Low occurrence rates of ubiquitously present leptocephalus larvae in the stomach contents of predatory fish
Miller, M. J., Dubosc, J., Vourey, E., Tsukamoto, K., and Allain, V. Low occurrence rates of ubiquitously present leptocephalus
larvae in the stomach contents of predatory fish. - ICES Journal of Marine Science
Michael J. Miller 1 2
Jeff Dubosc 0
Elodie Vourey 0
Katsumi Tsukamoto 1
Valerie Allain 0
0 Oceanic Fisheries Programme, Secretariat of the Pacific Community , BP D5, 98848 Noumea Cedex, New Caledonia
1 Laboratory of Eel Science, Department of Marine Science and Resources, College of Bioresource Sciences, Nihon University , 1866 Kameino, Fujisawa-shi, Kanagawa 252-0880 , Japan
2 Atmosphere and Ocean Research Institute, The University of Tokyo , 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564 , Japan
Leptocephali, the larvae of eels, grow to large sizes and are widely distributed in tropical and subtropical oceans. Their role in oceanic food webs is poorly known because they are rarely reported as food items in fish stomach content studies. Data from 13 years of research on the trophic dynamics of Pacific Ocean predatory fish indicate that among 8746 fish of 76 species/taxa (33 families) that had been feeding, only 16 fish of 6 species had remains of 34 leptocephali in their stomachs. Only 0.013% of the 256 308 total prey items were leptocephalus larvae, and 0.03% of the total prey items were juvenile or adult eels (mostly snipe eels: Nemichthyidae). There were 10 fish of 2 species of lancetfish (Alepisaurus spp., n ¼ 152), 2 rainbow runners (Elagatis bipinnulata, n ¼ 222), and 2 yellowfin tuna (Thunnus albacares, n ¼ 3103) that had leptocephali in their stomach contents, but all except one T. albacares (contained 15 leptocephali) had each eaten ≤3 leptocephali. A swallower, Pseudoscopelus sp., and a frigate tuna, Auxis thazard, had eaten single leptocephali. Twenty-eight bigeye tuna, Thunnus obesus, had eaten 76 juvenile/adult nemichthyid or serrivomerid eels. A literature survey found that only 15 out of 75 examined publications listed leptocephali in the stomach contents of a total of 6 species out of 42 300 predatory fish of 40 species. The transparency of leptocephali and their apparent mimicry of gelatinous zooplankton could contribute to lower rates of predation. Their soft bodies likely digest rapidly, so although this study and existing literature indicate that leptocephali sometimes contribute to predatory fish diets, particularly for fish that do not exclude gelatinous prey types, and fish with low digestion rates in their stomachs such as lancetfish, their levels of contribution to fish diets and the impacts of predators on eel recruitment remain uncertain.
Alepisaurus; Anguilliformes; leptocephali; Pacific Ocean; predation; predator avoidance; stomach contents
Leptocephali are a ubiquitously present but poorly known type of
fish larvae that live in the surface layer of the world’s warm water
(Castle, 1984; Bo¨hlke, 1989a; Smith, 1989; Miller, 2009)
They are the larvae of eels of the Anguilliformes and the other
elopomorph orders of the Albuliformes (including the notacanths)
(Bo¨hlke, 1989b; Inoue et al., 2004; Miller and
. The most well-known eels are the freshwater
eels of the Anguillidae, which are important fisheries species in
some parts of the world
(Tesch, 2003; Tsukamoto and Kuroki,
. There are also several important commercially harvested
coastal marine eels, particularly of the genera Conger (Congridae)
and Muraenosox (Muraenesoscidae), and a wide range of more
than 800 species of marine eels are present in all types of tropical
to southern temperate habitats down to 4000 m
Miller and Tsukamoto, 2004)
. Interestingly, despite the anguillid
species living in freshwater and estuarine habitats for their juvenile
growth stage before spawning offshore in the ocean
et al., 2002; Tesch, 2003; Aoyama, 2009)
and marine eels inhabiting
coastal, continental slope, deep-benthic, and mesopelagic habitats,
the leptocephalus larvae of all eels, as well as those of the other
elopomorphs, inhabit the upper few hundred metres of the ocean
(Castonguay and McCleave, 1987; Miller, 2009)
Compared with other fish larvae that also live in the ocean surface
layer, leptocephali are unusual because of their extreme
transparency, large maximum sizes, unique morphology and physiology,
and drastic metamorphosis into completely different body forms
as they enter the juvenile stage
(Smith, 1989; Pfeiler, 1999; Miller,
. Surveys for leptocephali in various parts of the world show
that larvae of a variety of eel families are consistently present in
the surface layer of the ocean in tropical and subtropical areas and
can sometimes be quite abundant near the edges of continental
shelves or within offshore spawning areas
Kleckner, 1987; Tsukamoto, 1992; Miller and McCleave, 1994,
2007; Miller et al., 2002, 2006; Richardson and Cowen, 2004;
. The leptocephali of the European eel, Anguilla
anguilla, for example, become distributed all across the North
Atlantic after being spawned in the Sargasso Sea, as they are
transported to their recruitment areas in Europe and North Africa
(Schmidt, 1922; Miller et al., 2015)
. The characteristics of anguillid
larvae may have been an important component of the evolution and
speciation of freshwater eels
(Kuroki et al., 2014)
, yet their ecological
role and those of marine eel leptocephali within marine
communities are very poorly known.
