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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 554: 141–155, 2016
doi: 10.3354/meps11824 Published July 28
INTRODUCTION
How catadromous anguillid eels can migrate long
distances from their freshwater or estuarine habitats
through the seemingly featureless ocean and find
their pelagic spawning areas has been one of the
great mysteries in eel biology (Schmidt 1923,
McCleave 1987, Tsukamoto 2009, Righton et al.
2012). After they reproduce, they die, and their lar-
vae (called leptocephali) become widely distributed
as they drift with the currents toward recruitment
areas (Schmidt 1923, Shinoda et al. 2011, Miller et al.
2015a). Among the 19 species or subspecies of
anguillids, the European eel Anguilla anguilla
migrates the longest distance — up to 7000 km
(Aoyama 2009) to reach their spawning area in the
Sargasso Sea of the western North Atlantic (WNA;
Schmidt 1923). The western part of their spawning
area is shared with American eel A. rostrata
(McCleave et al. 1987), which migrates up to about
3500 km. Similar distances are covered by A. japon-
ica in the western North Pacific (WNP; Aoyama
2009). These temperate anguillid eel migrations are
among the longest 1-way migrations known for any
fish species (Alerstam et al. 2003). Even though some
tropical species spawn offshore after only short
© Inter-Research 2016 · www.int-res.com*Corresponding author: robert.schabetsberger@sbg.ac.at
Hydrographic features of anguillid spawning areas:
potential signposts for migrating eels
Robert Schabetsberger1,*, Michael J. Miller2, Giorgio Dall’Olmo3, Roland Kaiser1,
Finn Økland4, Shun Watanabe2, Kim Aarestrup5, Katsumi Tsukamoto2
1Department of Cell Biology, University of Salzburg, 5020 Salzburg, Austria
2College of Bioresource Sciences, Nihon University, Kanagawa 52-0880, Japan
3Plymouth Marine Laboratory, Plymouth PL1 3DH, UK
4The Norwegian Institute of Nature Research, 7047 Trondheim, Norway
5National Institute of Aquatic Resources, Technical University of Denmark, 8600 Silkeborg, Denmark
ABSTRACT: Catadromous anguillid eels (genus Anguilla) migrate from their freshwater or estu-
arine habitats to marine spawning areas. Evidence from satellite tagging studies indicates that
tropical and temperate eel species exhibit pronounced diel vertical migrations, from between
150−300 m nighttime depths to 600−800 m during the day. Collections of eggs and larvae of
Japanese eels A. japonica suggest they may spawn at these upper nighttime migration depths.
How anguillid eels navigate through the ocean and find their spawning areas remains unknown;
thus, this study describes the salinity, temperature and geostrophic currents between 0 and 800 m
depths within 2 confirmed and 3 hypothetical anguillid spawning areas during likely spawning
seasons. Within the 4 ocean gyres in which these spawning areas are located, many eels would
encounter subducted ‘Subtropical Underwater’ water masses during their nighttime ascents that
could provide odor plumes as signposts. Four of the spawning areas are located near the western
margins of where subducted water masses form cores of elevated salinities (~35.0 to 36.8) around
150 m depths, and one is located near the center of subduction. Low salinity surface waters and
fronts are present in some of the areas above the high-salinity cores. Spawning may occur at tem-
peratures between 16 and 24°C where the thermocline locally deepens. At spawning depths,
weak westward currents (~0 to 0.1 m s−1) prevail, and eastward surface countercurrents are pres-
ent. Anguillid eels possess acute sensory capabilities to detect these hydrographic features as
potential signposts, guiding them to their spawning areas.
KEY WORDS: Anguilla · Diel vertical migration · Orientation · Satellite telemetry · Spawning
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Mar Ecol Prog Ser 554: 141–155, 2016
migrations (Aoyama et al. 2003), all the known
anguillid eel spawning areas are over deep water
(>1000 m) in areas with warm surface currents, prob-
ably because the genus is derived from an ancestral
mesopelagic eel species (Inoue et al. 2010).
Besides the 2 confirmed spawning areas in the
WNA and WNP, at least 3 more offshore spawning
areas must exist in the other ocean gyres based on
species’ ranges and current patterns, but these areas
have not yet been confirmed by the collection of
small larvae (see ‘Materials and methods’). Relatively
few leptocephali of the 6 species of anguillid eels
present in the western (WSP) and central (CSP)
South Pacific have been collected and genetically
identified (Kuroki et al. 2008; A. australis, A. dieffen-
bachii, A. marmorata, A. megastoma, A. obscura, A.
reinhardtii) and the same is true for the 4 species in
the western Indian Ocean (WIO; Jespersen 1942,
Miller et al. 2015b; A. bengalensis, A. bicolor, A. mar-
morata, A. mossambica). Considerably more lepto-
cephali of some of those species have been collected
offshore of West Sumatra in the eastern Indian Ocean
(Jespersen 1942, Aoyama et al. 2007). Catches of
small leptocephali of A. celebesensis and A. borne -
ensis in the central Indonesian Seas indicate those
species can spawn after comparatively short migra-
tions close to major landmasses (Aoyama et al. 2003).
