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opeN
Received: 05 October 2015
Contrasting movement strategies
among juvenile albatrosses and
petrels
sophie de Grissac1,2, Luca Börger3, Audrey Guitteaud1 & Henri Weimerskirch1,2
accepted: 26 April 2016
Published: 18 May 2016
Animal movement is a fundamental eco-evolutionary process yet the behaviour of juvenile animals
is largely unknown for many species, especially for soaring seabirds which can range widely over
the oceans at low cost. We present an unprecedented dataset of 98 juvenile albatrosses and petrels
(nine species), tracked for the first three months after independence. There was a startling diversity
within and among species in the type and scale of post-natal movement strategies, ranging from
area-restricted to nomadic patterns. spatial scales were clustered in three groups that ranged from
<3000 km to >6000 km from the natal nest. In seven of the nine species, the orientation of flight
paths and other movement statistics showed strong similarities between juveniles and adults,
providing evidence for innate orientation abilities. our results have implications for understanding the
development of foraging behaviour in naïve individuals and the evolution of life history traits such as
survival, lifespan and breeding strategy.
Juvenile and immature individuals play a key role in the dynamics of animal populations1, particularly in
long-lived species for which they can represent up to 50% of the total population2. It is therefore essential to
account for the specific traits and strategy of juveniles when modelling the fate of populations3. However, for most
species, the behaviour and fate of juveniles remain almost unknown. In animals with parental care, the critical
stage for juveniles is when they start to move and forage independently. At this stage, juveniles generally suffer
high mortality, which is likely a result of low foraging efficiency or non-optimal morphology compared to that
of adults4,5. How such naïve individuals navigate in their environment, especially for large scale dispersive movements such as migration or exploration, has been identified as a priority for research6.
The concept of dispersal, or natal dispersal, is often used to describe the movement of a juvenile leaving its
natal grounds to breed elsewhere7. This therefore excludes the post-fledging movements of highly philopatric species, which return to breed at their natal colonies. However, as pointed out in recent studies8, dispersal includes
the “movement of new fledglings in all directions with no inherent directional preferences”. These movements
may, in time, lead to ‘true’ dispersal, in the most commonly used sense7, or to the birds’ return to their colony of
origin.
Substantial individual variability has been documented in the dispersal behaviour of terrestrial animals7,9.
Individuals move in heterogeneous environments, making their displacement landscape-dependant. Indeed,
non-flying terrestrial animals are severely constrained by movement costs related to energy landscapes10,11. While
birds are far less constrained, terrestrial birds still generally follow topographic features and landmasses during
their migration or dispersal, and use specific sites for stop-overs8.The case of seabirds is very different, as adults
have capacities for large scale movements over open, comparatively featureless oceans12,13. This is particularly
true for procellariiform species (albatrosses and petrels), which can undertake extremely long migratory movements14,15. When juvenile petrels and albatrosses leave their nests for the first time, they have ‘the world as their
oyster’, in that they can potentially fly at low metabolic costs, using winds to move in a vast, apparently homogenous, environment. These naive birds face no topographic constraints on where and when to move. Whilst the
oceanic realm is certainly not a featureless environment for seabirds that are known to be sensitive to oceanographic features such as bathymetry, currents, wind zonation, eddies, or odours such as dimethyl sulphide16, the
1
Centre d’Etudes Biologiques de Chizé, UMR 7372 CNRS & Université de La Rochelle, Villiers en Bois, France. 2UMR
9220 CNRS IRD ENTROPIE, Université de la Réunion, Saint Denis, France. 3Department of Biosciences, College of
Science, University of Swansea, Swansea, UK. Correspondence and requests for materials should be addressed to
S.D.G. (email: sophie.degrissac@cebc.cnrs.fr)
Scientific RepoRts | 6:26103 | DOI: 10.1038/srep26103
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Juveniles
Taxa
Species Mass
code
(kg) Colony
N
Amsterdam albatross
Diomedea amsterdamensis