Leptocephali live in the upper few hundred metres of the ocean
and some make diel vertical migrations within the upper 250 m, or
deeper near continental shelves
(Castonguay and McCleave, 1987;
Ross et al., 2007; Miller, 2009)
. Unlike most fish larvae, they
appear to feed exclusively on particulate organic material, such as
marine snow, giving them low trophic isotopic signatures
et al., 1993; Mochioka and Iwamizu, 1996; Miller et al., 2013a)
Some species grow to large sizes of 250 mm or larger, although
most taxa reach 60 – 120 mm
(Castle, 1984; Bo¨hlke, 1989a;
Miller et al., 2013b)
. They appear to be capable swimmers
(Wuenschel and Able, 2008) and many seem to avoid large plankton
nets during the day in clear oceanic waters, with the largest
leptocephali potentially avoiding nets even at night
(Miller et al., 2013b)
Importantly though in relation to predator – prey relationships,
they also appear to use a dynamic form of shape-change behaviour
of curling their bodies into fully or partially formed coil shapes,
which seems to make them resemble the silhouettes of gelatinous
(Miller et al., 2013c)
. This type of behaviour has
been also observed in other marine animals
may occur because only a limited number of fish seem to feed on
gelatinous zooplankton in warmer-water areas
(Purcell and Arai,
2001; Arai, 2005)
. Because of this, the shape-change behaviour of
leptocephali has been hypothesized to reduce predation by acting as a
form of Batesian Mimicry
(Miller et al., 2013b)
. This behaviour
might reduce predation by some types of predatory fish, and their
laterally compressed transparent bodies and forwards-or-backwards
swimming ability probably make leptocephali adapted to avoid
detection or actively avoid capture by predators (Miller, 2009).
Most food habits studies on predators such as tunas, billfish, and
other scombrids that live in the same habitats as eel larvae do not list
leptocephali among the types of fish that were found in stomach
(e.g. Bertrand et al., 2002; Potier et al., 2007; Young et al.,
2010; see Supplementary Table S1)
. The pelagic top-predators are
opportunistic feeders foraging in the epipelagic layer (0 – 200 m)
and in deeper waters on micronektonic fish, molluscs, and
crustaceans of sizes ranging between ,1 and 20 – 30 cm
1968; Sund et al., 1981; Me´nard et al., 2006; Dambacher et al.,
2010; Young et al., 2010)
, so they should have the potential to
prey on leptocephali. Most of these predators are considered to be
(Fritsches and Warrant, 2001; Fritsches et al.,
, so their ability to see the highly transparent leptocephali
may be a factor in determining the predator – prey relationships
between leptocephali and predators that forage in areas where
they are present. Other types of fish larvae are known to be preyed
on by both invertebrate and fish predators
(Bailey and Houde,
, but leptocephali grow to much larger sizes than most fish
larvae, which along with their extreme transparency, makes them
a special case among fish larvae.
There is a general lack of information about the predator – prey
dynamics of leptocephali
(Appelbaum, 1982; Miller, 2009)
the consumption of substantial numbers of leptocephali has only
been reported in a few rare cases
(Grassi, 1896; Matsui et al.,
. One modelling study examined the theoretical effect of
mortality of European eel leptocephali presumably from predation or
other factors, but the model parameters were not based on any
information directly related to leptocephali
(Bonhommeau et al., 2009)
Our study used an ongoing research programme and database on
the trophic ecology of predatory fish in the western and central
Pacific Ocean region described in
Allain et al. (2012)
the general occurrence of leptocephali in the stomach contents of
mostly pelagic top-predator fish. A literature review of previous
studies on these types of fish was also conducted to examine the
presence of leptocephali in the stomach contents. This provides the
opportunity to assess the prevalence of leptocephali in stomach
contents of a range of mostly oceanic predatory fish species and to
begin to evaluate the possible contribution of leptocephali to
oceanic food webs as prey, and if predators may have much influence
on the recruitment of eel populations. The presence of juvenile and
adult eels in the stomach contents database and in the previous
studies examined is also briefly evaluated.
