Fish and Fisheries. 2021;00:1–18.
Received: 22 April 2021
Revised: 9 September 2021
Accepted: 21 September 2021
DOI : 10.1111/faf.126 21
A unifying hypothesis for the spawning migrations of
temperate anguillid eels
Caroline M. F. Durif1 | Hans Hagen Stockhausen2 | Anne Berit Skiftesvik1 |
Alessandro Cresci1 | Daniel Nyqvist3 | Howard I. Browman1
This is an open access article under the terms of the Creat ive Commo ns Attri bution-NonCo mmercial License, which permit s use, distribution and reproduction
in any medium, provided the original work is properly cited and is not used for commercial purposes.
© 2021 The Authors. Fish and Fisheries published by John Wiley & Sons Ltd.
1Institute of Marine Research, Ecosystem
Acoustics Group, Austevoll Research
Station, Storebø, Norway
2Institute of Marine Research, Bergen,
3Department of Environment, Land and
Infrastructure Engineering, Politecnico di
Torino, Turin, Italy
Caroline M. F. Durif, Institute of Marine
Research, Ecosystem Acoustics Group,
Austevoll Research Station, Sauganeset 16,
5392 Storebø, Norway.
This work was funded by the Norwegian
Institute of Marine Research's project “Fine-
scale interactions in the plankton” (Project
# 15579) and the Norwegian Research
Council (MAREEL: The importance of the
marine habitat for the critically endangered
European eel, Project #280658)
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 catadro-
mous eels during their spawning migration; as magnetosensitivity and compass ori-
entation 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 spawn-
ing 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.
Anguilla sp., compass orientation, geomagnetic field, magnetic inclination, magnetic total
intensity, secular variation
DURIF et al.
1 | INTRODUCTION
Many fish undertake long distance migrations to feed and spawn.
How these migratory species find their way to distant areas, across
several thousand kilometres, is a mystery. Anguillid eels are char-
acterized by long- distance migrations between growth habitats and
spawning areas. All 19 species of anguillids (Anguilla sp., Anguillidae),
also called freshwater eels, breed in open- ocean areas but spend
their growth phase in coastal and freshwater habitats (Tesch, 2003).
They are almost all panmictic (each species is structured as one
population), having unique spawning areas that are located over
deep water (Aoyama, 2009; Miller, 2009; Tesch, 2003; Tsukamoto
et al., 2002). Anguillid eels also have in common that the exact time
and location of their spawning site is either uncertain or unknown
because spawning events have never been observed in the wild. For
some species, approximate spawning locations have been identified
by careful examination of the distributions of their leptocephalus
larvae— or eggs in the case of the Japanese eel (Anguilla japonica)—
collected during scientific surveys (e.g. Kuroki et al., 2020; Miller
& Tsukamoto, 2017; Schmidt, 1922; Tsukamoto et al., 2011). In ad-
dition, sexually mature specimens of the A. japonica and the mar-
bled eel (A. marmorata) have been collected, putatively on or near
their spawning area (Chow et al., 2009; Kuroki et al., 2009; Miller &
Tsukamoto, 2017; Tsukamoto, 2006; Tsukamoto et al., 2003, 2011;
Yoshinaga et al., 2011).
Anguillid eels are, for the most part, widely distributed during
their growth phase. For example, the European eel (A. anguilla)
occurs in habitats between Norway and Morocco, but spawns in
the Sargasso Sea (Als et al., 2011; Pujolar, 2013; Schmidt, 1922;
Tesch, 2003). How eels find their way back to their unique spawn-
ing area is still a mystery. 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. Although oceanic/sa-
linity 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).
However, for the Atlantic eels, they do not align with the known
distribution of leptocephalus larvae and cannot explain the full ex-
tent of the migration.
One possible cue that could guide the orientation of eels during
their migration is the geomagnetic field. This environmental cue
is omnipresent and is unaffected by time of day or oceanographic
or weather conditions. It could guide eels as a “compass,” that is, a
direction relative to magnetic North, but can also potentially pro-
vide positional information, that is, act as a kind of GPS (Lohmann
et al., 2007). This “map” can be derived from components of the
geomagnetic field, such as inclination (I), horizontal (H), vertical (Z)
and total int ensit y (F), and/or declination, the values of which change
gradually over the earth's surface. Many fishes can perceive magnetic
field information (Cresci et al., 2019; Hellinger & Hoffmann, 2009;
O'Connor & Muheim, 2017; Putman, Scanlan, et al., 2014; Quinn
& Brannon, 1982; Shcherbakov et al., 2005; Walker, 1984; Willis
et al., 2009). Compass orientation, manifested as changes in the
swimming direction relative to the direction of magnetic north,
has been demonstrated in the continental life- stages of A. anguilla
(Cresci, 2020; Cresci et al., 2017; Durif et al., 2013). Whether eels
use other components of the magnetic field, such as intensity and
inclination (i.e. the magnetic map hypothesis), which could provide
them with positional information during migration, remains unknown
(Durif et al., 2017). Such a magnetic map has been demonstrated
in many animals, including birds, butterflies, newts, spiny lobsters,
salmon and sea turtles (Boles & Lohmann, 20 03; Freake et al., 2006;
Lohmann et al., 2007; Mouritsen, 2018; Munro et al., 1997; Phillips
et al., 2002), but not as yet in eels.