It is still a mystery as to how silver eels navigate
through the ocean to find their offshore spawning
areas. No information is available regarding the ex-
tent to which eels might use ‘beaconing’ (odor cues
that build up a gradient), ‘trail following’ (odor trails
from conspecifics), ‘route reversal’ (memory of sign-
post series), ‘path integration’ (knowledge of own
current position with respect to the goal in terms of
distance and direction), ‘compass orientation’ (e.g.
sun, moon, magnetic compass; genetic and/or experi-
ence based components), ‘vector orientation’ (genetic
or acquired information about distance and direction
of the goal), or ‘true navigation’ (navigation, map and
compass mechanism) as listed by Papi (2006) during
different stages of their journey. They possess various
sensory systems (vision, hearing, mechanoreception,
pressure detection, chemo-, electro-, and magneto -
reception; McCleave 1987, Tesch 2003, Tsuka moto
2009, Hunt et al. 2013, Westerberg 2014), and orien-
tation and navigation according to the earth’s mag-
netic field (see Nishi et al. 2004, Durif et al. 2013),
temperature gradients, odor trails (Westin 1990, van
Ginneken & Maes 2005), or ocean currents (Rommel
& McCleave 1973) may also potentially be used.
Oceanographic fronts, which are narrow boundaries
separating different water masses, have been hypoth-
esized to provide hydrographic structures that define
the spawning areas of anguillid eels. In the Sargasso
Sea, 2 temperature fronts consistently form in the
Subtropical Convergence Zone at about 22 and 24°C
during the February to April spawning season (see
Miller et al. 2015a), which gradually move northward
with seasonal warming (Ullman et al. 2007). Lepto-
cephali are consistently found south of the northern
front (Kleckner & McCleave 1988, Munk et al. 2010).
In the WNP, A. japonica spawns within the westward-
flowing North Equatorial Current (NEC) along the
seamount chain of the West Mariana Ridge (Tsuka -
moto et al. 2011, Aoyama et al. 2014). Adult eels, their
fertilized eggs, and recently hatched preleptocephali
have been collected exclusively along the seamount
ridge (Chow et al. 2009, Kurogi et al. 2011, Tsukamoto
et al. 2011, Aoyama et al. 2014), which seems to act as
a longitudinal signpost (Tsukamoto et al. 2003, 2011).
The latitude of spawning appears to be influenced by
a shallow salinity front formed by rainfall that can
move north or south, with spawning occurring on the
south side of the front (Kimura & Tsukamoto 2006,
Tsukamoto et al. 2011, Aoyama et al. 2014). Spawning
can take place at a wider range of latitudes when the
front is absent (Aoyama et al. 2014).
A new research approach of tagging migratory-
stage silver eels with pop-up satellite archival trans-
mitters (PSATs) has revealed information about their
unknown spawning areas and migration behavior.
The pop-up locations of New Zealand longfin eels
A. dieffenbachii have pointed towards a possible
spawning area east of New Caledonia in the WSP
(Jellyman & Tsukamoto 2010) that is generally con-
sistent with estimates obtained from modelling larval
transport (Jellyman & Bowen 2009). Silver eels of
2 tropical anguillids, the giant mottled eel A. mar-
morata and the Polynesian longfin eel A. megastoma,
that were tagged within the archipelago of Vanuatu
in the WSP, both had their tags pop-up in a poten-
tially shared spawning area northwest of Fiji (Scha-
betsberger et al. 2015).
Tagged temperate and tropical anguillid eels have
shown surprisingly similar oceanic diel vertical migra -
tion (DVM) patterns (Fig. 1), although most of them
were still far from their destinations. The eels pre-
dominantly migrate at 100 to 350 m depths during
the night and then quickly descend to 600 to 800 m at
dawn, remain there during the day, and ascend again
at dusk (Aarestrup et al. 2009, Jellyman & Tsukamoto
2010, Manabe et al. 2011, Schabetsberger et al. 2015,
Wysujack et al. 2015, Béguer-Pon et al. 2015) (Fig. 1).
Some species, such as A. rostrata (Béguer-Pon et al.
2015), A. japonica (Manabe et al. 2011), and A. dief-
142
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Schabetsberger et al.: Hydrographic structure of anguillid spawning areas
fenbachii (Jellyman & Tsukamoto 2010) occasionally
enter shallower water <100 m. The upper nighttime
migration depth seem to be adjusted in response to
the amount of moonlight, presumably to avoid epi -
pelagic, nocturnally foraging predators (Schabets -
berger et al. 2013, 2015, Chow et al. 2015). The sub-
surface upper nighttime migration depths reported in
most of these studies raise the question about how
migrating eels can detect the surface features of tem-
perature or salinity fronts that are mostly only pres-
ent in the upper 100 m (Kleckner & McCleave 1988,
Aoyama et al. 2014) if they remain deeper when
approaching the spawning area.
Among all 19 Anguilla species, spawning-condition
adult eels and eggs have only been collected for A.
japonica and A. marmorata (adults only), and they
were likely caught at depths between 150 and 300 m
(Chow et al. 2009, Tsukamoto et al. 2011, Aoyama et
al. 2014), which corresponds to the upper nighttime
migration depths of eels in the PSAT studies. This
suggests that the water masses at these depths
should be evaluated for potential oceanographic
structures that eels may use to locate their spawning
areas. The most distinctive hydrographic feature at
these depths is the high-salinity Subtropical Under-
water (STUW) that is present in all the major ocean
basins (Fig. 2A), which is formed by saltier water
being subducted from the surface into the lower ther-
mocline (Price 2001).