AMAL
8.0
A
11
123 ± 91
(21–280)
8
329 ± 48
(252–369)
Wandering albatross
Diomedea exulans
WAAL
10.9
C, K
23
159 ± 89
26–379)
10
222.3 ± 13
(330–366)
Yellow-nosed albatrosss
Thalassarche carteri
YNAL
2.6
A
4
48 ± 40
(3.0–94)
10
320 ± 31.6
(198–297)
Black-browed albatross
Thalassarche melanophris
BBAL
3
K
12
69 ± 30
(15–96)
10
373 ± 26
(165–249)
Sooty albatross
Phoebetria fusca
SOAL
2.8
A, C
13
107 ± 79
(2–254)
10
310 ± 52
(174–375)
Light mantled sooty
albatross
Phoebetria palpebrata
LMSA
3.3
C, K
7
90 ± 60
(8–186)
10
136 ± 28
(273–366)
Northern giant petrel
Macronectes halli
NOGP
5
C, K
10
118 ± 61
(44–227)
10
346 ± 15
(351–387)
Southern giant petrel
Macronectes giganteus
SOGP
5
C
5
96 ± 65
(43–190)
10
322 ± 8
(120–144)
White-chinned petrel
Procellaria aequinoctialis
WCPE
1.2
C, K
13
48 ± 42
(15–109)
10
271 ± 14
(303–336)
98
96 ± 37
88
292 ± 73
Giant petrels
Total
N
Tracking
time
Scientific name
Mollymawks
Petrel
Adults
Species
Great albatrosses
Sooty albatrosses
Tracking
time
Table 1. Dataset information. Abbreviation used, mass, colony of origin and number of birds equipped with
tracking duration (mean ± standard deviation (minimum–maximum)) by species, for juveniles and adults.
Masses are only indicative for species and obtained from literature73. A, C and K are respectively Amsterdam,
Crozet and Kerguelen Islands.
spatial scales are larger than in terrestrial habitats by many orders of magnitude17. This adds further interest to the
question of how these animals forage in the marine environment.
In most seabird species, juveniles leave their natal grounds independently from their parents, and thus have
to explore the environment and learn to forage entirely on their own. Existing studies on land birds have shown
that juveniles may follow an innate navigation programme to some extent, while acquiring cues to improve their
foraging proficiency14. The innate parts of juvenile movements can be similar to the movements of adults for some
species18, while for others they may differ19,20 with respect to the timing21,22, track characteristics (e.g. sinuosity23)
or route choice (e.g. less productive areas4,22,24). These differences in terrestrial birds have generally been explained
by the lack of experience in juveniles25 leading to navigation errors. Though a lower competitiveness on foraging
grounds in relation to adults26 may also have selected for endogenous post-fledging dispersal programmes that
favour intra-specific spatial segregation. However, very limited data exist to allow a general understanding of the
dispersal movements of juvenile seabirds within and across species. Without a strict endogenous programme and
highly constraining landscape features, we may expect juvenile seabirds’ movements to vary considerably within
and between species.
Here we present the first cross-species study of post-fledging movements in juvenile seabirds, comparing the
large-scale movement strategies of juveniles from nine closely related procellariiform species during their first
months at sea. The nine species, i.e. two species of great albatrosses, two species of mollymawk albatrosses, two
species of sooty albatrosses, two species of giant petrels and one species of petrel (Table 1), constitute an ideal
study system as they breed in the central Indian Ocean (Supplementary Fig. 1) and face similar environmental
conditions when they leave their natal breeding sites. Adults of the nine species exhibit contrasting movement
patterns during the inter-breeding period, i.e. when they are not central place foragers. They either show a typical
migratory behaviour, i.e. moving regularly from breeding grounds to winter quarters and back27, ranging widely in
the Southern Ocean with no specific destination, or remain near the breeding grounds throughout the year20,28–30.
These species also show contrasting life history strategies, with great albatrosses and sooty albatrosses being
longer lived than the other species, and juvenile survival being very different between species31–33. By comparing
movement types and characteristics, we can test whether juveniles of each species follow a programmed route,
whether their routes or destinations follow those of the adults or whether they differ in timing, directionality, sinuosity or targeted habitat type8,23,34. For example, rapid movement away from the natal colony or use of different
areas than those used by adults may reduce intraspecific competition since it is generally assumed that competition between immatures and older birds leads to spatial segregation between age-classes4,19,26. Such competition
may have consequences on individual fitness and population dynamics4,35.