1. INTRODUCTION 1
2. METHODS 3
2.1. Overview of the methods 3
2.2. Study species and their spawning areas 3
2.3. Description of the data 8
2.3.1. Geomagnetic data 8
2.3.2. Migration routes and spawning areas of
3. RESULTS 8
3.1. Geomagnetic gradients between growth and
3.2. Secular variation 9
4. DISCUSSION 11
4.1. A general mechanism for navigation of
migrating temperate anguillid eels
4.2. Migratory steps 1 and 2: Imprinting and the
magnetic map hypothesis
4.3. Migratory steps 3 and 4: «Aiming off» 12
4.4. Migratory step 5: The end of the journey 13
4.5. Use of inclination (I) and/or total intensity (F)
in the navigation of eels
4.6. Geomagnetic secular variations 14
4.7. Perspectives 14
CONFLICT OF INTEREST 15
AUTHOR CONTRIBUTIONS 15
DATA AVAILABILITY STATEMENT 15
DURIF et a l.
True navigation requires that an organism forms a mental grid
in relation to the target destination and adjusts its “compass” as it
moves towards that destination (Phillips, 1996). The grid, or map,
can be composed of two environmental gradients ideally aligned
perpendicular to one another (Wallraff, 1990). These can be altitude,
depth, temperature, for example, but can also be components of
the geomagnetic field, such as inclination (I) and/or total intensity
(F) (Gould, 1980). Both, F and I, decrease from the poles towards
the equator in a North– South gradient. Thus, magnetic field isolines
(representation on a map of the areas characterized by the same
value of a magnetic field component) most often run parallel to each
other along the East– West axis (Bostrom et al., 2012). This means
that an animal can navigate along a North– South axis by using I or
F. However, because there is no distinct gradient of either I or F
over longitude, navigation based on this cue becomes more difficult
when moving along the East– West axis. For example, it appears un-
likely that A. anguilla could navigate back to its spawning area in the
Sargasso Sea by following gradients of I or F.
Complicating the magnetic map hypothesis are the variations
and drift in the Earth's magnetic field that occur over decades, so-
called secular variation. Due to this, the geomagnetic characteristics
of the geographical location of the target area (spawning area) will
typically vary between generations of eels, or even during the life
cycle of an individual eel. While imprinting this target location during
the early- life stages (hatching and larval stage), versus inheriting it,
could help solve this problem, it may not completely resolve it in the
case of anguillid eels that have a long life cycle. For those eels, the
initial magnetically imprinted location may correspond to a different
geographical location when the eel undertakes its return migration
up to 30 years later. Thus, while the geomagnetic field is often cited
as the most probable environmental cue that could guide anguillid
eels during their migrations, how eels could make use of it in practice
has never been explained.
In this study, we investigated whether certain components of
the geomagnetic field are available for eels to use as guidance cues
in their migration between their growing and spawning areas and
whether such patterns are consistent over the distribution area of
different anguillid species. We present a comprehensive hypothesis
on the orientation mechanisms of anguillid eels throughout their life
cycle. Specifically, we propose that adult eels find their spawning
areas by following the features of the magnetic field (both target
values as well as magnetic field gradients) that they have imprinted
during their migration towards the continental shelf as lar vae and
post- larvae. To test this hypothesis, we assessed (i) whether retrac-
ing the magnetic gradients along the migratory route of eel lep-
tocephali is consistent with the migratory routes of adult eels on
their way back to the spawning area; (ii) whether these gradients
are consistent between different anguillid species present in both
southern and northern hemispheres and (iii) how secular variation
would affect the navigation accuracy of eels over the timeframe of
their average longevity. To accomplish this, we used existing models
to calculate the geomagnetic inclination and field intensity in four
different oceans and examined the distributions of five temperate
species of eel, A. anguilla, A. rostrata (American eel), A. japonica,
A. australis (short- finned eel), A. dieffenbachii (New Zealand longfin
eel), to identify whether similar patterns of the geomagnetic field
exist between their growing and spawning areas.
2 | METHODS
2.1 | Overview of the methods
To examine whether suitable magnetic gradients are present be-
tween the growth and the spawning area, we mapped the magnetic
components (intensity F and inclination I) along with biological data
(larval drift and known trajectories of returning adult eels) of five
temperate eel species. Our conclusions are based on calculations of
the ranges of values and the overlap between growth and spawn-
ing areas of different species as well as maps to assess consistency
To evaluate the effect of secular variation on the potential dis-
placement of eels we calculated the magnetic components at the
spawning areas for different time intervals representing the lifecycle
of an eel. We calculated the difference in total magnetic intensity
and inclination between hatching and spawning (ΔF = Fhatch − Fspawn;
ΔI = Ihatch − Ispawn) of a hypothetical eel born in 1900 and assumed
several ages at maturation (or age at silvering). We did this for A. an-
guilla, A. rostrata and A. japonica, for which we have the most precise
location of spawning areas. To determine relevant time intervals, we
used information on age of eels at maturity (i.e. silvering). Silvering
depends on growth and, therefore, on environmental conditions such
as temperature. Eels in the southern part of the distribution mature
at an earlier age than eels in the north (Daverat et al., 2012; Durif
et al., 2009; Svedäng et al., 1996; Vøllestad, 1992). A rough average
for silver A. anguilla females is 10 years in the south and 20 years
in the north (Durif et al., 2009, 2020; Poole & Reynolds, 1996).
Silver males are much smaller and younger and migrate at ap-
proximately 5 years of age in the south and 10 years in the north
(Durif et al., 2009). Actual ranges are 3 and 57 years for females
and between 2 and 33 years for males (Durif et al., 2009; Poole &
Reynolds, 1996). Therefore, we calculated ΔF and ΔI between 5 and
50 years, at intervals of 5 years. We used the same range/intervals
for the A . japonica silver eels, although they are much younger (ap-
proximately 9– 10 years; Yokouchi et al., 2012).
2.2 | Study species and their spawning areas
All anguillid eels are characterized by five life stages whose durations
vary according to the species: (a) the larval phase or leptocephalus
which is fully oceanic; (b) the glass eel stage which begins when eels
approach the continent and during which they actively orient to-
wards the coastline and freshwater habitats; (c) the yellow eel stage
which is the continental phase during which eels grow and accumu-
late fat; (d) the silver eel stage during which eels migrate towards the
DURIF et al.
sea and start their sexual maturation and (e) the reproductive stage,
about which we know very little, because sexually mature eels have
never been caught alive in the wild.