These high-salinity waters are subducted from the
surface mixed layer into the thermocline within the
centers of the wind-driven subtropical ocean gyres
(Qiu & Huang 1995, Qu et al. 2013). This process
consists of downward pumping from Ekman con -
vergence and horizontal advection by lateral geo -
strophic flow (Huang & Qui 1998 and references
therein). When these water masses are transferred
beneath the mixed layer (~100 to 350 m), they are
shielded from the atmosphere, and thus their proper-
ties are only slowly modified through mixing in the
ocean interior (Williams 2001). This type of water is
found within the spawning areas of the Atlantic eels
(Kleckner & McCleave 1988), A. japonica (Aoyama et
al. 2014), and in the presumed spawning regions in
the WIO (Pous et al. 2010). The STUW in the WSP
(Qu et al. 2013) is a prominent feature at the pop-up
locations of A. marmorata, and A. megastoma and
has been hypothesized to possibly help migrating
eels locate this area (Schabetsberger et al. 2013, 2015).
The objective of the present study was to show the
temperature and salinity structure and calculated
geostrophic currents plotted from data obtained from
autonomous drifting buoys (Argo floats) to interpre-
tively evaluate the hydrographic structure and cur-
rent flow patterns at the DVM migration depths of
eels in each subtropical gyre where anguillid spawn-
ing occurs or may occur. Possible spawning depths
were tentatively considered for inter-comparison of
areas to be between 150 and 250 m in accordance
with previous information from A. japonica (Tsuka -
moto et al. 2011, Aoyama et al. 2014). The potential
significance of STUW and other features are dis-
cussed in relation to the eels’ vertical migration
behavior and sensory capabilities.
MATERIALS AND METHODS
Defining spawning area locations
The Sargasso Sea spawning area of Anguilla angu -
illa and A. rostrata in the WNA was discovered by
Schmidt (1923) through the collection of recently
hatched larvae and has been subsequently studied
143
Fig. 1. Diel vertical migrations of individual migrating anguillid silver eels (Anguilla spp.) tagged with pop-up satellite trans-
mitters in (A) the western North Atlantic (Aarestrup et al. 2009), (B) western North Pacific (S. Watanabe unpubl. data), and
(C,D) western South Pacific (Schabetsberger et al. 2013, 2015). Grey areas: nighttime periods
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Mar Ecol Prog Ser 554: 141–155, 2016
during many cruises; thus the areas where spawn-
ing occurs have been defined by the presence of
small leptocephali (see Miller et al. 2015a, Fig. 2A).
We analysed data from March 2014 (Table 1), be -
cause larvae were collected during surveys in March
and April of that year (P. Munk & R. Hanel pers.
comm.).
Spawning areas in the WIO are not yet known
because only a few large leptocephali of the 4 species
in the region were collected during the Carlsberg
Foundation’s Expedition Round the World (Jespersen
1942) at stations in the Mozambique Channel and
north of Madagascar, and during more recent sur-
veys in the area (Miller et al. 2015b). Based on otolith
microstructure analyses of glass eels and elvers col-
lected in the region, a spawning area near the Mas-
carene Plateau was predicted and evaluated by drift
simulations (Robinet et al. 2008, Réveillac et al. 2009,
Pous et al. 2010). We defined an estimated spawning
area in this part of the WIO (Fig. 2A) and analysed
data for October 2013 (Table 1) in accordance with
information in Pous et al. (2010). Several species of
tropical eels are known to spawn locally off West
Sumatra in the eastern Indian Ocean (A. bicolor;
Jespersen 1942, Aoyama et al. 2007) and within the
Indonesian Seas (A. borneensis, A. celebesensis;
Aoyama et al. 2003). However, these more local
spawning areas (Fig. 2A) were not examined in the
144
Fig. 2. (A) Global map of salinity at 150 m depth from Argo float data for (long-term mean, 2001−2013) showing the elevated
salinities of subducted Subtropical Underwater (STUW) within the subtropical gyres. Rectangles: estimated spawning areas of
anguillid eels (bold: confirmed, analysed; dashed: hypothetical, analysed; thin: confirmed, not analysed; see Table 1). Black
transect lines indicate meridional sections shown in Fig. 3. Grey areas along coastlines indicate freshwater distribution of
anguillid eels. WIO: western Indian Ocean; WNP: western North Pacific; WSP: western South Pacific; CSP: central South
Pacific; WNA: western North Atlantic. (B) Global ocean surface currents derived from satellite altimeter and scatterometer
data for July 2013. White transect lines and enclosing rectangles show locations of meridional sections and enlarged maps in
Figs. 3 & 4, respectively, with current velocity arrows within the rectangles in bold for emphasis
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Schabetsberger et al.: Hydrographic structure of anguillid spawning areas
present study because they are
close to major landmasses and out-
side the major oceanic gyres and
only require short migrations in
order for the eels to spawn offshore
over deep water. In addition, there
is little or no coverage from the
Argo floats to record the hydro-
graphic conditions there.
The spawning area in the WNP
has been studied extensively since
its discovery in 1991, and its loca-
tion has been confirmed (Tsuka -
moto 1992, Tsukamoto et al. 2003,
2011, Shinoda et al. 2011, Aoyama
et al. 2014). In 2008, the first
spawning adults of A. japonica and
A. marmorata were caught along
the ridge at depths above 350 m
(Chow et al. 2009). Eggs of A.
japonica were first collected in
2009 (Tsukamoto et al. 2011)
and then again during cruises in
2011 and 2012 (Aoyama et al.