The stomach contents of predatory fish collected from tuna fishing
vessels catching fish near the surface (purse-seine and
poleand-line) and at greater depths within the upper 400 m (longline)
between 2001 and 2014 were examined in the laboratory as part of
(Allain et al., 2012)
or ongoing research of the
Oceanic Fisheries Programme of the Secretariat of the Pacific
Community (SPC). These collections were made across a wide
region of the southwest Pacific Ocean ranging from just offshore
of northeastern Indonesia, eastward offshore of Papua New
Guinea (PNG), through southern Micronesia and the Solomon
Islands, near New Caledonia, Fiji, the Cook Islands, New Zealand,
and across French Polynesia (Figure 1a). A wide range of fish were
caught and sampled for stomach contents that included 8 species/
taxa of tunas and other Scombridae, 6 billfish, 7 Carangidae, 6
Gempylidae, 19 sharks or rays, and 39 other species, with the
common commercial species of tuna (yellowfin, Thunnus albacares;
skipjack, Katsuwonus pelamis; albacore, Thunnus alalunga; bigeye,
Thunnus obesus), wahoo (Acanthocybium solandri), and dolphinfish
(Coryphaena hippurus) being caught in the greatest abundances,
with substantial numbers of lancetfish (Alepisaurus spp.) and
rainbow runners (Elagatis bipinnulata) also being caught (Table 1;
Prey were identified to lowest taxonomic level, counted, and
weighed and measured when digestion was not too advanced.
Leptocephali in the Indo-Pacific usually have not been matched
with their adult species yet
(Miller and Tsukamoto, 2004, 2006)
and leptocephali in this research effort were only sometimes
identified to family or species level or measured for length because they
were typically in poor condition due to partial digestion. Juvenile
or adult eels were classified to family, genus or species using their
distinctive features. The abundance of leptocephali in the stomach
contents of predatory fish was evaluated using individuals with
nonempty stomachs (74.0% of 11 814 fish examined; 76 of 85 predator
species/taxa; 33 of 36 families).
Examination of the literature about the food contents of predatory
fish was also conducted using 75 published papers or reports that
included 40 species (Supplementary Table S1). This literature
review included mostly pelagic predatory fish that are of commercial
or recreational importance, and did not include many of the smaller
mesopelagic fish or coastal fish that may sometimes overlap in their
distributions with leptocephali. Therefore, it is not intended to be a
comprehensive literature review of this broad subject for all types of
predatory fish. However, the diets of 184 species of coastal or
continental shelf fish along the southeast US coast that overlap with the
habitats of some types of leptocephali such as the Ophichthidae have been
(Marancik and Hare, 2005)
, as well as the diets
of 50 species of fish along the northeast US coast
(Smith and Link,
and 52 fish species along the US west coast (Dufault et al.,
reported on the stomach contents of 50
predatory reef and inshore fish species from Puerto Rico and the
Virgin Islands. In addition, most mesopelagic fish appear to feed on
crustaceans or other invertebrates
(Clarke, 1980; Roe and Badcock,
1984; Bernal et al., 2013)
, or sometimes other mesopelagic fish
(Butler et al., 2001)
, and the stomach contents of 1000 mesopelagic
fish 25 species of 10 families in the North Atlantic were previously
checked for the presence of leptocephali
The stomach contents of 11 814 fish of 85 species/taxa (36 families)
were checked from fish that were caught in many areas of the
western Pacific mostly between 108N and 258S, and also near New
Zealand (Figure 1). The 8746 fish of 76 species/taxa (33 families)
with food in their stomachs contained 256 308 prey items of 598
taxa. Among those fish, 16 individuals (ind.) of 6 species had from 1
to 15 leptocephali in their gut contents. There were 34 leptocephali
in total that were eaten by lancetfish Alepisaurus ferox (7 ind.: 9
larvae), Alepisaurus brevirostris (1 ind.: 1 larvae), and Alepisaurus sp.