The specific questions we want to address in this study are (1) Do closely related seabird species differ in their
movements during the first months of independence at sea? (2) Do naïve juvenile birds have similar movement
patterns to those of their parents? (3) Do the movement trajectories provide evidence of an innate navigation
programme, implying unique fixed departure directions or direct orientation towards specific foraging areas
instead of random movements? We discuss the implication that differences in movement behaviour may have on
the evolution of life history components such as juvenile survival.
Scientific RepoRts | 6:26103 | DOI: 10.1038/srep26103
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NSD models
Taxa
Giant petrels
Mollymawks
Petrels
Sooty albatrosses
Great albatrosses
Nomad
Half
migration
Migration
Range at 3
months
Movement
Scale
0
66%
33%
0
17350 ± 2565
large
0
100%
0
0
23859 ± 2299
large
YNAL
0
0
100%
0
4869
medium
Species
Home-range
NOGP
SOGP
BBAL
0
14%
86%
0
5971 ± 1648
medium
WCPE
0
0
100%
0
4117 ± 510
medium
LMSA
0
0
50%
50%
2221 ± 1421
small
SOAL
57%
43%
0
0
1730 ± 702
small
AMAL
0
43%
57%
0
2943 ± 1525
small
WAAL
0
33%
66%
0
4233 ± 2285
medium
Table 2. Prevalence of different movement modes for juveniles of nine procellariiform species identified
using the Net Squared Displacement (NSD) modelling method and movement scale at 3 months.
Results
Comparison between juveniles. General movement patterns. The Net Squared Displacement (NSD)
method36 was used to model and identify typical large-scale movement types (Supplementary Methods 2-Fig. 1).
We observed that juveniles showed striking interspecific differences in displacement behaviour in the first three
months after leaving the natal colony. Movement types ranged from sedentary to nomadic patterns (Table 2,
Fig. 1), and included migratory-like movements and a specific pattern that we named “large-scale looping type”
(Fig. 1c). The majority of northern (67%) and southern (100%) giant petrels showed a typical nomadic-type
movement with large dispersal distances (range at three months >6000 km, Table 2), and an eastward trajectory, with all individuals circumnavigating Antarctica within the first three months after leaving the natal colony
(Table 2, Fig. 1a). Some individuals stopped for variable durations in specific areas before resuming their eastward movements and four individuals, for which the tracking time exceeded six months, completed a circumpolar movement and started a second one. In contrast, most juvenile mollymawks (100% of the yellow-nosed
albatrosses and 86% of the black-browed albatrosses) and white-chinned petrels (100%) showed migratory-type
movements fitted by the “half-migration” model. Specifically, the migratory–like movements of these species included a transit phase of 10–30 days with rapid directional movement, followed by a settling phase in a
restricted area. Since these movements lacked the return trip, typical of true complete migration, during the 3–6
month study period, we named the corresponding model ‘half-migration model’ (e.g.: Fig. 1b). These movements
were carried out over medium spatial scales (the range at three months was shorter than 6000 km but longer than
3000 km, Table 2, Fig. 1b). Juvenile sooty albatrosses and Amsterdam albatrosses showed more individual variability that included all displacement types on a small to medium spatial scale (range at three months <3000 km).
Overall, the displacement types of these three latter species were not characterized by any clear prevalent displacement strategy, with most individuals remaining within a limited range from the colony through looping
movements. We therefore grouped these individuals into a category named “large-scale looping type” (Fig. 1c).
Wandering albatrosses showed an even higher intraspecific variability with some individuals moving over a small
scale in the Indian Ocean and showing a looping behaviour (Fig. 1d: white dots), whereas others (60%, Table 2)
moved further toward the Australian coast and/or into the Pacific Ocean (Fig. 1d: black and grey dots), adopting
either half-migratory type movements or large-scale nomadic type movements. These differences in displacement
lead juveniles of the nine species to relocate to three broad geographic areas, with small-scale dispersers (most
sooty and great albatrosses) remaining in the central Indian Ocean, medium scale dispersers (mollymawk albatrosses, petrels and some wandering albatrosses) making some excursions out of the Indian Ocean, and large scale
dispersers (giant petrels and some wandering albatrosses) leaving the Indian Ocean, with some birds undertaking
entire circumpolar navigations.