We focused on five anguillid species (Figures 1– 4), in the north-
ern hemisphere (A. anguilla, A. rostrata and A. japonica) and in the
southern hemisphere (A. australis and A. dieffenbachii). A. rostrata
and A. anguilla spawn in slightly overlapping areas of the Sargasso
Sea; this is known from the distribution of catches of their larvae
(McCleave et al., 1987; Miller et al., 2015; Schmidt, 1922). A. an-
guilla individuals that have embarked on their spawning migration
have been tracked as far as the Azores (albeit only one individual),
a location that represents approximately half of the journey to the
FIGURE 1 (a) Isolines of geomagnetic total intensities (contours every 500 NT) and (b) inclination (contours every 2°) calculated for the
year 2014. Geographic distribution (source = IUCN) and spawning areas are represented in green and orange boxes of Anguilla rostrata and
A. anguilla respectively. The dots represent collections of leptocephalus larvae (data source: ICES Eggs and Larvae database). The size of dots
is proportional to the length of the larvae (3– 88 mm). A. rostrata has been recorded in South America but its occurrence is rare (Benchetrit &
McCleave, 2015). The grey arrows represent major currents in the Atlantic Ocean (AC, Azores Current; FCC, Frontal Counter Currents; GS,
Gulf Stream; NAC: North Atlantic Current)
DURIF et a l.
FIGURE 2 (a) Isolines of geomagnetic total intensities (contours every 1,000 nT) and (b) inclination (contours every 2°) calculated for the
year 2014. Growth (source = IUCN) and spawning areas are represented in green and orange boxes for Anguilla australis and A. dieffenbachii
respectively. The grey arrows represent major currents in the South Pacific (EAC, East Australian Current; SEC, South Equatorial Current; TF,
DURIF et al.
FIGURE 3 Anguilla japonica. (a) Isolines of geomagnetic total intensities F (contours every 1,000 nT) and (b) inclination I (contours every
2°) calculated for the year 2014. Growth (source = IUCN) and spawning (box) areas are represented in green. Leptocephalus larvae are
depicted in orange (larval collection data were redrawn from Shinoda et al., 2011). The grey arrows represent major currents: Mindanao,
North Equatorial (NEC) and Kuroshio currents. Japanese eel release (yellow triangles) and tag surfacing location (red square) of PSAT (popup
satellite tag) from Higuchi et al. (2021)
DURIF et a l.
spawning area (Aarestrup et al., 2009; Righton et al., 2016). An indi-
vidual of A . rostrata was tracked for 2,400 km from Canada down to
the Sargasso Sea, providing the first direct evidence of the location
of the Atlantic spawning area (Beguer- Pon et al., 2015).
Anguilla japonica spawns in the North Equatorial Current (NEC),
west of the Mariana Islands (Tsukamoto et al., 2003). Eggs of A. ja-
ponica (Aoyama et al., 2014; Tsukamoto et al., 2011; Yoshinaga
et al., 2011) as well as two sexually mature males (Chow et al., 2009)
and two post- spawning females (Kurogi et al., 2011), were collected
along the West Mariana Ridge. Several migration routes have been
proposed for A. japonica, one that runs opposite of the Kuroshio
current and one that runs on a more direct southern trajectory
(Tsukamoto, 2009). However, these have not been entirely verified
by tracking or collection of migrating individuals.
Seven species and subspecies of anguillid eels are present in the
South Pacific region (Jellyman, 1997)— we focused on the two for
which there is the most knowledge. A. australis is found in eastern
Australia and New Zealand, while A. dieffenbachii is only found in
New Zealand. Some anguillid leptocephali were collected south of
the Solomon Islands and provided preliminary evidence that the
spawning area of A. australis is in the South Equatorial Current
(Aoyama et al., 1999; Kuroki et al., 2008). Data from tracked eels
and circulation models suggest that both species spawn in slightly
overlapping areas between New Caledonia and Fiji (Jellyman &
Bowen, 2009; Jellyman & Tsukamoto, 2010). Further, genetically
identified larvae of A . australis (16– 46 days) were collected south
of the Solomon Islands but also 1,600 km to the east which, when
taken together with the age of the larvae, suggests that the spawn-
ing area is near the Vanuatu Archipelago (Kuroki et al., 2020).
2.3 | Description of the data
2.3.1 | Geomagnetic data
To test the magnetic imprinting hypothesis, we plotted and mapped
the total intensity of the geomagnetic field (F) and the inclination
of its lines (I), in the distribution areas of the eel species described
FIGURE 4 Reconstructed migrations of tagged Atlantic eels (triangles: Anguilla rostrata, Beguer- Pon et al., 2015; Beguer- Pon et al., 2017;
circles: A. anguilla, Righton et al., 2016). Paths correspond to the two eels that were tracked for the longest distance. Open circles/triangles
represent geolocation estimates or terminal positions— when the tag came off prematurely— of other tagged eels from Righton et al. (2016)
and Beguer- Pon et al. (2017). Isolines represent geomagnetic total intensities (dark grey, contours every 1,000 nT) and inclination (light grey,
contours every 2°) calculated for the year 2014. Growth (source = IUCN) and spawning areas are represented in green and orange boxes for
A. rostrata and A. anguilla respectively
DURIF et al.
above. All calculations were made using the International and
Definite Geomagnetic Reference Fields (IGRF, DGRF, Thebault
et al., 2015). IGRF models are models of the geomagnetic main field,
modelling sources inside the earth without taking into account ex-
ternal sources or static crustal anomalies. Values were calculated for
∆long = 1° and ∆lat = 0.5°. Magnetic field values were interpolated
usin g the kr iging metho d to dr aw is olines of equ al intensi tie s/i nclina-
tions. Contour maps were created using Manifold System 8.0.