2014). Spawning occurs during
new moon periods based on both
back-calculated hatching dates of
leptocephali and when the eggs
and preleptocephali have been col-
lected. The eels spawn somewhere
below the thermocline because the
eggs and preleptocephali appear to
accumulate at about 150 m depths
(Tsukamoto et al. 2011, Aoyama et
al. 2014). The spawning area of A.
marmorata overlaps with that of
A. japonica (Kuroki et al. 2009),
and the newly discovered anguillid
species A. luzonensis may also
spawn offshore in the NEC (Kuroki
et al. 2012). We defined the spawn-
ing area as extending across most
of the latitudes where eggs and
preleptocephali have been col-
lected (Fig. 2A) and analysed a
time period that corresponded to
the June 2011 egg collections
(Table 1; Aoyama et al. 2014).
In the WSP a few leptocephali of
5 of the 6 species in the region
were collected (Jespersen 1942,
Miller et al. 2006, Kuroki et al.
2008), indicating that spawning
145
Ocean Anguilla Estimated Analysis Status of Salinity Temp. Westward Westward Eastward
gyre Species spawning area time period estimate (°C) currents at surface surface
150 m (m s−1) currents currents
WNA A. anguilla 24−30° N, Mar−Apr 2014 Confirmed, with 36.4−36.8 18−22 0.0−0.04 AC GS
50−73° W leptocephali <5 mm
A. rostrata 23−29° N, GSR
60−76° W
WIO A. bicolor West of 60.5° E, Oct 2013 Hypothetical, with 35.2−35.4 16−22 0.04−0.06 SEC SCC
A. bengalensis 13−19° S leptocephali >40 mm,
A. marmorata transport modelling
A. mossambica
WNP A. japonica 12−16° N, Jun 2011 Confirmed, with eggs, 34.6−35.0 16−24 0.06−0.14 NEC SCC
A. luzonensis 141−143° E preleptocephali, and
A. marmorata spawning adults
WSP A. australis Larvae: 5−20° S, Jul 2013 Hypothetical, with 35.0−36.0 16−24 0.00−0.08 SEC SECC
A. dieffenbachii 160° E−175° W; leptocephali >15 mm, ECC FBCC
A. marmorata Tagged eels from PSAT data
A. megastoma Vanuatu: 8−12° S,
A. obscura 170−175° E
A. reinhardtii
CSP A. marmorata 15−20° S, Jul 2013 Hypothetical, no larvae, 35.4−36.2 18−24 0.00−0.06 SEC SCC
130−135° W based on species ranges
A. megastoma and population structure
A. obscura
Table 1. Ocean gyres, eel species, estimated spawning areas and seasons used in this study, as well as research status of each estimated spawning area, and hydro-
graphic conditions of salinity, temperature, and geostrophic currents estimated from Argo float data at the presumed spawning depths of 150 to 250 m. WNA: western
North Atlantic; WIO: western Indian Ocean; WNP: western North Pacific; WSP: western South Pacific; CSP: central South Pacific. PSAT: pop-up satellite archival trans-
mitters. AC: Antilles Current; GSR: Gulf Stream Recirculation; SEC: South Equatorial Current; NEC: North Equatorial Current; ECC: Equatorial Counter Current;
GS: Gulf Stream; SCC: Subtropical Counter Current; SECC: South Equatorial Counter Current; FBCC: Fiji Basin Counter Current
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Mar Ecol Prog Ser 554: 141–155, 2016
likely occurs somewhere within the westward flow-
ing South Equatorial Current (SEC). Presently, no
leptocephali of A. dieffenbachii have been found
(Jellyman & Bowen 2009). The smallest leptocephali
of A. marmorata (Kuroki et al. 2008) were found close
to the pop-up locations of PSAT tags attached to
adult A. marmorata and A. megastoma released in
Vanuatu, which pointed to a potential shared spawn-
ing area (Schabetsberger et al. 2015). Therefore, we
defined a large spawning area in the WSP that is con-
sistent with the small leptocephalus catches and
encompasses the narrower area where satellite tags
surfaced (Fig. 2A). Although tropical eels may spawn
throughout various times of the year (Jellyman 2003),
we analysed data for July 2013, as tagged eels from
Vanuatu presumably reached their spawning area
between June and September of that year (Table 1;
Schabetsberger et al. 2015).
In the CSP, separate spawning populations of A.
marmorata and A. megastoma seem to exist based on
morphometric (Ege 1939, Watanabe et al. 2008, 2011)
and genetic analyses (Minegishi et al. 2008) of adult
eels. From the arrival of glass eels, Marquet (1992)
hypothesized that a relatively narrow eastern spawn-
ing area is located east of the Tuamotu Archipelago
(also see Jellyman 2003), although as yet no larvae
have been caught in the region. Due to the un -
certainty associated with the location and timing of
spawning in this region, we used this proposed
spawning area (Fig. 2A, Table 1), which is within the
representative water mass of the region and the same
time period as for the WSP. In Vanuatu, silver eels
appear to predominantly migrate during the rainy
season between January and April and reach the
spawning area approximately 3 mo later (Schabets-
berger et al. 2013). Weather conditions and migration
distances seem to be similar in the CSP.