Orientation at departure and further bearings. Departure flight directions taken by juveniles from their natal
colony (Fig. 2: black points) had two distinct patterns. 1: An oriented trajectory with very little inter-individual
variability in flight directions (within species, departure headings range was ≤π/4, indicating little variation in
direction, Rayleigh test of uniformity: all P < 0.01,). This was the case for nomadic (giant petrels) and migratory
type species (mollymawks and white-chinned petrel). These two groups of species also showed a high consistency
in orientation with time, since the directionality of their position with respect to the colony at month 2 and 3
(Fig. 2: grey and white points) was similar to the direction taken at departure (bearings range <π/4) with a small
shift toward east for white-chinned petrels. 2: A high variability in departure heading toward east, west and north
for the three species exhibiting large-scale looping movements, i.e. the two sooty albatrosses (heading toward
north, π > range < π/2, Rayleigh test: P > 0.1) and Amsterdam albatrosses (range >π, Rayleigh test: P = 0.73).
This group with non-oriented flights at departure showed no further consistency in orientation since positions
were similarly scattered after two and three months. Finally, most wandering albatrosses had a restricted departure direction (direction range = 1.8 rad, just over π/2) toward NE, but the directionality of positions were not
consistent beyond departure.
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Figure 1. Typical juvenile trajectory patterns (left) and corresponding NSD curves (right, red lines are best
NSD model fits) illustrated by (a) Northern giant petrel (nomadic type), (b) Black-browed albatross (halfmigration type), (c) Sooty albatross (large-scale looping type best fitted here by a home-range NSD model).
Panel (d) shows 3 different trajectory types of juvenile wandering albatross and NSD fits corresponding (red
line) with nomadic type movement (black dots, full red line), half-migratory type movement (grey dots,
dashed red line) and large-scale looping movement (white dots, dash-dot red line). White star and diamond are
respectively Crozet and Kerguelen colonies. Maps have been generated with R64 and the “ggplot2” library72 and
free-access coastline data (from naturalearthdata.com).
Sinuosity and daily distance travelled (DDT). First, the paths of nomadic-type species (giant petrels) were typified
by a lower sinuosity (S < 0.5) than other species (linear mixed model & post-hoc Tukey test: P < 0.05 when compared to all species except wandering albatross and yellow-nosed albatross, Fig. 3a & Supplementary Results 1).
They also had the highest DDT (354 ± 58.9 km (SD)) of all species when averaged over the 3 months (linear
mixed model & post-hoc Tukey test: P < 0.05 when compared to all species except light-mantled sooty albatross
(P = 0.054 when compared to northern giant petrel), Fig. 3b and Supplementary Results 2). The DDT varied
between individuals but showed no clear trend over time (linear mixed model & post-hoc Tukey test p-values in
Supplementary Table 2). Second, migratory-type species performed trajectories that directly (low sinuosity <0.5)
and rapidly (high DDT >240 km) took them from their natal colony to a restricted foraging area during the
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Figure 2. Orientations. Departure directions (black dots) and rhumb bearing of the position at 2 months (grey
dots) and 3 months (white) with respect to the departure point, i.e. the birth colony.
Figure 3. Sinuosity and daily distance travelled. (a) Average sinuosity of the trajectory during the first 15
days at sea of month 1 (black dots), month 2 (grey dots) and month 3 (white dots). (b) Average daily distance
travelled (DDT) ± one standard error (bars) during the 15 first days of months 1 (black), 2 (grey) and 3 (white).
first month (i.e. during the transit phase). Once the destination was reached (during the 1st (mollymawks) or 2nd
month (white-chinned petrel)) there was an increase in sinuosity (linear mixed model & post-hoc Tukey test:
P < 0.05 except for yellow-nosed albatross, Supplementary Table 2) and a decrease in DDT (linear mixed model
& post-hoc Tukey test: all P < 0.05, Supplementary Table 2). This phase corresponds to the settlement time, when
the NSD curve reaches the asymptote. The reason why white-chinned petrels settled later than mollymawks (i.e.