(2 ind.: 2 larva), rainbow runners, E. bipinnulata (2 ind.: 4 larvae),
yellowfin tuna, T. albacares (2 ind.: 16 larvae), a frigate tuna, Auxis
thazard (1 ind.: 1 larva), and a swallower, Pseudoscopelus sp. (1 ind.:
1 larva) as shown in Table 1. The percentage of individuals of each
of these types of fish that had eaten leptocephali was 0.06% for
yellowfin tuna, 3.2% for the less abundant frigate tuna, 6.6% for the lancetfish
in general, and 0.9% for rainbow runners (Table 1). Although most
leptocephali were identified as Anguilliformes larvae only, some
were identified as belonging to the Bathymyrinae
Ariosoma-type: Miller et al., 2013d)
eaten by a rainbow runner and a
lancetfish, Congrinae (Congridae) eaten by the swallower, and
Ophichthidae eaten by the frigate tuna and lancetfish. It is also
possible that a few individuals of bigeye and skipjack tuna may have
had leptocephali in their stomach contents, but were only labelled as
Anguilliformes, with no stage listed in the database. The
developmental stage or taxa of anguilliform fish (n ¼ 14) eaten by two great
barracuda (Sphyraena barracuda) were also not specified.
Most of the fish that had leptocephali in their stomach contents
were collected in the region to the northeast of PNG, except for the
lancetfish, which were mostly caught around New Caledonia, and
The number or percentage of fish (with food contents) that had leptocephalus larvae or juvenile/adult eels in their stomach contents is shown (number of
leptocephali or eels eaten is shown in parentheses). Species that included leptocephali or juvenile/adult eels in previous studies are also noted (see
Supplementary Table S1 for details). Poorly sampled species for some families shown are pooled at the bottom of the table within the “other families” category.
the swallower that was caught northwest of Fiji (Figure 1). Yellowfin
tuna were caught all across the sampling region, but the two fish that
contained leptocephali were in the PNG region. The yellowfin tuna
caught in the vicinity (4.988S, 159.598E) of the large atoll called
Frindsbury Reef was the only fish that had many leptocephali
(n ¼ 15) in its stomach contents. Frigate tuna were only collected
near PNG (not shown), and the one fish that had a leptocephalus
was caught near the coast (Figure 1a). The swallower that contained
a leptocephalus was caught near Fiji (Figure 1a).
The examination of stomach contents in previous studies of
mostly oceanic predators found that out of 75 published papers or
reports including 128 datasets about individual species (some
papers include data on more than one species) 42 387 predatory
fish of 40 species, only 15 papers listed the presence of leptocephalus
larvae in the stomach contents (Supplementary Table S1). This
included 8 out of 16 studies on lancetfish (A. ferox) that listed
leptocephali in the stomach contents. Only 1 out of 21 studies on
yellowfin tuna reported leptocephali being in stomach contents, but 2 out
of 7 studies on skipjack tuna included leptocephali. Only 1 (bullet
tuna) out of 26 studies on other species of tuna, and 1 (white
marlin) out of 22 datasets on 10 species of billfish reported
leptocephali being present. Two out of 11 studies on dolphinfish listed
leptocephali as prey. These various studies that listed leptocephali in the
stomach contents were conducted in a wide range of ocean areas
including the Pacific, Indian Ocean, Atlantic, and the Mediterranean
Sea. A few leptocephali might have been present among the gut
contents examined in some studies if they were included in categories
such as “unidentified fish” or “fish larvae”.
Some juvenile/adult eels had been eaten by 28 bigeye tuna,
T. obesus, which mostly consisted of snipe eels of the family
Nemichthyidae (n ¼ 74) and a few sawtooth eels of the family
Serrivomeridae (n ¼ 2). Two individual bigeye had each eaten
16 or 17 snipe eels. Single individuals of albacore and yellowfin
tuna, a moonfish (Lampris guttatus), and a lancetfish had also
eaten 1 – 3 juvenile/adult eels. In the literature survey of 75 papers,
the studies with juvenile/adult eels present in stomach contents
included 5 species of tuna in 9 studies and 7 species of other types
of fish in 9 studies (Supplementary Table S1). Similar to
leptocephali, these studies listing eels as prey items were conducted in all
the ocean basins where this type of research has been conducted.
This study evaluated how frequently leptocephali are present in the
stomach contents of predatory pelagic fish using the large 2001 –
2014 SPC database also used by
Allain et al. (2012)
southwestern Pacific Ocean region and by examining the presence or
absence of these larvae in other previously published stomach
contents studies. The stomach contents of 9000 fish examined from
the western Pacific in the present study indicated that there were
only 16 fish of 6 species that had eaten leptocephali recently
enough to be distinguished in their stomach contents. This database
included 40 species that seemingly could prey on leptocephali based
on their feeding ecology or the habitats they use, as well as 34
species such as sharks and rays, triggerfish, or smaller coastal
predatory fish that might not be expected to feed on leptocephali.