Hydrographic analysis
The hydrographic structures of the 4 subtropical
gyres in which anguillid eels are present were exam-
ined graphically in areas shown in Fig. 2 and defined
in Table 1 (WNA, WIO, WNP, WSP and CSP). Patterns
of salinity, temperature, and currents at the 2 con-
firmed offshore spawning areas in the Atlantic and
North Pacific and within presumed spawning areas in
the Indian and the South Pacific oceans were plotted
in both vertical sections from 0 to 800 m and
horizontal sections at 150 m, which corresponds to the
upper DVM swimming depths of migrating eels and
the depths at which eggs and newly hatched larvae
may accumulate after spawning. Current systems are
defined in Table 1. The common patterns of hydro-
graphic conditions among all spawning areas were
qualitatively evaluated for similarities and differences.
The Argo project has deployed a global array of
about 3900 profiling floats that drift freely in the
ocean, where they measure temperature and salinity
from 0 to 2000 m every 10 d and then transmit the
data to satellites (www.argo.ucsd.edu/). Gridded tem -
perature and salinity fields from Argo floats with a
spatial resolution of 1°, a temporal resolution of 1 mo,
and 25 vertical levels from the surface to 2000 dbars
were used in the analysis (Hosoda et al. 2008). Geo-
strophic currents were calculated with respect to a
reference depth of 2000 m. Bathymetry data were
gathered from the ETOPO1 1 min dataset (www.
ngdc. noaa.gov/mgg/global/global.html). Global ocean
surface currents were plotted from data derived from
satellite altimeter and scatterometer data (Ocean
Surface Currents Analysis Realtime, www.oscar.
noaa.gov).
RESULTS
Salinity
Within all 4 investigated subtropical gyres, tongues
of high-salinity subducted STUW were present at the
upper nighttime migration depths of eels (between
100 and 350 m; Figs. 1 & 2A). The areas of formation
of the STUW, indicated by high surface salinity, occur
in the eastern parts of the gyres (Fig. 2A); the
STUW then extends obliquely towards the equator,
being carried by horizontal circulation. Four oceanic
spawning areas of Anguilla species are located near
the western margins (Fig. 2A) of where subducted
water masses form either cores of higher salinities
(WNA: 36.8; WNP: 35.0; WSP: 36.0) or inclined layers
of subducted water masses (WIO: 35.4; CSP: 36.2)
stretch down from the surface and bend equatorward
into the thermocline (Figs. 3A−D & 4A−D). The hypo-
thetical spawning area in the CSP, where no lepto-
cephali have ever been caught, is within the for -
mation area of STUW (Figs. 2A, 3E & 4E). In the
Pacific Ocean, the spawning areas are more or less
congruent with the latitudinal extension of high-
salinity waters, while in the Indian Ocean and the
Atlantic they are located northwest of them (Fig. 2A).
At the presumed spawning depths around 150 to
250 m, salinities ranged from 34.6 to 36.8, and
were highest in the WNA and lowest in the WNP
(Figs. 3A−E & 4A−E, Table 1). In 3 areas (WIO, WNP,
146
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Schabetsberger et al.: Hydrographic structure of anguillid spawning areas
WSP), shallow lenses (<100 m) of lower salinity water
masses were present, with salinities ranging from
34.0 to 35.0. Differences were also observed among
the 5 studied areas in the structure and upper
depths of the lower salinity water below the STUW
(Fig. 3A−E).
Temperature
Within the spawning area regions, surface temper-
atures (22 to 29°C) increased towards lower latitudes,
with a more gradual shoaling of isotherms along
higher latitudes in the WNP compared to the other
areas (Fig. 3F−J). Within these broader latitudinal
gradients, shallow temperature fronts may form lo -
cally (for example, in areas where different water
masses meet; Fig. 3K−O), but they are too narrow to
be visible in the temperature fields interpolated from
Argo data. Temperatures at estimated spawning
depths within or near the thermocline ranged from
16 to 24°C. The vertical structure of the thermocline
was congruent with the extension of the high-salinity
STUW in all areas (Fig. 3A−J). At the presumed
spawning latitudes the thermocline locally deepens
(Fig. 3F−J) and tongues of warmer water, stretching
east to west at 150 m, are bordered by colder water to
the north and south (Fig. 4F−J). Only in the WNA
(Fig. 4F) and the WIO (Fig. 4G) does spawning seem
to occur just north of these elevated temperatures at
spawning depths. Differences in the temperature
structure were also seen at deeper depths, with the
10°C isotherm reaching near or deeper than 800 m in
the WNA, but mostly remaining from 350 to 600 m
in the other areas (Fig. 3F−J).
Currents
Predominantly westward surface currents were
present in the anguillid spawning areas (Figs. 2B &
3K−O, Table 1). However, eastward countercurrents
also occurred. In the WNA, the Subtropical Counter
Current (SCC) was indicated to be above presumed
spawning depths (Fig. 3K), because fronts with east-
ward currents are known to exist in this area. In the
WIO (Fig. 3L), the spawning area was located just
north of the eastward SCC. In the WNP (Fig. 3M), the
spawning area extended within the NEC, south of
the SCC and north of the North Equatorial Counter
Current (NECC). The WSP had the most complex
current structure, with 4 bands of alternating east−
west current flows being present (Fig. 3N). Spawning
locations within this area could include both branches
of the SEC and the South Equatorial Counter Current
(SECC) or the Fiji Basin Counter Current (FBCC). In
the CSP, the spawning area extended across the
border of the eastward SCC and the westward
SEC (Fig. 3O). Weak westward currents that ranged
from 0 to 0.14 m s−1 prevailed at the presumed
spawning depths of the 5 areas (Fig. 4K−O, Table 1).