with transits lasting 30 to 40 days compared to 14 to 26 days in mollymawks) is that all individuals started heading north (Kerguelen colony) or north-east (Crozet colony) until they reached latitudes of 30°S (around the 9th
day), which corresponds to the latitude of Trade winds, i.e. easterly winds. Following this, individuals adopted a
westerly heading to reach their final destination off the coasts of South Africa. Finally, the group with large-scale
looping movements (sooty and Amsterdam albatrosses) had high orientation variability, medium sinuosity (close
to 0.5 or higher) and medium DDT (241 ± 72 km (SD)) right from the first month, with no significant trend over
the whole period (Fig. 3a, Supplementary Tables 2).
Distance to colony and habitats. During the first 15 days all species moved rapidly and directly away from the
natal colony (mean range at 15 days = 1323 ± 786 km (SD)). After one month, nomadic giant petrels had reached
a significantly longer range than the other species (linear mixed model and & post-hoc Tukey test: P < 0.05,
Supplementary Table 3) and tended to stay in oceanic waters (Bathymetry <−3000 m, Table 3 & Supplementary
Fig. 2). They encountered significantly cooler surface temperatures than other species (linear mixed model and &
post-hoc Tukey test: P < 0.05, Supplementary Fig. 2) mainly because of their passage into the Pacific Ocean. Some
northern giant petrels however, stopped for variable duration in neritic waters, for example in the productive
Chilean Patagonian shelf (where chlorophyll a values >3 mg.m3). Migratory-type species rapidly increased their
distance to the colony until they reached slope edges off Australia (mollymawks, mean bathymetry >−2000 m
for both species, waters significantly shallower than that of other species (linear mixed model and & post-hoc
Tukey test: P < 0.05, Table 3 & Supplementary Fig. 2) or oceanic waters along eastern South-African coasts in the
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Juveniles
Taxa
Giant petrels
Mollymawks
Petrels
Sooty albatrosses
Great albatrosses
Species
Movement
scale
Habitat
NOGP
large
SOGP
large
Adults
(%individuals)
Dispersion
distance
Variation at
asymptote
O
(70%)
836 ± 143
357 ± 65
N/O
O
(80%)
1291 ± 186
364 ± 110
N/O
Habitat
YNAL
medium
N
(100%)
5004 ± 476
488 ± 265
N
BBAL
medium
N
(81%)
3985 ± 328
291 ± 88
N
WCPE
medium
N/O
(57%/43%)
5415 ± 328
605 ± 174
N
LMSA
small
O
(100%)
3862 ± 438
1084 ± 241
O
SOAL
small
O
(90%)
4817 ± 1124
759 ± 430
O
AMAL
small
O
(89%)
3078 ± 966
712 ± 147
O
WAAL
medium
O/N
(77%/23%)
5456 ± 457
1018 ± 847
N/O
Table 3. Dispersion distances and habitats visited by juveniles and adults. All adults’ trajectories fitted
by the migratory type NSD model, the dispersion distance is the distance to colony of the migratory model
asymptote and the variation around the asymptote is calculated with the residuals of the model. Habitats are
oceanic (O) and neritic (N).
Figure 4. Latitudes. Mean latitude ± one standard error (bars) attained during the third month at sea by
juveniles (white circles) and by adults during inter-breeding season (black circles). Significant differences
between juveniles and adults are **P < 0.05 and ***P < 0.01 (Wilcoxon test).
Agulhas current area (white-chinned petrels, mean bathymetry = −3493 ± 391 m (SD), Table 3, Supplementary
Fig. 2). White-chinned petrels foraged at lower latitudes than other species (Fig. 4) and encountered warmer
surface temperatures than other species (Supplementary Fig. 2, significant difference only compared to giant
petrels, wandering, black-browed and light-mantled sooty albatross; linear mixed model and post-hoc Tukey
test: P < 0.05). The three looping species that remained within a 3000 km radius of their natal colony foraged
almost exclusively in deep oceanic areas (respectively 100, 90% and 89% of individuals of the two sooty species and Amsterdam albatrosses, Table 3; mean bathymetry = −3793 ± 178 m (SD), see Supplementary Fig. 2).