Similarly, only 12% of the datasets about individual species that
were examined listed leptocephali as being in the stomach contents
of more than 42 300 predatory fish of 40 species that might have the
chance to feed on these larvae, but more than half of those papers
including leptocephali were about the lancetfish, A. ferox
(Supplementary Table S1). These two types of information indicate
that leptocephali are very rarely encountered in studies of the
stomach contents of most large predatory fish from tropical to
southern temperate latitudes where leptocephali are present. In
addition, detailed summaries of 113 papers about the food habits of 184
species of coastal or continental shelf fish in the western North
Atlantic that were compiled by
Marancik and Hare (2005)
lists of stomach contents of 50 reef and inshore predatory fish
species of the West Indies
did not mention
leptocephali or eel larvae. This, and because other major data summaries of
the food contents of many species of coastal fish also do not mention
(Dufault et al., 2009; Smith and Link, 2010)
leptocephali have not been detected as being an important food
item in many species of coastal fish.
The same may be at least partly true for fish larvae in general,
because only 10 of the 75 papers examined in the literature survey
in Supplementary Table S1 listed fish larvae as being present in
their stomach contents data. However, fish larvae were more
commonly found in the SPC database examined in this study than
were leptocephali, with 351 fish of 16 species having fish larvae in
their stomach contents. The majority of the 3508 larvae were
eaten by 303 tuna of 6 species, but 25 lancetfish, 12 rainbow
runners, and 3 dolphinfish, species which had also eaten
leptocephali, had eaten fish larvae. In addition, the database included 908
fish of 17 species that ate 4577 fish with an uncertain larvae/juvenile
development stage designation. Most fish larvae are quite small
compared with the sizes of the predators examined, and juvenile
fish were listed more frequently in the database (2527 fish of 35
species ate 21 463 juvenile fish) and in the literature survey (19
studies listed juveniles), since these would be larger and would
digest less rapidly than fish larvae or leptocephali. Determining
the development stage of small fish is often difficult though, and
the terminology of the early developmental stages of fish is not
universally established and accepted
(Leis and Carson-Ewart,
due to the diversity in ways fish develop. Consequently, the
number of larvae extracted from the database examined in this
study and the number of studies from the literature mentioning
fish larvae are uncertain and should be considered with caution.
Even though leptocephali grow as large as or larger than many
juvenile fish, their body form is quite different from juvenile eels, so it is
not difficult to distinguish between the larval and juvenile stages
Although leptocephali seem to be rare or absent in the food
contents of oceanic predatory fish as noted previously
1982; Miller, 2009)
, as well as in coastal fish
Marancik and Hare, 2005; Dufault et al., 2009; Smith and Link,
, the large SPC stomach contents database and the
examination of many previous studies indicate that leptocephali are
sometimes eaten by several types of fish. More than one individual of
lancetfish, yellowfin tuna, and rainbow runners had consumed
leptocephali according to the database, along with single individuals of
three other species. However, one yellowfin tuna in the western
equatorial Pacific had consumed 15 leptocephali and 2 skipjack
tuna near the coast of PNG had eaten “many” Anguilla obscura
leptocephali (41 – 48 mm; Matsui et al., 1970), which proves that at
least individual fish will feed on leptocephali beyond just a
random encounter with a single larva if the circumstances are
favourable to do so. Among the 39 studies on tuna stomach contents
that were examined, leptocephali were listed in only 1 study on
yellowfin tuna, 2 on skipjack tuna and 1 on bullet tuna
(Ronquillo, 1953; Nakamura, 1965; Mostarda et al., 2007;
Supplementary Table S1)
, and no leptocephali were listed for
bigeye tuna or for 8 other tuna species. For dolphinfish, two
papers listed leptocephali
(Wu et al., 2006; Varghese et al., 2014)
Only 1 species of billfish was reported to have eaten leptocephali
(J u´nior et al., 2004)
, and none of the papers on wahoo or
mostly single papers on 14 other species listed any leptocephali
(Supplementary Table S1). However, if leptocephali were
common in stomach contents of these predators, they would have
been reported, and none of the studies on these large predatory
fish have ever mentioned or discussed leptocephali as prey of
these fish, except for listing them in the tables.
