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Catadromous anguillid eels (genus Anguilla) migrate from their freshwater or estuarine 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 temperatures 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 present. Anguillid eels possess acute sensory capabilities to detect these hydrographic features as potential signposts, guiding them to their spawning areas.
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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,
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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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Hamburg, Germany
Submitted: March 17, 2016; Accepted: June 29, 2016
Proofs received from author(s): July 14, 2016
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... Eels perform daily vertical migrations, swimming at depths of 100-300 m during night-time and at 600-800 m during daytime (Aarestrup et al., 2009;Righton et al., 2016;Schabetsberger et al., 2016), resulting in hydrostatic pressures ranging from 11 to 80 atm (Righton et al., 2012). Because the gas pressure in water is not dependent on the hydrostatic pressure, this results in an extraordinarily high partial pressure gradient between the flexible-walled swimbladder lumen and the surrounding tissues. ...
... Experiments were performed using European and American eels, but due to availability and logistics not all experiments could be performed on both species. The two species belong to the same genus and can hardly be separated by visual inspection, and they are even known to hybridize (Pujolar et al., 2014a(Pujolar et al., , 2014b. A. anguilla and A. rostrata spawn in the Sargasso Sea and show a similar vertical migration pattern during their spawning migration (Aarestrup et al., 2009;Righton et al., 2012;Schabetsberger et al., 2016). Previous experimental studies on swimbladder function used American and European eels successfully, and no difference in function was observed (Pelster et al., 1992(Pelster et al., , 1994Pelster & Scheid, 1992a, 1992b. ...
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Leakiness of the swimbladder wall of teleost fishes must be prevented to avoid diffusional loss of gases out of the swimbladder. Guanine incrustation as well as high concentrations of cholesterol in swimbladder membranes in midwater and deep‐sea fish have been connected to a reduced gas permeability of the swimbladder wall. On the other hand, the swimbladder is filled by diffusion of gases, mainly oxygen and CO2, from the blood and the gas gland cells into the swimbladder lumen. In swimbladder tissue of the zebrafish and the Japanese eel aquaporin mRNA has been detected, and the aquaporin protein has been considered important for the diffusion of water, which may accidentally be gulped by physostome fish when taking an air breath. In the present study expression of two aquaporin 1 genes (Aqp1aa and Aqp1ab) in swimbladder tissue of the European eel, a functional physoclist fish, was assessed by immunohistochemistry, and expression of both genes was detected in endothelial cells of swimbladder capillaries as well as in basolateral membranes of gas gland cells. In addition, Aqp1ab was present in apical membranes of swimbladder gas gland cells. We also found high concentrations of cholesterol in these membranes, which were several‐fold higher than in muscle tissue membranes. In yellow eels the cholesterol concentration exceeded the concentration detected in silver eel swimbladder membranes. We suggest that aquaporin 1 in swimbladder gas gland cells and endothelial cells facilitates CO2 diffusion into the blood, enhancing the switch‐on of the Root effect, which is essential for the secretion of oxygen into the swimbladder. It may also facilitate CO2 diffusion into the swimbladder lumen along the partial gradient established by CO2 production in gas gland cells. Cholesterol has been shown to reduce the gas permeability of membranes and thus could contribute to the gas tightness of swimbladder membranes, which is essential to avoid diffusional loss of gas out of the swimbladder. This article is protected by copyright. All rights reserved.
... The orientation mechanisms needed for them to synchronize their migration so that they congregate at the same time and location, despite beginning their migration from such different starting points, have to be reliable and efficient over long distances and timeframes. Adult migrating eels swim in pelagic water at depths between 200 and 800 m (Aarestrup et al., 2009;Schabetsberger et al., 2016). At those depths in the open ocean there are few or no guideposts. ...
... At those depths in the open ocean there are few or no guideposts. Although oceanic/salinity fronts are present in the spawning areas of most Anguillid species (Aoyama et al., 2014;Kleckner & McCleave, 1988;Munk et al., 2010;Schabetsberger et al., 2016), these features are not precise or predictable enough to guide adult migrating eels to a common spawning area. Odours from hydrothermal activity have also been put forward as a possible cue (Chang et al., 2020). ...