2.3.2 | Migration routes and spawning areas of eels
The spatial data for the distribution of A. anguilla, A. rostrata and
A. japonica were obtained from the IUCN website. The distribu-
tion areas for A. australis and A. dieffenbachii, were obtained from
FishBase (Froese & Pauly, 2017). Locations of spawning areas and
migratory routes were obtained from the literature (Beguer- Pon
et al., 2015, 2017; Higuchi et al., 2021; Kuroki et al., 2020; Miller
et al., 2015; Miller & Tsukamoto, 2017; Righton et al., 2016; Shinod a
et al., 2011; Takeuchi et al., 2021). Data from Pop- up Satellite Tag
(PSAT) tracked A. anguilla silver eels on their way to the spawn-
ing area were provided by David Righton on behalf of the authors
(Righton et al., 2020). The larval drift of A. anguilla and A. rostrata
were described through larval collections made during surveys and
were downloaded from the International Council of the Exploration
of the Sea (ICES) Eggs and Larvae database. Larval collection loca-
tions of A. japonica were redrawn from Shinoda et al. (2011).
3 | RESULTS
3.1 | Geomagnetic gradients between growth and
The spawning areas of A. japonica, A. rostrata and A. anguilla are
located south of their growth area while A. australis and A. dief fen-
bachii spawn nor th of their grow th area (Figures 1– 3). Whi le the geo-
graphical configurations between eels from both hemispheres are
opposite, the gradients of the geomagnetic parameters are similar:
The magnetic intensity values (F) and inclination (I) in the growth
areas of the five species examined are always similar or higher than
in the spawning areas with little (ΔF < 10 000 nT; ΔI < 10⁰) or no
overlap (Table 1, Figures 5– 6).
In the case of Atlantic eels, larvae drifting with the Gulf Stream
along the North American coast experience a steep gradient of
increasing F and/or I (Figure 1). Further drifting towards the east
results in movements roughly parallel to the F and I isolines, de-
pend ing on the ir fi nal dest inati on. The ro utes of adul t silve r eel s, as
known from tracked individuals, retrace these magnetic gradients
in the op pos ite dire ction. Th at is , tracke d eels followed a steep gr a-
dient of decreasing F and/or I almost perpendicular to the isolines
(Figure 4). Tracks of both species were parallel to each other, keep-
ing a heading of approximately 200⁰ for A . anguilla and 190⁰ for
A. rostrata. A. anguilla changed its course at F = 41 000 nT, I = 49⁰
and the last detections were at isolines F = 43 000 nT, I = 54⁰ for
both species. Following either one of these “target isolines” by
maintaining a compass heading of approximately 260⁰ would lead
the adult eels to the spawning area.
The situation for A. australis and A. dieffenbachii in the
southern hemisphere is comparable to that of A. rostrata and
A. anguilla regarding both magnetic components and oceanic
circulation. Larvae drifting with the South Equatorial Current
and East Australian Current experience gradients of increasing
F and/or I at the beginning of the drift period which level off as
larvae drift east to reach New Zealand in the same manner as in
the Atlantic Ocean for A. anguilla (Figures 1– 2). Migrating adults
that swim towards decreasing F and/or I until target isolines
F = 43 0 00 nT, I = 40⁰ (for A. australis) and F = 46 00 0 nT, I = 46⁰
(for A. dieffenbachii), and follow these isolines, would arrive at
their spawning area.
The configuration is slightly different for A. japonica as F and I
isolines run perpendicular to one another in the spawning area.
However, larvae drifting with the North Equatorial Current (NEC)
and Kuroshio current still experience increasing F and I (Figure 3).
The migratory routes of adult eels, as they are known from PSAT
studies, also follow the reverse gradient moving towards lower F
and I (Figure 3). Their trajectories were slightly deviated towards the
south east. Tags were released before eels reached the spawning
area (or the spawning area isolines), but if eels had kept these head-
ings they would have arrived in the spawning area by shifting their
orientation by approximately 90⁰ to the right once they had reached
the target isolines (Figure 3).
TABLE 1 Characteristics of the distribution of magnetic total intensity (F) and inclination (I) values at the spawning areas of five species
of anguillid eels (Anguilla spp.). Values were calculated for the year 2014
I (⁰) (min– max)
F (nT) (min– max)
OverlapGrowth area Spawning Growth area Spawning
A. anguilla 4 6 – 7 7 4 2 – 5 6 10 39,000– 53,000 3 7 , 8 4 7 – 4 4 , 9 4 9 5,949
A. rostrata 4 6 – 7 4 4 6 – 5 6 10 37,000– 53,000 3 8 , 9 7 1 – 4 4 , 8 4 1 9,758
A. japonica 21– 5 5 3– 1 6 041,000– 48,000 3 6 , 5 1 3 – 3 8 , 0 0 1 0
A. australis 48– 72 −29 to −44 049,000– 61,000 3 9 , 1 2 0 – 4 5 , 7 7 3 0
A. dieffenbachii 60 – 70 −42 to −50 053,000– 59,000 43,772– 47,790 0
DURIF et a l.