One type of fish whose stomach contents more frequently
contain leptocephali are lancetfish, of the genus Alepisaurus. The
long-snouted lancetfish, A. ferox, is often caught on pelagic fisheries
longlines and its food habits have been studied in several areas. In the
present study, in addition to 1 of the 8 shortsnouted lancetfish,
A. brevirostris, and 2 of the 5 Alepisaurus sp. having eaten a
leptocephalus, 6% of the 165 A. ferox had eaten 1 – 2 leptocephali. This is
consistent with the finding that 8 of the 16 studies on A. ferox
included leptocephali, which were conducted in the Atlantic
, eastern Pacific
(Haedrich and Nielsen, 1966)
(Moteki et al., 1993; Choy et al., 2013)
, southwest Pacific
, eastern Indian Ocean and Coral Sea
and Hattori, 1976)
, and Surga Bay Japan
(Kubota and Uyeno,
1970; Ito et al., 2005)
. The most detailed information about the
leptocephali consumed by lancetfish was that of Fourmanoir (1969),
which reported that 110 A. ferox had eaten 32 leptocephali of the
Congridae (17 larvae, 8 species), Nemichthyidae (14, 2 species),
and Muraenidae (1) families along with 610 other fish prey of 92
reported that the five leptocephali
eaten by four lancetfish (772 – 1276 mm) near Bermuda were
60 mm in length. There were five Ariosoma and one Muraenesox
leptocephali eaten near Hawaii
(Moteki et al., 1993)
leptocephali eaten by lancetfish in the eastern Pacific were two large
( 350 – 400 mm) notacanthid leptocephali (Albuliformes), which
were a species referred to as Leptocephalus giganteus
and Nielsen, 1966)
that grow to large sizes of .1.5 m
. Seemingly, the highest rates of leptocephalus consumption
by lancetfish were the 160 Conger myriaster leptocephali that were
eaten by 44 A. ferox in Surga Bay, Japan
(Ito et al., 2005)
, and the
27 “young anguilliforms” (97 – 220 mm) that were found in 30 of
the 35 A. ferox stomachs examined from the eastern Indian Ocean
and Coral Sea by
Fujita and Hattori (1976)
. Leptocephali were not
among the prey categories listed for lancetfish in eight other
(e.g. Potier et al., 2007; Varghese et al., 2014;
Supplementary Table S1)
To be able to carefully assess the meaning of the low rates of
occurrence of leptocephali in the stomach contents of the predatory
fish examined here and the higher rates of occurrence in lancetfish,
several factors need to be considered. Leptocephali are highly
transparent when alive
, which might provide a form of
, thus reducing their frequency of
detection by mobile predators. Because leptocephali appear to be able to
avoid being captured even by large plankton nets during the day
(Miller and McCleave, 1994; Miller et al., 2006, 2013b)
, they also
may be able to use their swimming ability to move away from
approaching predators before they are seen. In addition, the factor
of leptocephali using shape-change behaviour of curling their
bodies into various coil shapes that may make them resemble the
silhouettes of gelatinous zooplankton
(Miller et al., 2013c)
be considered. This behaviour could reduce predation by some types
of fish by acting as a form of Batesian Mimicry
(Ruxton et al., 2004)
because relatively few fish species seem to extensively feed on
gelatinous zooplankton in warmer-water areas
(Purcell and Arai, 2001;
. For example, a recent study including 1518 fish of 12
predator species including tuna, billfish, dolphinfish, barracuda,
and lancetfish in the eastern Arabian Sea does not even mention
gelatinous zooplankton, because only low percentages of jellyfish were
found in one species (silky shark, Carcharhinus falciformis) and salps
were only found in another species
(yellowfin tuna; Varghese et al.,
. Considering the likely presence of the gelatinous
zooplankton where these fish were feeding, the predators may have search
images for prey items that help them exclude gelatinous
zooplankton from their diet. If this is true, they may also exclude leptocephali
that have curled up in front of them because they resemble their
search images of gelatinous zooplankton
(Miller et al., 2013c)
This tactic of shape-change by leptocephali would not work for
predator species that are thought to feed on gelatinous zooplankton
such as ocean sunfish
(Pope et al., 2010)
, which in one case has been
found to feed on many European eel leptocephali in the Straits of
Messina of Italy
. That observation indirectly suggests
that the leptocephali had been curling up using the shape-change
behaviour when they detected the larger fish, because ocean
sunfish appear poorly adapted to actively pursue and capture
swimming larvae that were approaching their recruitment areas
et al., 2013c)
. The curling strategy may not work very well with
lancetfish either, which appear to be ambush predators (Romanov
and Zamorov, 2002) that may not be highly selective in their
search images for prey, because non-food debris is often present
in their stomachs
(Kubota and Uyeno, 1970; Ito et al., 2005)
have higher rates of ingestion of marine debris of anthropogenic
origin than other fish, with clear or white plastic having the
highest rate of ingestion
(Choy and Drazen, 2013)
. Lancetfish can
be cannibalistic if other food types are not abundant
et al., 2008)
and also sometimes eat transparent organisms such as
salps, polychaetes, and heteropods
(Haedrich, 1964; Kubota and
Uyeno, 1970; Fujita and Hattori, 1976; Ito et al., 2005; Potier
et al., 2007; Romanov and Zamorov, 2007)
. Interestingly, they
frequently consume Phronima amphipods that live inside transparent
barrel-shaped chambers made from gelatinous zooplankton
, especially in the Atlantic Ocean
. One 1265 mm
fish contained 32 Phronima, seemingly 29 chambers (salp tests)
along with 146 salps
lancetfish were consuming the 20 – 40 mm Phronima along with
their chambers in the Atlantic where they were the most important
food item. An appropriate sized curling leptocephalus would have a
similar silhouette as these chambers, so this may be another case of
when the shape-change of leptocephali would not deter predation.