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Anguillid eels grow in freshwater but spawn in the open ocean. The cues that guide eels over long distances to the spawning area are unknown. The Earth's magnetic field can provide directional and positional information and is likely used by catadromous eels during their spawning migration; as magnetosensitivity and compass orientation have been reported in eels. To test whether this is theoretically possible, we compared the migratory routes of five species of temperate eels that undertake long migrations with the geomagnetic field of their distribution/spawning areas. We found that, regardless of the species and although routes are different between life stages, larvae of those species always drift along paths of increasing magnetic inclination and intensity, while adults follow reverse gradients. This is consistent with an imprinting/retracing hypothesis. We propose a general navigation mechanism based on larvae imprinting on a target magnetic intensity (or inclination) at the hatching area and on the intensity (or inclination) gradient during larval drift. Years later, adults retrace the magnetic route by following the gradient of decreasing total intensity (or inclination) values that occurs towards lower latitudes. As they reach the target value, adults switch to compass orientation to stay on the target isoline and reach the spawning area. The proposed mechanism fits for all temperate eels examined. Knowledge about navigational strategies of eels is important to evaluate the effectiveness of management strategies that involve stocking of juveniles displaced from one area to another to rebuild local populations.
... Various species respond to signposts. These include birds (Beck and Wiltschko, 1988;Fransson et al., 2001), turtles (Lohmann et al., 2001), eels (Schabetsberger et al., 2016;Naisbett-Jones et al., 2017), salmon (Putman, 2015;Scanlan et al., 2018) and lobsters (Boles and Lohmann, 2003). Signature magnetic and physical properties act as signposts. ...
... Signature magnetic and physical properties act as signposts. Examples include regionspecific magnetic intensity, temperature, odor, water salinity or currents (e.g., Fransson et al., 2001;Schabetsberger et al., 2016). For example, particular magnetic intensities can trigger animals to change directions during migration (Putman, 2015;Naisbett-Jones et al., 2017;Scanlan et al., 2018), reorient themselves to avoid ecological barriers and dangerous conditions (Beck and Wiltschko, 1988;Lohmann et al., 2001), or land at stopover sites for refueling (Fransson et al., 2001). ...
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Cognition, defined as the processes concerned with the acquisition, retention and use of information, underlies animals’ abilities to navigate their local surroundings, embark on long-distance seasonal migrations, and socially learn information relevant to movement. Hence, in order to fully understand and predict animal movement, researchers must know the cognitive mechanisms that generate such movement. Work on a few model systems indicates that most animals possess excellent spatial learning and memory abilities, meaning that they can acquire and later recall information about distances and directions among relevant objects. Similarly, field work on several species has revealed some of the mechanisms that enable them to navigate over distances of up to several thousand kilometers. Key behaviors related to movement such as the choice of nest location, home range location and migration route are often affected by parents and other conspecifics. In some species, such social influence leads to the formation of aggregations, which in turn may lead to further social learning about food locations or other resources. Throughout the review, we note a variety of topics at the interface of cognition and movement that invite further investigation. These include the use of social information embedded in trails, the likely important roles of soundscapes and smellscapes, the mechanisms that large mammals rely on for long-distance migration, and the effects of expertise acquired over extended periods.
... These DVM behaviors consist of swimming at much deeper depths during the day (mostly <800 m), and then coming up to shallower depths during the night (mostly >100 m). The exact depths of swimming appear to vary according to species or the hydrographic structure as observed in the studies cited above and as discussed by Schabetsberger et al. (2016). When freshwater eels start their spawning migration, they undergo several morphological changes, for example, eye diameter increases, melanization and extension of pectoral fins occurs, there is an increased development of swim bladder components (rete mirabile, gas gland and submucosa), and the belly of eels becomes a metallic silver color before Tsukamoto (1994) (yellow line), Matsui (1972) (red lines) and Yokose (2008) (white line) as shown by Tsukamoto (2009). ...
... approximately 5-7 • C in daytime during their DVM regardless of the depths of those temperatures . Schabetsberger et al. (2016) compared the DVMs of some anguillid species to an example DVM of the Japanese eel, which suggests some species like the Giant mottled eel A. marmorata and the Polynesian longfinned eel A. megastoma may also use a similar (about 5-7 • C) temperature to determine their daytime swimming depths (Schabetsberger et al., 2013(Schabetsberger et al., , 2015. However, this is clearly not the case for the European eel A. anguilla that has been observed to swim at both warmer and colder temperatures during the day . ...