The strongest currents occurred outside the spawn-
ing areas, either to the north in the WNA (Gulf
Stream, GS) and the WSP (Equatorial Counter Cur-
rent, ECC), or to the south in the WNP (NECC).
DISCUSSION
Hydrographic features of spawning areas
Eels have been hypothesized to use hydrographic
features such as temperature and salinity fronts or
major current patterns to help decide where to
spawn (reviewed in Tsukamoto 2009), but our under-
standing of the importance of these and other
oceanic signposts and the sensory capabilities of eels
to detect them is still at a very early stage. In the
present study, we compared salinity, temperature,
and current patterns on a global scale and at a fine
scale within 2 confirmed and 3 hypothetical spawn-
ing areas in 4 different subtropical ocean gyres.
Spawning probably occurs within subducted high-
salinity water masses (i.e. STUW) where the thermo-
cline locally deepens, and within weak westward
currents. Low-salinity pools and stronger west- or
eastward currents are present above, which poten-
tially cause the formation of oceanographic fronts
(Fig. 5).
One interesting observation is that the STUW
water mass is present at the upper nighttime migra-
tion depths of eels in all of the spawning areas. This
water is subducted from the mixed layer into the
stratified thermocline and spreads horizontally over
large areas of all 4 subtropical gyres. However, with
the exception of the estimated spawning location in
the CSP, the analysed spawning areas are all located
along the western or northwestern edges of these
tongues of higher salinity water (Fig. 2). Vertically,
the spawning areas appear to be located at the lower
edges of the cores or within the STUW and near the
thermocline, as previously suggested in the WNP
based on the distributions of egg and prelepto-
cephalus catches (150 to 250 m; Aoyama et al. 2014).
The cores of the STUW water masses are centered
at about 150 m depths, as seen in individual surveys
147
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Mar Ecol Prog Ser 554: 141–155, 2016
148
Fig. 3. Meridional sections through spawning areas between 0 and 800 m depths (y-axis) of (A−E) salinity, (F−J) temperature
(°C), and (K−O) geostrophic currents (U, m s−1; red: eastward currents, blue: westwards currents) during known or presumed
spawning times. Dashed rectangles: assumed latitudinal and vertical extensions of spawning areas. Major west- and eastward
currents are identified (see Table 1)
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Schabetsberger et al.: Hydrographic structure of anguillid spawning areas 149
Fig. 4. Horizontal sections of (A−E) salinity, (F−J) temperature (°C), and (K−O) geostrophic currents (U, m s−1; red:
eastward currents; blue: westwards currents) at a depth of 150 m during known and presumed spawning times. Dashed
rectangles: latitudinal and longitudinal extensions of spawning areas; black vertical lines: positions of meridional sections
shown in Fig. 3. Abbreviations as in Table 1
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Mar Ecol Prog Ser 554: 141–155, 2016
(Kleckner & McCleave 1988, Roden 1998, Miller et
al. 2006, Aoyama et al. 2014). Due to the subduction
process, the STUW is injected into intermediate
depths and results in a deepening of the thermocline
(Price 2001, Williams 2001).
Above these subducted water masses, pronounced
temperature and weaker salinity gradients exist. Our
analysis showed there are areas of low-salinity water
in the upper 100 m at the spawning areas in the WIO,
WNP, and WSP. These lenses of low-salinity water
are caused by tropical rainfall (Kimura & Tsukamoto
2006). Oceanographic fronts not shown in this large-
scale analyses are known to form locally in the WNA
(Kleckner & McCleave 1988, Munk et al. 2010, Miller
et al. 2015a) and the WNP (Kimura & Tsukamoto
2006, Tsukamoto et al. 2011, Aoyama et al. 2014).
Similarly, fronts may also develop in the WIO at the
edges of the shallow layer (~50 m) of low-salinity sur-
face water (New et al. 2007) and in the WSP just
north of Fiji, where small anguillid larvae have previ-
ously been collected at the edges of the so called
‘western Pacific fresh pool’ (Roden 1998, Miller et al.
2006, 2009).
Transport of larvae to the major recruitment areas
is ensured by spawning predominantly within west-
ward surface currents (i.e. NEC, SEC) and at depths
where weak but consistent westward flows were
observed. However, eastward flowing countercur-
rents were also present within or near the spawning
areas. In the WNA, eastward transport within the
SCC has been proposed as a supplementary drift
route to the GS for A. anguilla larvae (McCleave
1993, Munk et al. 2010, Miller et al. 2015a). Dynamic
seasonal alterations of westward and eastward flow
patterns exist in the WIO (Schott et al. 2008), the WSP
(Chen & Qiu 2004), and the CSP (Martinez et al.
2009) that are strongly influenced by Indian Ocean
Dipole and El Niño−Southern Oscillation events,
respectively. This may result in occasional eastward
transport of leptocephali (Watanabe et al. 2014,
Schabetsberger et al. 2015), explaining for example
the presence of Anguilla spp. as far east as Pitcairn
Island or the Galapagos Archipelago.