Amsterdam albatrosses encountered warmer waters at lower latitudes than others (Fig. 4, Supplementary Fig. 2).
Finally, wandering albatrosses showed a strong individual variability with respect to the distance from the colony
(from small to large dispersal range) and the habitat frequented, comprising both neritic (continental slopes or
oceanic features like ridges) and oceanic areas (Table 3, Supplementary Fig. 2).
With respect to chlorophyll a, although there was a tendency for some species, such as northern giant
petrels, black-browed, yellow-nosed and wandering albatrosses, to favour waters with higher chlorophyll a
(Supplementary Fig. 2), the differences were only significant between northern giant petrels and three species:
sooty albatrosses, Amsterdam albatrosses and white-chinned petrel (linear mixed model and & post-hoc Tukey
test: P < 0.05)
Comparison with non-breeding adults. When the breeding season ended, adult birds left the colony for
an extended period, during the winter time for most species, returning to the colony 5–12 months later for a new
breeding season. By fitting the migratory model to their trajectories, the NSD method identified three distinct
at-sea dispersal scales for the adults of the nine species (Table 3). First, adult giant petrels stayed all year round
close to their colony with low variation around an asymptotic range (Table 3). All the other species moved on
average >3000 km from the colony (Table 3). Adult mollymawks moved to a distance of 5000–6000 km (medium
scale) with little variation around the asymptotic range (Table 3). In other words, they moved rapidly to a specific
zone, the wintering area, where they remained, with only small scale movements. This wintering area was the
same for all individuals of the species and was located over neritic waters; nearby and over the Australian continental shelf. The two species of Sooty albatrosses and Amsterdam albatrosses had medium to long inter-breeding
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dispersal distances with higher range variations (larger wintering area scale) and a high variability within species (Table 3). These three species foraged mainly in oceanic habitats. White-chinned petrels were intermediate
between the two latter groups and wandering albatrosses showed strong inter-individual variability with individuals belonging to the three groups and foraging both in neritic and oceanic waters (Table 3).
Finally, adults foraged at significantly higher latitudes than juveniles for six of the nine species (Wilcoxon
test: P < 0.05 for northern giant petrel, black-browed, Amsterdam, wandering and both sooty albatrosses, Fig. 4).
Adult and juvenile white-chinned petrels foraged at similar latitudes but different longitudes with adults foraging
west of South-Africa (mean longitude = 14.72 ± 2.17°E (SD)) and juveniles foraging mostly east of South-Africa
(mean longitude = 40.83 ± 1.11°E (SD)). There was no significant difference in latitude for southern giant petrels,
but, as for white-chinned petrels, there was a longitudinal segregation between juveniles and adults caused by
their different strategies (nomadic vs resident movement type).
Discussion
Our study is the first to provide a comprehensive examination of juvenile movement strategies among seabirds.
It shows clearly that (1) although species are closely related, the juveniles of the nine species differ extensively in
their movement patterns when they leave their colony of origin, and (2) that for each species the movement types
of juveniles in the first three months following independence are generally similar to those of wintering adults,
except for the two species of giant petrel. In addition, movement patterns appear to be similar within most species, but show high variability for some species with individuals showing mixed strategies.
Interspecific variability in movement strategies and comparison with adults. Overall, the
juveniles of the nine species showed very large-scale post-fledging movements from basin-wide movements to
circumpolar trips. A common behaviour found in all species is the preliminary rapid movement that takes all
individuals away from the vicinity of their colony of origin. This behaviour may allow a reduction of competition
with breeding adults present around the colony at this time, especially in the large albatrosses where breeding
adults are present throughout the year. After this first transit phase, individuals used three very different main
types of large-scale movement patterns.