Article
Pop-up satellite archival tags (PSAT) have been used to study the mysterious open ocean spawning migrations of several anguillid eel species including the Japanese eel, Anguilla japonica. To compare migration behaviors of Japanese eels in each general geographic region of their spawning migration, 7 silver eels (852–992 cm, 1095–1809 g) were tracked with PSATs and their swimming behaviors in regions of east of Japan, south of the Ogasawara Islands, and in their spawning area was analyzed. Three eels released from coastal Japan migrated east or southeastward, likely including some transport by the Kuroshio in the initial phase of the spawning migration. An eel released from the coast of Japan changed swimming depths as it crossed meanders and different water masses on different sides of the eastward flow of the Kuroshio Extension. An eel released west of the Ogasawara Islands moved mostly southward from the release site toward the spawning area where an eel released in the spawning area showed very stable diel vertical migrations (DVM). Five eels showed stable DVM for 9–47 days (60.0–72.1%) of the tracking periods (14–69 days), and 2 other eels showed abnormal behaviors. The daily rhythms of DVM behavior transitioned between shallower/warmer water at night (12.0–535.2 m/12.5–24.5 °C) and deeper/colder water during daytime (593.0–941.0 m/4.5–9.5 °C). The swimming depths of 5 eels had positive correlations with lunar age, moon altitude and sun altitude. Eels experienced almost the same daytime minimum water temperature (5.7 ± 0.98 °C) in the 3 areas regardless of depth, suggesting that they stop descending when they reach a temperature of approximately 5 °C. The ascending and descending occurred between around sunset and dusk, and dawn and sunrise, respectively. Three eels were ingested by predators near dawn (5:05–6:35) at depths of 119.5, 59, and 423.5 m when the eels start the decent phase of their DVM. Potential predators were estimated to be fish that have heat conservation ability such as tuna and swordfish based on rapid increases in recorded temperature. This study suggests that Japanese eels probably use similar DVM behaviors regardless of the location or environmental conditions during their spawning migration and that the swimming depths are determined by light and thermal environments. These behaviors are likely essential for predation avoidance.
... Differences were larger in 2018, though 67% of relative relationships maintained their directionality despite smaller differences among islands. selection via these cues have been observed in other pelagic spawning fishes, such as bluefin tuna Thunnus thynnus [93], blue whiting Micromesistius poutassou [94], and many eel species that share an evolutionary history with bonefish [95]. Further efforts in bonefish active tracking and hydrographic sampling are needed to confirm these hypotheses. ...
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Biophysical models are a powerful tool for assessing population connectivity of marine organisms that broadcast spawn. Albula vulpes is a species of bonefish that is an economically and culturally important sportfish found throughout the Caribbean and that exhibits genetic connectivity among geographically distant populations. We created ontogenetically relevant biophysical models for bonefish larval dispersal based upon multiple observed spawning events in Abaco, The Bahamas in 2013, 2018, and 2019. Biological parameterizations were informed through active acoustic telemetry, CTD casts, captive larval rearing, and field collections of related albulids and anguillids. Ocean conditions were derived from the Regional Navy Coastal Ocean Model American Seas dataset. Each spawning event was simulated 100 times using the program Ichthyop. Ten-thousand particles were released at observed and putative spawning locations and were allowed to disperse for the full 71-day pelagic larval duration for A . vulpes . Settlement densities in defined settlement zones were assessed along with interactions with oceanographic features. The prevailing Northern dispersal paradigm exhibited strong connectivity with Grand Bahama, the Berry Islands, Andros, and self-recruitment to lower and upper Abaco. Ephemeral gyres and flow direction within Northwest and Northeast Providence Channels were shown to have important roles in larval retention to the Bahamian Archipelago. Larval development environments for larvae settling upon different islands showed few differences and dispersal was closely associated with the thermocline. Settlement patterns informed the suggestion for expansion of conservation parks in Grand Bahama, Abaco, and Andros, and the creation of a parks in Eleuthera and the Berry Islands to protect fisheries. Further observation of spawning events and the creation of biophysical models will help to maximize protection for bonefish spawning locations and nursery habitat, and may help to predict year-class strength for bonefish stocks throughout the Greater Caribbean.
... Years of research rich in excitement and suspense: disappointment alternating with encouraging discoveries and periods of rapid progress with others during which the solution of the problem seemed wrapped in deeper darkness than ever Although our study did not yet yield definitive evidence of the mechanism(s) of navigational influence such as perhaps ocean currents, olfactory cues, temperature fronts, magnetic fields or seamounts [29][30][31][32][33] , ours is the first direct evidence of migrating adult European eels reaching the presumed breeding place in the Sargasso Sea. This is an encouraging discovery that completes the map of the spawning migration route that has emerged over the last 10 years 17-21 and offers some light on how to develop future work. ...