Hydrographic signposts for eel orientation
Our global hydrographic analyses show that eels
swimming at the observed nighttime migration
depths would encounter various types of hydro-
graphic features that characterize their spawning
areas. They would either start migrating within the
STUW or encounter it near the spawning area as
weak zonal gradients in salinity when moving
towards the STUW cores. The salinity discontinuities
would be crossed twice a day during DVM based on
PSAT tagging studies (e.g. Aarestrup et al. 2009,
Jellyman & Tsukamoto 2010, Schabetsberger et al.
2015), with the eels migrating below the STUW dur-
ing the day and within it at night. The spawning
areas seem to be located where the thermocline is
weakening and extending deeper, with westward
currents being stronger than at deeper depths. The
eels would therefore experience different types of
vertical gradients on either side of these areas during
their DVMs. The salinity and temperature structures
at deeper daytime depths do not seem to provide
markers of spawning locations, however. It may be
unlikely that migrating eels can detect very gradual
horizontal gradients of salinity, temperature, or cur-
rents, especially in the context of their vertical migra-
tions, but subducted STUW water masses may con-
tain specific olfactory cues. The renewal time for
STUW is estimated to be 10 to 15 yr (Price 2001), so
150
Fig. 5. Schematic representation of (A) generalized salinity, (B) temperature (°C), and (C) current patterns, which may provide
signposts for migrating eels to detect their presumed spawning areas and depths. Spawning likely occurs in high-salinity
waters, near the thermocline, and within weak westward drift. Not all spawning areas show the same patterns of hydrographic
structures shown in Fig. 3
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Schabetsberger et al.: Hydrographic structure of anguillid spawning areas
compared with the surface mixed layer they may
provide stable water mass signatures that can be
detected by migrating eels.
Whether eels recurrently ascend to shallower
water to search for more ephemeral oceanographic
features above the STUW in order to locate their
spawning areas remains unknown until more tele-
metric data become available. For example, 2 A. mar-
morata and 1 A. megastoma tagged with PSATs in
Vanuatu that may have reached their spawning area
northwest of Fiji almost never entered waters above
90 m throughout their entire journey, and only once
did an eel come up to 75 m (Schabetsberger et
al. 2013, 2015). There is evidence that A. rostrata
(Béguer-Pon et al. 2015), A. japonica (Manabe et al.
2011), and A. dieffenbachii (Jellyman & Tsukamoto
2010) more frequently ascend to shallower water
above 75 m depth; however, in these studies the eels
may have been more severely affected by longer
holding before release and more invasive attachment
or implantation techniques (see Økland et al. 2013),
as tagged fish seem to exhibit irregular vertical
migrations in shallower water when they are ex -
hausted (Schabetsberger et al. 2015).
Using shallow oceanographic fronts, spawning area
landmarks would seemingly require the eels to enter
the upper 100 m at night to detect them, unless the
fronts are linked to deeper features. In the Sargasso
Sea (Kleckner & McCleave 1988) and the WSP
(Roden 1998, Miller et al. 2006), the edges of the
STUW cores correspond to regions where shallow
temperature/density fronts occur, but it is unknown if
these features move latitudinally in synchrony. Both
the salinity front within the A. japonica spawning
area (Kimura & Tsukamoto 2006, Aoyama et al. 2014)
and the temperature fronts in the Sargasso Sea
(Kleckner & McCleave 1988, Munk et al. 2010) are
most prominent above 100 m. Therefore, unless the
eels can perceive altered patterns of sound or light
transmission below fronts, or chemical components
of different water masses that sink downward on
either side, they may not be able to detect these
dynamic features without entering shallow water.
However, swimming at the base of these hydro-
graphic structures may provide sufficient sensory
input for them to determine their position in relation
to the different water masses above. Some eel spe-
cies such as A. rostrata (Béguer-Pon et al. 2015)
might be adapted to search for shallow features, but
it remains to be determined how important fronts are
as signposts, since A. japonica must have used other
cues when the salinity front was absent (Aoyama et
al. 2014).
Sensory ecology of finding spawning areas
Eels have a variety of sensory systems that would
enable them to detect hydrographic properties as
they move vertically through about half a km of the
water column every day while migrating toward the
spawning area, but the relative importance of these
sensory cues for navigation remains unknown. They
might be able to perceive strong horizontal and
vertical salinity gradients with sensory cells in their
highly sensitive nares, gills, esophagus, oral cavity,
and gastrointestinal epithelia (Tesch 2003, Evans et
al. 2005, Kültz 2012). In addition, they have a com-
plex set of osmosensors in their brain, pituitary gland,
and vasculature (Kültz 2012). Eels might also back-
track to follow imprinted odor trails from specific bio-
logical communities within certain water masses
(McCleave 1987, Westin 1990, Tsukamoto et al. 2003,
van Ginneken & Maes 2005). To locate mates, they
could follow odors from other eels, as released
mucus, urine, and/or bile salts are potential phero -
mones (Huertas et al. 2008).
Once within the spawning areas, there are vertical
gradients of salinity and temperature that eels could
use to detect their preferred spawning depths. For
example, within the high-salinity cores of STUW, an
eel ascending or descending at a speed of 5 m min−1
would experience salinity changes of more than 1.0
within 1 h. Concurrently, eels should be able to rec-
ognize the thermocline during their DVMs, assuming
their sensitivity is similar to some freshwater fish
that can detect rapid temperature changes down
to 0.05°C (Bardach & Bjorklund 1957). Additionally,
there is evidence that fish can accurately sense their
depth with the swimbladder acting as a pressure
receptor organ (Holbrook & Burt de Perera 2011).