Similarly, the diet of Ceratoscopelus warmingii, which had eaten
(five fish had eaten single leptocephali; Appelbaum,
, has an unusually diverse diet compared with other
, because they have been found to eat
siphonophores, ctenophores, and heteropods along with many other taxa
. It was unclear however, if some of the C. warmingii in
the study of
had consumed the leptocephali
within the net, since some of the leptocephali were found partly in
the mouth or in the oesophagus. Net feeding is not a consideration
for predators such as tuna and lancetfish that are not caught in
plankton nets though.
The higher frequency of lancetfish consumption of leptocephali
may also be partly related to their digestive system structure, because
they digest their prey in the intestine, not the stomach, making them
have good-condition food contents
have little ossification and are filled with jelly-like
glucosaminoglycan materials (GAG) overlain by a thin layer of muscle
Pfeiler, 1999; Miller, 2009)
, so they likely digest quickly, making
them unrecognizable shortly after being eaten if they are exposed
to digestive fluids. Therefore, the occurrence of leptocephali in
stomach contents might depend on how soon they were eaten
before the predator was captured to a greater degree than for prey
species with hard parts or large muscle masses. Tuna have high
metabolic rates and digest their food two to five times faster than
, so this may further reduce the
occurrence of leptocephali in studies of their stomach contents.
Experiments conducted by
Olson and Boggs (1986)
prey with low lipid content and non-compact musculature were
completely evacuated from stomachs 6 h after feeding. Prey lost
up to 20% of their weight within a few minutes after ingestion by
(Olson and Boggs, 1986)
, so leptocephali, with
only a thin layer of epidermis and muscle tissue outside of the
mucinous pouch containing the GAG, might become unrecognizable
very quickly. Small semi-transparent fish larvae in general may
digest rapidly and become un-identifiable with 15 – 30 min after
. Rapid digestion has also been
hypothesized to be occurring for gelatinous zooplankton that
might be consumed by tunas and billfish in the Mediterranean
Sea, after stable isotope mixing model results suggested that
gelatinous zooplankton were being consumed in greater numbers than
(Cardona et al., 2012)
. Consumption of leptocephali
that have a lower trophic position than gelatinous zooplankton
(Miller et al., 2013b)
could also cause a similar result in isotope
studies on predators.
This potential for rapid digestion and also the transparency of
leptocephali in combination with their apparent ability to mimic
gelatinous zooplankton makes it difficult to assess the degree to
which these unusual larvae are consumed by predatory fish. One
possibility is that they are eaten by some species such as yellowfin
tuna in some areas more frequently than stomach contents data
indicate, but they are not consumed as much by the wide range of
predatory fish as would be expected from the widespread presence
and abundances of leptocephali, because of their various apparent
predator avoidance adaptations. Leptocephali should directly
overlap in the upper 250 m of the ocean with a wide range of
predators such as tunas and billfish
(Young et al., 2010)
leptocephali likely show diel vertical migrations from the upper 100 m at
night to depths of 250 – 300 m during the day in open ocean areas
(Castonguay and McCleave, 1987; Miller, 2009)
. Overlap could
also occur where leptocephali can be abundant at specific times
and places such as along the edge of the continental shelf after
marine eels have been spawning
(Miller et al., 2002; Miller and
, in the offshore spawning areas of mesopelagic
(Miller and McCleave, 1994; Miller et al., 2006)
, or within
some anguillid eel spawning areas
(McCleave and Kleckner, 1987;
. They also appear ubiquitously present
throughout the subtropical gyres and boundary currents of the world’s
oceans and in warm inland seas
(Miller, 1995; Wouthuyzen et al.,
2005; Ross et al., 2007; Miller et al., 2006, 2015; Miller and
Tsukamoto, unpublished data)
. Although leptocephali are likely
present where fish predators feed from tropical to southern
temperate latitudes, it is difficult to clearly assess their likely abundances in
the places where predators were feeding in this and previous studies.