Article
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The European eel (Anguilla anguilla) is critically endangered (according to the most recent IUCN assessment) and has suffered a 95% decline in recruitment since the 1980s, attributed in part to factors occurring during the marine phases of its life-cycle. As an adult, the European eel undertakes the longest spawning migration of all anguillid eels, a distance of 5000 to 10,000 km across the Atlantic Ocean to the Sargasso Sea. However, despite the passage of almost 100 years since Johannes Schmidt proposed the Sargasso Sea as the breeding place of European eels on the basis of larval surveys, no eggs or spawning adults have ever been sampled there to confirm this. Fundamental questions therefore remain about the oceanic migration of adult eels, including navigation mechanisms, the routes taken, timings of arrival, swimming speed and spawning locations. We attached satellite tags to 26 eels from rivers in the Azores archipelago and tracked them for periods between 40 and 366 days at speeds between 3 and 12 km day⁻¹, and provide the first direct evidence of adult European eels reaching their presumed breeding place in the Sargasso Sea.
... However, oceanic spawning events of anguillid eels have never been witnessed, so questions about when and where they aggregate and spawn have remained, even after the spawning areas of some other anguillid species have been determined (Miller & Tsukamoto 2017, Kuroki et al. 2020. Recently, telemetry technologies have been used to investigate the spawning migration routes of temperate (Manabe et al. 2011, Béguer-Pon et al. 2015, Chow et al. 2015, Righton et al. 2016, Higuchi et al. 2018 and tropical (Schabetsberger et al. 2013(Schabetsberger et al. , 2016 anguillid eels, and although those studies demonstrated that anguillid eels perform clear diel vertical migrations while migrating back to their spawning areas, most studies did not provide much information about spawning locations. ...
Article
Facultative catadromous eels migrate back to the sea to reproduce, but their spawning behavior and locations have remained elusive. Using environmental DNA (eDNA), we identified a likely spawning site location and time of spawning of the Japanese eel. We detected Japanese eel eDNA at 400 and 600 m and recorded a likely sighting of this species at about 220 m using a deep-tow camera system 6 d before the new moon. A strong eDNA signal was obtained at 400 m from the apparent spawning event the morning after the estimated peak of eel spawning, 3 d before the new moon. These findings indicate that Japanese eels were already within the area where they were going to spawn at least 6 d before the new moon and then may have spawned near the strong eDNA station 3 d before the new moon. We concluded that the eDNA analysis is useful in searching for spawning sites and determining the timing of spawning of aquatic organisms with external fertilization that causes a temporary surge in eDNA, although prior knowledge of likely spawning sites is needed.
... For American eel a two-to three-fold increase in rete length has been reported, and in the Japanese eel a 1.6-fold increase has been detected [27,28]. Recent tracking studies revealed that migrating silver eels perform daily vertical migrations covering depth changes of several hundred meters [24,29,30]. The concomitant changes in hydrostatic pressure significantly affect the volume of the flexible-walled swimbladder, and it has been assumed that swimbladder function is improved during the process of silvering [24,31]. ...
Article
Full-text available
Background In physoclist fishes filling of the swimbladder requires acid secretion of gas gland cells to switch on the Root effect and subsequent countercurrent concentration of the initial gas partial pressure increase by back-diffusion of gas molecules in the rete mirabile. It is generally assumed that the rete mirabile functions as a passive exchanger, but a detailed analysis of lactate and water movements in the rete mirabile of the eel revealed that lactate is diffusing back in the rete. In the present study we therefore test the hypothesis that expression of transport proteins in rete capillaries allows for back-diffusion of ions and metabolites, which would support the countercurrent concentrating capacity of the rete mirabile. It is also assumed that in silver eels, the migratory stage of the eel, the expression of transport proteins would be enhanced. Results Analysis of the transcriptome and of the proteome of rete mirabile tissue of the European eel revealed the expression of a large number of membrane ion and metabolite transport proteins, including monocarboxylate and glucose transport proteins. In addition, ion channel proteins, Ca ²⁺ -ATPase, Na ⁺ /K ⁺ -ATPase and also F 1 F 0 -ATP synthase were detected. In contrast to our expectation in silver eels the expression of these transport proteins was not elevated as compared to yellow eels. A remarkable number of enzymes degrading reactive oxygen species (ROS) was detected in rete capillaries. Conclusions Our results reveal the expression of a large number of transport proteins in rete capillaries, so that the back diffusion of ions and metabolites, in particular lactate, may significantly enhance the countercurrent concentrating ability of the rete. Metabolic pathways allowing for aerobic generation of ATP supporting secondary active transport mechanisms are established. Rete tissue appears to be equipped with a high ROS defense capacity, preventing damage of the tissue due to the high oxygen partial pressures generated in the countercurrent system.