For all species, the spawning areas are located at the same
magnetic isoline as the southern (northern in the southern hemi-
sphere) limits of the species distribution (Figures 1– 3). For ex-
ample, A. anguilla occurrence extends down to Morocco which
has the same magnetic intensity/inclination as the south- eastern
limit of the spawning area (Figure 1). For the A. rostrata, the mag-
netic isolines running through the spawning area, end up in the
Dominican Republic, which roughly corresponds to the southern
limit of A. rostrata distribution— at least to a limit below which
almost no larvae have been collected. The configurations of the
Gulf of Mexico and of the Mediterranean Sea are analogous:
although they are at different latitudes, they display similar
magnetic values. The F and I isolines at the Strait of Gibraltar
correspond exactly to the lower distribution limit of A. rostrata
in Cuba (F = 41 000 nT and I = 49⁰). Eels hatching in the most
south eastern corner of the spawning area would also experience
increasing F and I while drif ting towards either the Gulf of Mexico
or the Mediterranean.
3.2 | Secular variation
When considering a mean age at silvering of 20 years and a hatch-
ing date in 1900 (Atlantic eels), ΔF in the Sargasso Sea is <1,000 nT,
ΔI < 1.3⁰ (Figure 7). Between 1900 and 1920, this corresponds to a
spatial displacement of the geomagnetic features of the spawning
site of about 200– 500 km (when using F) and about 130 km (when
using I). For A. japonica, with a mean age at silvering of 10 years, ΔF
in the North Pacific is <100 nT and ΔI < 0.3⁰ which corresponds to
maximum displacements of 20– 50 km and 30 km respectively using
F and I.
4 | DISCUSSION
4.1 | A general mechanism for navigation of
migrating temperate anguillid eels
The migratory routes of five species of anguillid eels (A. anguilla,
A. rostrata, A. japonica, A. australis and A. dieffenbachii) are consistent
with the use of the geomagnetic field as a navigational cue to reach
their spawning area. The mechanism that we propose is possible
using only one component, either magnetic intensity (F) or inclina-
tion (I). Although, the use of I is less likely for reasons that are dis-
cussed later, we cannot completely exclude it until we obtain further
evidence of the actual migratory route of silver eels.
The general long- distance navigation mechanism for anguillid
eels can be described in five steps, for which we provide additional
support below. No animal is believed to rely solely on geomagnetic
cues for orientation (Clites & Pierce, 2017; Mouritsen, 2018) and our
FIGURE 5 Total magnetic intensities
(F, nT) modelled in growth areas and
spawning areas of five different species
of anguillid eels. In the Northern
hemisphere (top figures): Anguilla
anguilla, A. japonica and A. rostrata. In the
Southern hemisphere: A. australis and
DURIF et al.
FIGURE 6 Inclination angles (I°)
modelled in growth areas and spawning
sites of five different species of anguillid
eels. In the Northern hemisphere (top
figures): Anguilla anguilla, Anguilla
japonica and A. rostrata. In the
Southern hemisphere: A. australis and
FIGURE 7 Differences in magnetic parameters (total intensity and inclination) that a silver eel would experience upon return to the
spawning area where it hatched according to its age. Values represent the difference in total magnetic intensity (F) and inclination (I) at the
spawning area between of a hypothetical eel hatching in 1900 and spawning at different ages between 5 and 80 years old (age at silvering).
ΔF = Fhatch − Fspawn and each triangle the difference ΔI = Ihatch − Ispawn. Values were calculated at 63°W, 25°N (left panel, European (Anguilla
anguilla) and American eel (A. rostrata) spawning area) and at 140°E, 12°N (right panel, Japanese eel (A . japonica) spawning area)
DURIF et a l.
model, although it relies mainly on magnetoreception, also includes
physiological cues which are discussed below. The proposed mecha-
nism is conceptualized in Figure 8 and is described as follows:
1. Larvae hatch and imprint the local intensity or inclination (Fhatch
2. Larvae drift towards their growth area and register the F (or I)
gradient that they experience along the way until they reach their
3. Years later, at the time of the spawning migration, adults follow
the reverse magnetic gradient that they have imprinted as juve-
niles, which, as far as the species examined are concerned, cor-
responds to decreasing F (or I).
4. Adults reach the target isoline, Fhatch (or Ihatch) and keep a compass
heading to stay on the target isoline.
5. As the entire eel spawning population congregates towards the
target isoline, individuals become fully sexually mature and are
ready for spawning. The timing of sexual maturation likely deter-
mines the geographic location along the longitudinal axis which
may vary slightly from year to year.
4.2 | Migratory steps 1 and 2: Imprinting and the
magnetic map hypothesis
Silver (adult) eels take different oceanic/geographic routes than the
ones taken as larvae, thus they can be considered as a first- time
migrant. The only way for a first time- migrant to reach its target
is to inherit the information (Mouritsen, 2018). In the case of eels,
pre- programmed navigation seems unlikely given secular variation.
We show that the “magnetic routes” of larvae and adults are alike
and therefore that adult eels have had the opportunity to learn or
imprint the magnetic information necessary for the return journey.
FIGURE 8 General mechanism for the navigation of temperate anguillid eels (Anguilla sp.) using the geomagnetic field (F: total intensity,
I: inclination). Step 1: The target isoline (either F or I) is imprinted at a very early larval stage; step 2: Leptocephalus larvae imprint the F or
I gradient during their larval drift towards the continent; step 3: Adult eels migrate along the reversed F or I gradient; step 4: Adult eels
reach the target imprinted isoline and orient according to a compass heading to remain on the isoline; step 5: Physiological (end of sexual
maturation) and olfactory cues (coming from conspecifics) provide the stop signal. Eels congregate and spawn. Each quadrant repeats the 5
steps in the four possible geographical configurations between growth and spawning areas. Light dashed arrows represent the leptocephalus
drift towards the continent. Darker arrows depict the reproductive migration
DURIF et al.