Eels may also perceive the hydrodynamic field
around them, although in the open ocean they are
immersed within the moving currents where there is
a lack of stationary reference points (Montgomery et
al. 2000). They may not feel the current itself, but
sense infrasound and weak electric/magnetic fields
induced by ocean currents (Rommel & McCleave
1973, Sand & Karlsen 2000, Manoj et al. 2006).
In addition to the perception of salinity/odor, tem-
perature, and current patterns, several other cues
might also be used by the eels. They may be sensitive
to large scale gradients in the inclination and the
intensity of the earth’ magnetic field (Durif et al.
2013), and potentially even to the fine-scale mosaic
of geomagnetic anomalies in the ocean floor (Walker
et al. 2002, Lohmann et al. 2008), but it is still un -
known if they rely on a large-scale geomagnetic map
151
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Mar Ecol Prog Ser 554: 141–155, 2016
and compass for true navigation, a sense that is
important for orientation in sea turtles and salmon
(Walker et al. 2002, Papi 2006, Lohmann et al. 2008,
Putman et al. 2014). Polarized light provides an
azimuth bearing for the sun down to several 100s
of meters (Waterman 2006), but navigation according
to a direct sun or moon compass is unlikely at the
depths eels are migrating, as these celestial bodies
would only be visible down to about 50 m in
clear and calm ocean water (Partridge 1990). Sharp
descents and ascents (50 to 605 m) during dawn and
dusk (so-called spike dives) seem to provide polar-
ized light and/or magnetic field intensity cues for ori-
entation in bluefin tuna Thunnus maccoyi (Willis et
al. 2009), so eels might also obtain similar cues dur-
ing their vertical migrations, although this requires
further research.
CONCLUSIONS
The present study briefly evaluated the hydro-
graphic structures associated with 2 confirmed and 3
hypothetical spawning areas of anguillid eels, and
discussed these features in relation to what is known
about the oceanic migratory behavior and sensory
systems of eels. Although it is clear that the mystery
remains about how these eels can find their spawn-
ing areas during such long migrations, our study sug-
gests some hypotheses about various features and
senses that may be involved during the different
stages of their migration. All spawning areas include
STUW and probably shallower oceanographic fronts,
and the properties of the water masses associated
with either or both of these features could be im -
printed on by the larvae and later used by the adults
to return. However, the relative importance of these
hydrographic features for navigation in relation to
the possible use of magnetic cues remains to be
determined.
It is also not yet known if the hydrographic condi-
tions within the STUW are in some way advanta-
geous for spawning eels in terms of enhanced egg
and larval survival. Salinities and temperatures at
these depths do roughly correspond to the optimum
conditions for egg development (salinity ~35; 20 to
25°C) in Anguilla anguilla (Sørensen et al. 2016) and
A. japonica (Okamoto et al. 2009, Ahn et al. 2012,
Unuma et al. 2012) as determined under laboratory
conditions. Additionally, salinity is a primary deter-
minant of the buoyancy of marine fish eggs, which
influences their vertical distributions and dispersal
(Sundby & Kristiansen 2015). Eel eggs seem to be
positively buoyant (Tsukamoto et al. 2009, Sørensen
et al. 2016), so spawning in elevated salinities would
accelerate uplift into warmer water.
For effective protection and management of eels,
more information is urgently needed on the marine
part of their life cycle (Jacoby et al. 2015). Important
steps are to locate more of the spawning areas in the
Indo-Pacific, to determine how the eels find their
spawning areas, and whether changes in ocean−
atmosphere conditions affect that ability or the sur-
vival of their larvae (Knights 2003, Tsukamoto 2009,
Miller et al. 2009, Righton et al. 2012). So far, the
oceanic spawning areas of 4 species (A. anguilla, A.
rostrata, A. japonica, A. marmorata) have been deter-
mined through research cruises targeting the collec-
tion of smaller and smaller leptocephali over several
years or decades. Satellite tags now provide a
comparatively inexpensive way to narrow down the
search areas. These transmitters can also provide
information on the behavior of eels that can then be
related to environmental conditions observed with
remote sensing technologies, especially as extra or
improved sensors (e.g. salinity, low light conditions,
magnetic properties) become available in the future.
Numerical models used to simulate migration path,
duration, DVM behavior, energy expenditure, and
ambient oceanographic conditions (Béguer-Pon et al.
2016, Chang et al. 2016) could then be better cali-
brated against actual measurements. Additionally,
the sensitivity of eels to magnetism, odors, infra-
sound, and polarized light could be further evaluated
in laboratory experiments.
Acknowledgements. Funding for this study was provided by
the Austrian Science Fund (P28381-B29). These data were
collected and made freely available by the International
Argo Project and the national programmes that contribute
to it (www.argo.ucsd.edu, http://argo.jcommops.org) and
by Ocean Surface Currents Analysis Realtime (OSCAR,
www.oscar.noaa.gov). We thank 5 anonymous reviewers for
their critical comments.
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Editorial responsibility: Myron Peck,
Hamburg, Germany
Submitted: March 17, 2016; Accepted: June 29, 2016
Proofs received from author(s): July 14, 2016
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