... Hydrographic structure and larval collections JMA hydrographic sections along 137°E indicated similar vertical water mass structures occurred each year during July in the subtropical gyre. Higher salinity water occurred in the upper 400 m in the north, and a more saline core of water (Subtropical Underwater (STUW) (see Schabetsberger et al. 2016) or Paci c Tropical Water) that had been subducted into the thermocline occurred at around 200 m at spawning latitudes within the NEC. The surface layer above the STUW was low in salinity and formed the salinity fronts at its northern edge. ...
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The diets of larval (leptocephali) anguillid and marine eels are poorly understood, despite studies on their gut contents or stable isotope ratios suggesting marine snow particles represent a food source. Concerns for Japanese eel Anguilla japonica stock conservation necessitate an improved knowledge of their larval ecology to better understand the causes of their recent decline in numbers and fluctuating recruitment into East Asia. To understand the distribution of and variation in size of leptocephali in relation to their feeding, we examine carbon and nitrogen stable isotope ratios of larvae from seven research cruises (2002–2013) in the North Equatorial Current spawning area. Preleptocephali (2–3 days old, ~5 mm total length) isotope ratios reflect maternal ratios, but feeding-stage leptocephali (8–56 mm) tend to have higher ∂15N values with decrease of latitude typically in areas south of a salinity front. Neither ∂15N nor ∂13C ratios are clearly related to longitude or larval size < 30 mm, but ∂13C values of larvae > 40 mm are lower further downstream in the North Equatorial Current and Subtropical Countercurrent. Differences in ∂13C values might be a function of varying spatial baselines in the two currents apart from the spawning area. Although among-year larval isotope ratio differences may reflect temporal baseline variation related to the location of the salinity front, more research with much wider range observations in the spawning season is required because ingested marine snow particles might differ with larval growth and location.
Article
Although juvenile anguillid eels live in freshwater/estuarine habitats, and marine eels live in diverse ocean environments ranging from shallow-to-deep continental shelf areas and around islands to deep-benthic habitats and deeper meso- and bathy- pelagic zones, the larvae (leptocephali) of all species mix together in the ocean surface layer. All types of eel habitats are present in the western South Pacific (WSP), so it is a unique region for studying long-lived leptocephali, especially because the westward flowing South Equatorial Current (SEC) and several countercurrents pass through many different WSP island groups and deep waters where both anguillid and marine eels live and spawn. Large mouth-opening IKMT sampling surveys for leptocephali were conducted in the southwest Pacific extending to French Polynesia in Jan-Mar 2013 (99 tows, 78 stations, 1052 larvae) and Jul-Sept 2016 (187 tows, 111 stations, 3976 larvae) that collected about 152 species of 18 anguilliform and elopomorph families. The larvae of mesopelagic serrivomerid eels were the most abundant taxa in all oceanic areas, and they were particularly abundant at northern SEC or equatorial latitudes. Australian and New Zealand anguillid eels had spawned in the western SEC areas, as previously detected, and the larvae of tropical anguillids were also only caught in western areas. The larvae of the mesopelagic nemichthyid and derichthyid eels were also widely distributed at lower abundances and with more patchy distributions, but larvae of Eurypharyngidae, Cyematidae, and Mongnathidae were rare. Shallow-water eel larvae were most abundant west of New Caledonia near the banks of the Chesterfield Islands, or near other island-groups, but they were rare in the 2 easternmost 2016 transects passing by both sides of Tahiti. Some conger eels were suggested to have spawned in offshore areas in the western region. Congrid Ariosoma and various shallow-water or slope eels had spawned in the region near the Chesterfield Islands or near New Caledonia where current jets can transport larvae westward, and eastward countercurrents exist. Some taxa of larvae of coastal species (muraenesocids, and elopomorphs) were extremely rare, all non-mesopelagic eel larvae were rare in the far-eastern transects, but the New Caledonia region with large shelf areas appears to be a high biodiversity region for marine eels, as it is for reef/shore fish in general.
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Chapter
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