These geomagnetic patterns are consistent between species and are
also consistent with the magnetic imprinting hypothesis (Figures 1–
6). Magnetic total intensity (F) and inclination (I) between growth
and spawning areas are almost identical between all five species
examined (A. anguilla, A. rostrata, A. japonica, A. australis and A. di-
effenbachii). Drifting larvae always experience increasing magnetic
inclination (I) and total intensity (F). The return routes of adults in
the open ocean, as far as they are known, correspond to the same
gradients but in the opposite direction. By imprinting either F or I
target isolines (at hatching), as well as the steepness of the gradients
experienced as larvae (during the drift), eels can home back to the
spawning area by retracing these magnetic patterns later as adults.
The range of the imprinted magnetic values (either F or I) may vary
depending on the extent of the larval dispersal. For example, a larva
drifting between the Sargasso Sea and the Mediterranean or to the
Gulf of Mexico will experience a smaller range of magnetic values
compared to larvae recruiting to Norway or Canada. Their imprinting
experience may define the range of variation of their magnetosensory
system for later use during the spawning migration. Such a calibra-
tion system was observed in the pigeon (Columba livia, Columbidae),
and the nematode (Caenorhabditis elegans, Rhabditidae), for which
the neuronal response became saturated when exposed to intensi-
ties larger than the geomagnetic field (Vidal- Gadea et al., 2015; Wu
& Dickman, 2012). Further indirect evidence for imprinting of geo-
magnetic components comes from several observations. Steelhead
trout (Oncorhynchus mykiss, Salmonidae) which, when raised under
an unnatural magnetic field failed to orient while those raised under
natural magnetic conditions did (Putman, Scanlan, et al., 2014).
Stocked eels that were translocated from France to Sweden as juve-
niles were not able to find their way out of the Baltic sea when they
reached the silver stage (Westin, 1990). Instead, they continued in
a south- westerly direction— as they would have oriented had they
been departing from France— and were found in the same area more
than 4 years later. Unusual behaviour of silver eels (stocked as juve-
niles) was also observed in Estonia, whereby 21% returned to their
river after an attempted migration (Tambets et al., 2021). One fish
was recaptured in Finland and only 13% were detected exiting the
Baltic. Similarly, translocated brown trout (Salmo trutta, Salmonidae)
lost their ability to home to their native river when deprived of en-
vironmental cues during their transport out to the sea (Jonsson &
4.3 | Migratory steps 3 and 4: «Aiming off»
As silver eels leave continental waters and reach the open ocean,
cues such as salinity or odour plumes from rivers, disappear. Beyond
continental shelves, migrating eels seem to follow decreasing mag-
netic intensities (F) and/or inclination (I) until they have reached the
isolines that correspond to their spawning area. This is supported
by data from tagged A . anguilla which were tracked for at least half
of the spawning migration (Righton et al., 2016). Interestingly, eels
did not take the shortest way back to the Sargasso Sea (Aarestrup
et al., 2009; Righton et al., 2016), but instead first headed south
along a gradient of magnetic intensities (or inclinations) that is simi-
lar to the one experienced at the beginning of their larval drift, along
the north American coast in the Gulf Stream (Figures 1 and 4). The
eel with the longest track changed its course around the magnetic
isoline (Figure 4, F = 41 00 0 nT, I = 49⁰) that runs through the spawn-
ing area in the Sargasso Sea. Eels released in the Mediterranean, and
thus already at (F = 41 000 nT, I = 49⁰), followed a western heading
towards the Azores (Amilhat et al., 2016). The tracks of more than
80 eels were reconstructed (Figure 4), and although many were pre-
dated upon, all trajectories converged on the Azores region (Righton
et al., 2016). Once there, eels would presumably maintain a western
heading towards the spawning area. The tracks of tagged A. japon-
ica were also consistent with our model (Higuchi et al., 2021). Eels
moved along decreasing F and I gradients at least until their tags
were released. Eels did not swim directly to the spawning area but
swam southeast of the spawning area. The authors hypothesized
that eels would later move southwest with the flow of Kuroshio re-
circulation or the subtropical gyre. Thus, “aiming off” seems to occur
in both species. This navigation technique involves aiming away from
the destination but instead heading towards a “line feature” such as
a stream (here a magnetic isoline) some distance to the left or to
the right of the target. Steps 3 and 4 of our model, as well as ob-
servations of tagged eels, are consistent with this efficient strategy,
which has at least two advantages: (1) It is the most efficient strat-
egy to find conspecifics. Rather than heading straight for a target,
beginning at one end and keeping a constant heading will increase
the chance of meeting conspecifics along the way. A. anguilla com-
ing from— for example, Norway— have a better chance of meeting
eels from Morocco along a narrow latitudinal band (F = 41 000 nT,
I = 49⁰) than at a target point. This is consistent with the panmictic
nature of this species. (2) This navigational strategy also allows for
the use of other orientation cues such as olfaction (see the discus-
sion of olfactory cues). Finally, the geomagnetic patterns along the
migratory route are compatible with an “aiming off” strategy (de-
scending F and I gradients then following the axis of the isoline) and
this is demonstrated in the trajectory of tagged eels.
Eels likely use compass orientation as they travel towards de-
creasing F and I, while periodically taking “measurements” until
they reach the target isoline where they switch compass heading.
Compass sense has been reported in the continental life stages of
the A. anguilla (Cresci et al., 2017; Durif et al., 2013). Such a mecha-
nism, which consists of a sequence of compass headings changing at
specific magnetic field values, is well documented in birds (Åkesson
& Helm, 2020; Kiepenheuer, 1984). For example, under laboratory
conditions pied flycatchers (Ficedula hypoleuca, Muscicapidae) shift
compass orientation when exposed to changes in magnetic field in-
tensity corresponding to those encountered during their natural mi-
gration (Beck & Wiltschko, 1982). During the experiments, the shifts
in heading occurred at the same time as for conspecifics during their
DURIF et a l.
