaged 1.5% d21, and were clearly dependent on the
highly variable abundances of both tuna larvae and
appendicularians. If the observed maxima of removal in
Fig. 8. (A) Mean (6 SE) gut fullness, expressed as a
proportion of maximum capacity, of little tunny and Auxis spp.
larvae collected during periodic postsunset sampling to estimate
gut evacuation rates. Total n 5 119, including 30 empty larvae at
3.5 h postsunset excluded from the weighted least squares linear
regression. Means are offset for clarity. (B) Size-specific relation-
ship of daily consumption estimates, in numbers of appendicular-
ians for little tunny and Auxis spp. larvae. Black lines represent
model estimates with shaded areas the SE calculated from
Gaussian error propagation of evacuation rate and daytime gut
fullness SE. Estimates are for 14 h of feeding (i.e., summer, also
the approximate period of maximum larval abundance).
the west had occurred at the average minimum environ-
mental abundance of appendicularians (which was in the
eastern SOF), percent removal rates would be substantially
higher, including values for July and August 2004 that
would have been near 16% d21 and 11% d21, respectively.
Knowledge of appendicularian population growth is
necessary for placing removal rates into a context of what
is sustainable; however, work in this area is limited,
especially in warm, oligotrophic waters and on the
abundant Oikopleura longicauda. Some estimates of gener-
ation times for Oikopleura dioica are 3–5 d at temperatures
of 20–22uC (Fenaux 1976; Troedsson et al. 2002) and a very
rapid 1–2 d in Jamaica at 29uC (Hopcroft and Roff 1995),
which is a temperature similar to the observed surface
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
estimates of daily specific growth rates of biomass that were
as high as 26 d21 for O. dioica (mean of 14.4 d21) and
17 d21 for O. longicauda (mean of 7.5 d21). However, these
measurements were made in relatively productive coastal
waters that also had substantially higher abundances of
appendicularians (location means of 440 and 3607 ind.
m23) than we observed in the SOF. Such rapid growth of
appendicularians, which is notably greater than that of
crustacean zooplankton, would allow for high levels of
predation and, thus, the high reliance on appendicularians
by abundant larval tunas. Without knowledge of the
consumption rates of the many other appendicularian
predators (Purcell et al. 2005), including several larval reef
fish taxa in this region (Llopiz and Cowen 2009), the
proportional contribution by larval tunas to appendicular-
ian predation mortality is unknown. Yet it appears that
larval tunas are unlikely to exert enough predation pressure
on appendicularians to result in a substantial depletion of
resources, and this is ensured by their horizontal distribu-
tions across the SOF because the occurrence of high larval
abundances and all four taxa is where prey availability is
greatest.
There are limitations to our estimates of prey removal.
However, we have used a direct approach that eliminates
several broad assumptions that are necessary when
empirical data are not highly resolved or daily rations
and concurrent distributions of prey and predator are
unavailable. The linear evacuation model used here for
tuna larvae yields daily ration estimates lower than those of
most models (Bochdansky and Deibel 2001; Llopiz and
Cowen 2008), and estimates of gut evacuation during a
nonfeeding period (after sunset) could be slower than those
from periods of continuous feeding (Canino and Bailey
1995). Additionally, only the taxa that fed nearly exclu-
sively on appendicularians were used in the analyses.
Therefore, our estimates of prey removal are conservative,
with the observed pattern and potential implications
remaining valid. Still, further investigation is merited
regarding the influence of predator and prey patchiness
(Lough and Broughton 2007; Young et al. 2009) or the
potential for nets, compared with plankton imaging
systems, to underestimate appendicularian abundance
(Remsen et al. 2004). Our use of a small mesh size
(150 mm) should reduce the chance of underestimates,
however, especially for Oikopleura.
Although an understanding of the average state of the
prey environment is important, the variability of prey
resources could also have implications. If a threshold level
of appendicularian abundance exists below which tuna
larvae feed suboptimally or can substantially deplete the
resource, the frequency with which larvae experience such
levels might influence total larval survival. If so, it is likely
that the western SOF will exhibit constraining prey levels
less frequently. In the context of a bet-hedging strategy of
frequent spawning over a long season, the western SOF
would be a better bet for experiencing larval prey levels
above any potential prey threshold. However, resources are
available in the central and eastern SOF, and skipjack tuna
and Thunnus spp. might occupy these niches to their own
benefit and to the exclusion of other taxa. Adult skipjack
tuna and Thunnus spp. populations also appear to
distribute their reproductive output more consistently
compared with the potentially periodic high spawning
output of little tunny (as observed in July and August
2004), which might only be supported by the higher prey
availability in the western SOF. Yet, even in the western
SOF, Oikopleura abundance was observed to vary consid-
erably between months at the same location and between
nearby locations in the same month. This variability
highlights the possibility for mismatches between larval
fish predators and their zooplankton prey, though on
distinctly smaller spatial and temporal scales than those
exhibited in higher latitudes, which are driven by the
seasonality of primary and secondary productivity peaks
(Cushing 1990). The possibility for such mismatches in
lower latitudes has been largely unaddressed despite the
long-standing hypothesis that frequent spawning over
broad temporal and spatial scales by many fish species in
low latitudes is a bet-hedging strategy for an unpredictable
environment (Johannes 1978).
A common descriptor of larval fish feeding success is
feeding incidence, or the proportion of larvae with food
present in the gut. In combination with the rapid digestion
994 Llopiz et al.
observed in larval tunas, the daytime feeding incidence of
nearly 99% indicates that feeding is frequent for larval
tunas in the SOF. These are the first data for larval tunas in
the western North Atlantic Ocean, but much lower daytime
feeding incidences have been reported elsewhere. In the
eastern Indian Ocean, 55% of Thunnus spp. and 42% of
skipjack tuna larvae contained food (Young and Davis
1990), and feeding incidences were ca. 60% for both black
skipjack (Euthynnus lineatus, a congener of little tunny) and
Auxis spp. in the Gulf of California (Sanchez-Velasco et al.