The observations of Grassi (1896; A. anguilla larvae eaten by ocean
sunfish) and Matsui et al. (1970; many A. obscura larvae eaten by 2
skipjack tuna) and the one yellowfin tuna in the present study that
ate 15 eel larvae indicate that leptocephali may be consumed in
large numbers at specific times and places, but this may only be
detected when predators are captured immediately after feeding
on the leptocephali because of the rapid digestion of larvae.
Another problem for understanding the amount of predation on
leptocephali is that their distribution and behaviour is not well
understood yet, because they are sometimes present at the surface
(,1 m) at night
(Ross et al., 2007; Miller, 2009)
even near the surface during the day where they have been captured
by seabirds, including one gannet and two noddy species in the
Atlantic and Pacific Oceans
(Seki and Harrison, 1989; Figueroa,
1997; Naves et al., 2002)
. Some species of leptocephali may vertically
migrate more than others
(Castonguay and McCleave, 1987)
leptocephali may be exposed to predators at various depths and light
levels. Predation might also occur on the metamorphosing
leptocephali that use tidal currents to enter shallow water during
recruitment to some tropical areas (see Miller, 2009), but leptocephali
were not reported in the diets of 50 predatory reef and inshore
fish species by
or in coastal predatory carangid
jacks or triggerfish (Supplementary Table S1) possibly due to
ingress at night. Other types of marine predators may also spatially
overlap with leptocephali, such as squid species that include fish in
their diets, but leptocephali do not appear present in their stomach
(e.g. Rosas-Luis et al., 2014)
or those of marine mammals
such as dolphins that also eat fish
(e.g. Amir et al., 2005; Pusineri
et al., 2007; Wang et al., 2011)
. Sea turtles feeding in the epipelagic
zone may also overlap spatially with leptocephali, and some
species are known to feed on gelatinous zooplankton in warm-water
(e.g. Tomas et al., 2001)
. A diver-caught siphonophore was
observed to have eaten an Ariosoma leptocephalus though
and Madin, 2010)
, and a net-caught chaetognath was found with
a small nemichthyid leptocephalus in its gut (Johnson et al.,
2006), but we are currently unaware of other reports of leptocephali
being consumed by marine animals.
The juveniles and adults of mesopelagic or sometimes coastal eels
are eaten by pelagic or coastal predators, as was shown by the
28 bigeye tuna that had eaten eels in the present study and by
11 species in the 75 previous studies we examined also having eels
in their stomach contents data (10 of the 21 studies on yellowfin
and bigeye tuna included eels; Supplementary Table S1). Some
marine mammals and sea snakes feed on benthic marine eels of
the Congridae and Muraenidae families
(Wang et al., 2011; Amir
et al., 2005; Ineich et al., 2007; Longenecker, 2010)
, so eels
and their larvae clearly contribute to some marine foodwebs.
However, the degree to which rapidly digestible, but possibly
highly predator avoidance adapted leptocephali are consumed by
marine fish appears to remain an open question that will require
further studies with various types of approaches to help better
understand the predator – prey relationships of these fascinating
and highly transparent fish larvae. At present, however, there
seems to be little indication that predation is major factor regulating
recruitment in fish that have a leptocephalus larva.
Supplementary material is available at the ICESJMS online version
of the manuscript.
This research was funded by the Pacific Islands Oceanic Fisheries
Management Project supported by the Global Environment
Facility. Co-funding was provided by the Australian Government
Overseas Aid Programme (AusAid) and the New Caledonian
Zone Economique de Nouvelle-Caledonie (ZoNeCo) programme.
We are grateful to the Pacific Islands countries and territories
observer programmes for the collection of samples, and we would like to
thank Caroline Sanchez, Cyndie Dupoux, and Malo Hosken for
their assistance with stomach content analysis.
Handling editor: Howard Browman
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