4.4 | Migratory step 5: The end of the journey
Our model does not require that eels possess navigational abilities
along the longitudinal axis, but instead relies on a strategy that will
allow for eels from all of the distribution area to congregate. The
spawning area as we know it, at least for the Atlantic eels, repre-
sents a very large area. Research cruises carried out in 2014 col-
lected larvae ≤20 days old across a longitudinal range of about
2000 km (Miller et al., 2019). Furthermore, at the time of spawning,
hundreds of millions— in some years possibly billions— of eels migrate
from Europe every year (ICES, 2020). Given this, a precise navigation
system to a specific target is not needed. Rather a common mecha-
nism to follow the same route and meet along this route would be
required. As for flycatchers (see above discussion), eels may rely on
an endogenous time program coupled with magnetic parameters of
specific locations throughout their migration and as they become
sexually mature. As in several other fish species, eels undergo ex-
treme morphological and physiological changes during the last steps
of their sexual maturation. Bodies of females become swollen (the
percentage of eggs relative to body mass can reach 50%), they un-
dergo osteoporosis and the energy stores in both sexes are depleted
(Durif et al., 2006; Fontaine et al., 1964; Sbaihi et al., 2009). In other
words, at full sexual maturation, eels are inefficient swimmers that
are physically unable to continue swimming long distances. In fact,
they die soon after ovulation/spermiation (Chow et al., 2009).
An additional cue that would reinforce orientation throughout
the reproductive migration is odour. Odour plumes, such as pher-
omones left by conspecifics, may provide a trail guiding eels, espe-
cially during the last part of the journey up to the Azores current.
In Salmonids, eggs and ovarian fluids produce odours that guide
adults to the breeding sites (Dittman & Quinn, 2020). In eels, ol-
faction is important throughout their life cycle. Glass eels are at-
tracted by the smell of their conspecifics (Cresci, 2020; McCleave
& Jellyman, 2002; Schmucker et al., 2016). Silver eels use olfaction
during their estuarine migration and olfactory cues trigger migra-
tion into rivers (Barbin et al., 1998; Durif et al., 2008). As progres-
sively more and more mature individuals pass along the same route,
they will leave olfactory signals. Tracked eels exhibited diel vertical
migrations (Aarestrup et al., 2009); this would be an effective way
to spread the olfactory tracks through the water column. In the
laboratory, sexually mature eels (artificially induced) showed higher
gene expression of receptors related to olfaction, which suggests
a role of olfaction in reproduction and possibly also in orientation
(Churcher et al., 2015).
4.5 | Use of inclination (I) and/or total intensity (F)
in the navigation of eels
We examined the patterns of I and F since they are both correlated
with latitude and are measurable components of the magnetic field.
In most configurations, the gradients were parallel and, therefore,
whichever parameter, F or I, is used by eels does not change the
overall mechanism. Our analysis of the potential effect of secular
variation suggests that I is the best candidate for magnetic naviga-
tion since maximum potential displacement (ΔImax = 130 km) was
lower than for F (ΔFmax = 500 km). However, comparing patterns of
I and F between species favoured F. Indeed, we found that F pat-
terns were very similar across species, while I patterns were differ-
ent near the A. japonica spawning area since the isolines of F and I
run perpendicular to each other (Figure 3). At present, it is not pos-
sible to determine which component is more likely to be used— or
if both are used— since we have very little knowledge on the routes
of migrating adults of A. japonica. If adult A. japonica were to adopt
the same strategy as the other species, that is, following a decreas-
ing gradient and then following an isoline, then patterns of F would
match. Silver eels would follow a south- easterly heading until iso-
line ~F = 36 000 nT, after which they would keep a constant head-
ing in a south- westerly direction until they reached the spawning
area (Figure 3).
From a physics point of view, one fundamental difference between
magnetic intensity and inclination is that F is a scalar value while I is
an angle. Thus, measuring variations in I is a much more complex feat
for an eel than measuring total intensity (F). As one approaches the
equator (where I is equal to zero), the signal- to- noise ratio will deteri-
orate much more for I than for F. Another advantage of F is that while
it also decreases towards the equator, it will not be zero at the equa-
tor and (for Thebault et al., 2015) will have values between 30,000
and 40,000 nT (while it is around 55,000 nT at the poles), depending
on the location along the equator. Further, while measurement of F
(scalar) is independent of one's position in space, I being an angle is
measured relative to the horizontal plane or to a gravitational refer-
ence system which makes it a challenge underwater. However, logger-
head sea turtles (Caretta, Cheloniidae) and eastern red- spotted newts
(Notophthalmus viridescens, Salamandridae) seem to accomplish this as
they can detect differences in I as small as 2– 3⁰ (Fischer et al., 2001;
Lohmann & Lohmann, 1994). Overall, our analyses and the physics,
appear to make F more likely to be used than I.
4.6 | Geomagnetic secular variations
For animals to use a magnetic map requires that they are highly
sensitive to gradients, and that they have a system/mechanism to
handle static magnetic anomalies (due to the magnetized sea floor),
short term variations (e.g. magnetic daily variations) and secular vari-
ation. Historically, the magnetic poles have been drifting between 10
and 20 km annually, but an acceleration (about 50 km/year) began
around 1990 in the northern hemisphere (Thebault et al., 2015).
Adaptations for maintaining migratory behaviour must be capa-
ble of handling fluctuations on these time- scales and this is also
an argument against a genetically programmed navigational target
(Courtillot et al., 1997).
There are several ways an organism can deal with secular variation.
Long- term temporal measurements might be factored out by regular
measurements of the magnetic field at one specific location (Freake
DURIF et al.
et al., 2006). In other words, an eel may “register” the changes over
its life cycle in its current location and adjust the target coordinates
that will be used during the spawning migration. However, this seems
unlikely given the long migration distances and the fact that the mag-
nitude of changes in the field varies across the Earth's surface.