1999)—although in the Mediterranean Sea, feeding inci-
dences of A. rochei and Thunnus alalunga were 88% and
98%, respectively (Catalan et al. 2007; Morote et al. 2008).
Additionally, it has been inferred that larval tunas in the
eastern Pacific Ocean might experience high levels of
starvation mortality (Margulies 1993). Without knowledge
of spawning output or larval feeding success by tunas in
other Atlantic Ocean regions, the relative advantage
conferred by the SOF ecosystem to larval survival is
unknown. However, the high abundances and successful
feeding of tuna larvae in the SOF indicate that this region is
likely to be an important spawning ground for these species.
Spawning within oligotrophic oceanic waters by tunas,
often after long migrations, has been hypothesized to
minimize predation on larvae with the potential trade-off of
experiencing poor larval feeding conditions (Bakun and
Broad 2003). This theory is largely supported by evidence
that many regions can often be nutritionally limiting
(Young and Davis 1990; Margulies 1993; Sanchez-Velasco
et al. 1999), even potentially yielding density-dependent
feeding and growth (Jenkins et al. 1991). However, the SOF
appear to provide a relatively favorable feeding environ-
ment, possibly because of appendicularian abundances.
This is supported not only by higher feeding incidences, but
also by higher reliance on appendicularians. For example,
two species of Thunnus in the eastern Indian Ocean did not
consume appendicularians during any period of develop-
ment (Young and Davis 1990), nor did T. alalunga in the
Mediterranean Sea (Catalan et al. 2007); A. rochei larvae in
the Mediterranean Sea had %FO for appendicularians of
only ca. 15% (Morote et al. 2008); and in the Gulf of
California, Auxis larvae consumed no appendicularians,
whereas E. lineatus did rely heavily on appendicularians but
also had %FOs for copepod nauplii and copepodites of
75% and 24%, respectively (Sanchez-Velasco et al. 1999).
One example consistent with our results in the SOF was
that of skipjack tuna in the eastern Indian Ocean, which
also almost exclusively consume appendicularians before
piscivory (Young and Davis 1990).
For larval tunas, the energy demands of fast growth and
warm temperatures (25–30uC in the SOF) add to the
challenge of feeding in an unproductive habitat. The
reliance on appendicularians might be a nutritional
‘‘loophole’’ (Bakun and Broad 2003) that helps larvae
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
particles than most zooplankton, allowing them to
assimilate nano- and picoplankton that dominate low-
latitude oceanic waters (King et al. 1980; Alldredge 1981;
Deibel and Lee 1992) and, thereby, exploit the microbial
food web to fuel their extremely high population growth
rates. Larval tunas, in turn, obtain relatively large, energy-
rich prey items (Purcell et al. 2005) that are generally
abundant and reliably available in an otherwise oligotro-
phic environment. Notably, despite these characteristics of
appendicularians, skipjack tuna, little tunny, and Auxis
spp. do not consume a large proportion of available food
that co-occurring taxa, including Thunnus spp., are feeding
on (Llopiz and Cowen 2009). As such, the exclusive
consumption of appendicularians among several types of
available prey is an interesting behavior in what has been
assumed to be a food-limited environment, wherein
starvation is often implicated as a large source of mortality.
Evolutionarily, however, specific trophic niches are consis-
tent with the occurrence of limited prey availability, but
further work on a much greater suite of co-occurring
predators and prey is needed to reconcile the paradoxical
results of feeding success, specific diets, and the potential
for competitive exclusion.
The characteristics of the spatial and trophic niches of
larval tunas are a function of the behavior of the individual
larvae, as well as the spawning of the adults. Clear
distinctions in diets and vertical distributions of larvae
are evident, highlighting the potential influence of food
acquisition on larval behavioral evolution. Moreover, adult
spawning habitat use yields a horizontal distribution of
larvae across the SOF that is consistent with patterns of
larval resource availability, presumably enhancing larval
survival. An alternative to this is that spawning occurs in
locations that are more related to the survival and feeding
of the adults, but this might be less likely for highly mobile
and migratory tunas. Although the spatial and temporal
scales involved in such processes are extensive, there is clear
support that the evolved larval distributions and feeding
behaviors optimize the feeding success and survival of
larval tunas in the oceanic plankton.
Acknowledgments
This project was made possible by the great efforts of Cedric
Guigand, Amy Exum, Lisa Gundlach, Peter Lane, Elizabeth
Crompton, Kevin Leaman, Peter Vertes, Su Sponaugle, and many
others that assisted on cruises, sorted samples, and provided other
logistical and intellectual support. Special thanks to the captain
and crew of the R/V F.G. Walton Smith. Manuscript drafts were
greatly improved by the suggestions of Martha Hauff, Su
Sponaugle, Don DeAngelis, and two anonymous reviewers.
Funding was provided by grants from the National Science
Foundation (Ocean Sciences-0136132) and from the Gulf States
Marine Fisheries Commission (Billfish-2005-017). Additional
support came from a gift from Arthur B. Choate to the University
of Miami’s Billfish Research Program, the Harding Michel
Memorial Fellowship, the National Oceanographic and Atmo-
spheric Administration’s Living Marine Resources Cooperative
Science Center, the Capt. Bob Lewis Billfish Challenge Scholar-
ship, and the Capt. Harry Vernon, Jr., Scholarship.
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Associate editor: Michael R. Landry
Received: 27 June 2009
Accepted: 29 November 2009
Amended: 22 December 2009