Another way to mitigate the displacement due to secular vari-
ation is to imprint the target destination at an early stage of the
life cycle rather than transmitting it to offspring (genetically pro-
grammed) (Lohmann et al., 2008; Putman, Scanlan, et al., 2014;
Putman, Scanlan, et al., 2014). This is supported by our findings
(see ‘Imprinting and the magnetic map hypothesis: steps 1 and 2’).
Yet, in such long- lived species as anguillid eels, there can still be
an effect of secular variation over the course of an eel's lifecycle.
Accounting for the age of silver A. anguilla, we calculated that the
maximum geographic displacement that would result from secular
variation in the Atlantic would be approximately 300 km if magne-
toreception was based on F and 100 km based on I. Displacements
for A . japonica silver individuals would be around 30 km. These are
very rough estimates which also depend on the years chosen, but
they give a reasonable order of magnitude which could be overcome
through olfactory cues given the extent of the spawning migration
(hundreds of millions of eels per year, ICES WGEEL (2020), esti-
mates for A. anguilla). Moreover, waves of migrating silver eels are
synchronized according to latitude: eels in the north leave earlier
than eels in the south as they have more distance to cover. As ex-
plained previously, age at migration decreases with latitude (Durif
et al., 2009; Jessop, 2010; Vøllestad, 1992). Females and/or males
from the southern part of the distribution may migrate after only
2 years, thus reducing the offset in the imprinted magnetic compo-
nents (ΔI and ΔF) to a negligible level, with ΔI ≈ 0.2⁰ and ΔF ≈ 50 nT
(Figure 7). This corresponds to a displacement of 10 to a maximum
of 20 km which can easily be resolved using olfactory cues given the
total annual number of spawners. Eels from the southern part of the
distribution probably arrive first and will provide essential olfactory
cues in the form of an odour plume conveyed by the Azores current
(which flows from the west) that will guide the rest of the spawners.
4.7 | Perspectives
Anguillid eels are fascinating in the sense that they are present
in both hemispheres and that different species share very simi-
lar biological characteristics and life- histories (catadromy, long-
distance migrations and long lifecycle). It seems reasonable that
temperate eels would use the same navigational strategy to home
to their spawning area having evolved from a common ancestor
(Inoue et al., 2010). Indeed, the mechanisms described in this
study for finding the spawning area— based on imprinting geomag-
netic gradients, retracing them later as adults, “aiming off” using
the imprinted target isoline and compass orientation— fit with the
geomagnetic pat terns present in the distribution area for all of the
species examined and the migratory routes of these eels as they
are currently known.
The model that we have described only applies to the oceanic
part of their migration and does not address the coastal part of the
journey where other sensory cues are available from continental wa-
ters (salinity gradients and odour plumes from rivers). While very
early life stages of eels probably do not orient actively, older larvae
that have reached the continental shelf and which ultimately meta-
morphose into glass eels, have become stronger and are likely capa-
ble of orientation and sensing other cues which would guide them
towards freshwater habitats (Chang et al., 2018; Cresci et al., 2021;
Rypina et al., 2014).
If our hypothesis is correct and eels need to imprint their migra-
tory route, then current stocking programs— in which juvenile eels
are translocated to eel- depleted areas— are unlikely to contribute
to the recovery of the population. Fishing for glass eels is currently
allowed in many EU countries under the condition that 50% of the
catch is dedicated to stocking. Glass eels are usually displaced from
southern Europe to the Baltic Sea. When this is done, translocated
glass eels are not exposed to the magnetic cues needed for suc-
cessful navigation back to the spawning area. In recognition of this
weakness in translocation programmes, reintroduction of brown
trout now includes towing juveniles in the sea to allow them to
learn environmental cues during their seaward journey. This in-
creases their chances of returning to their home river (Jonsson &
Jonsson, 2021). This is something that should also be considered
for eels and other species with analogous life histories that include
long- distance migrations.
Further knowledge on the migratory routes of adults, as well
as the location of spawning areas, will allow our hypotheses to be
tested more comprehensively. Until then, magnetic navigational
cue s, as de scribed here, could be incorporated into biophysical mod-
els to help guide future expeditions in search of eel spawning areas
and provide more knowledge on the spawning migration of anguillid
eels in a manner analogous to what has been applied to assess how a
lunar compass aids glass eel orientation (Cresci et al., 2021).
Finally, the migration orientation mechanism proposed here im-
plies that the location of the spawning area of A. anguilla is much
larger than had been thought and that it shifts as a result of secu-
lar variation. That may partly explain why it has proven difficult—
despite >100 years of effort— to locate it.
We thank David Righton for providing the tracking data. We also
thank the reviewers for their insightful comments which greatly im-
proved our manuscript.
CONFLICT OF INTEREST
The authors declare that they have no conflict of interest.
Caroline Durif: Conceptualization, Methodology, Investigation,
Visualization, Writing— Original draft, Funding acquisition. Hans
Hagen Stockhausen: Conceptualization, Investigation, Methodology,
Writing— Review and editing, Visualization. Anne Berit Skiftesvik:
DURIF et a l.
Conceptualization, Writing— Review and editing, Funding ac-
quisition. Alessandro Cresci: Conceptualization, Visualization,
Writing— Review and editing. Daniel Nyqvist: Conceptualization,
Writing— Review and editing. Howard Browman: Conceptualization,
Writing— Review and editing, Funding acquisition.
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in NMDC at http://doi.org/10.21335/ NMDC- 18702 39141, refer-
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How to cite this article: Durif, C. M. F., Stockhausen, H. H.,
Skiftesvik, A. B., Cresci, A., Nyqvist, D., & Browman, H. I.
(2021). A unifying hypothesis for the spawning migrations of
temperate anguillid eels. Fish and Fisheries, 00, 1– 18. ht t p s : //