Juveniles of the two species of mollymawks and white-chinned petrels all exhibited the same migratory strategy as the adults. Their trajectory parameters during the settlement phase are typical of foraging in a restricted
area – suggesting an Area Restricted Search37. In mollymawks, destinations of juveniles partly overlapped with
wintering zones of adults over the continental shelf or shelf-break. These species appear as ‘typical’ migratory species as the route to the wintering grounds corresponds to a narrow corridor used by all age groups, similar to that
seen in certain land birds8,18,38. Analyses at finer scales may help to determine how juveniles and adults interact in
specific overlapping winter feeding areas, e.g. in black-browed and yellow-nosed albatrosses, and how this affects
juvenile survival and/or foraging skill acquisition.
Conversely, juvenile white-chinned petrels head north to exploit favourable Trade winds at low latitudes that
allowed them to reach eastern Africa at low cost. In contrast, adults directly moved to the west to their over-winter
site. This leads to segregation between adults and juveniles, at least during the first part of winter. Adults use
mainly neritic productive waters of the Benguela current off western South-Africa, whereas juveniles use more
oceanic features like oceanic ridges in sub-tropical relatively warm waters (Fig. 4 and Supplementary Fig. 2).
Circumpolar nomadism, i.e. flying with dominant winds toward East, allowed juvenile giant petrels to rapidly
reach areas very distant from their colony and from resident wintering adults, resulting in an extreme case of
segregation whereby juveniles do not overlap at all with adults20. Spatial segregation between age classes during all
or part of the breeding cycle occurs in many species (e.g.22,23,39–41). It has been described for other procellariiform
species like black-footed albatross24 or Manx shearwater42 and is generally explained by competitive exclusion of
juveniles by experienced adults4 in the closest favourable foraging areas around the colonies. Whereas in many
taxa segregation arises from size differences between young and adult39,41, it has been suggested that in monomorphic species with deferred sexual maturity, like seabirds, experience rather than size may drive segregation42.
Competition between age classes may have important consequences for the dynamics of the population26 since
it may affect the reproductive success and survival of individuals8,43. Naïve young individuals excluded actively
from the best foraging places by adults can be forced to use suboptimal feeding areas4,42. Giant petrels are known
for being particularly aggressive competitors44, mainly scavenging when around the colony. Thus we can assume
that juveniles may not be competitive enough to access on land the seal and penguin carcasses or even fisheries
waste used by adults. Juveniles may feed more on pelagic resources until they are able to compete with experienced birds. This creates ontogenic niche divergence and will probably result in a progressive shift in diet during
the immaturity period. A similar pattern of spatial segregation was found between adult and juvenile giant petrels
in the Southern Atlantic45, where juveniles moved out of the adults’ range after 30 days, to forage in productive
upwelling areas that sustained many seabird species. In contrast to giant petrels from Crozet and Kerguelen,
Southern Atlantic juvenile giant petrels, while spatially segregated, feed in a similar oceanic system as adults (shelf
and shelf break)45.
The third strategy that involved large-scale looping movements at the scale of the Southern Indian Ocean was
used by juvenile sooty albatrosses, Amsterdam albatrosses and some wandering albatrosses. Overlap between
adult and juvenile of these species is probably reduced by the extensive size of the sector used in the large looping
movements, and by differences in latitudes.
Although strategies differ extensively among albatrosses and petrels, they are consistent within genus. Each
genus presents particular anatomic characteristics; different wing loading and wing shape that affect flight speed,
manoeuvrability and energetic requirements at take-off or landing46. These differences are likely to affect dispersive abilities as well as foraging ecology47, an interesting aspect to investigate in further detail in future research.
Albatrosses and petrels are known to make extensive use of wind to reduce energetic costs while flying46,48. In our
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study, fifty five percent of the individuals/species flew mainly with dominant winds, the Westerlies, at the beginning of their trip, and later on for giant petrels. Wind is probably a major factor affecting seabird dispersal and in
some species it has been shown that young birds are also affected by other environmental conditions18,25 such as
resource distribution49, e.g. signalled by dimethyl sulphide gradients (phytoplankton related odour)16.
Individual variability.
There were striking differences in individual variability within species, ranging from
strongly consistent juvenile displacement types to species with a high degree of intra-specific variability. Most
species belonged to the former category, whereas wandering albatrosses belonged to the latter, showing a mix
of the three movement strategies with a very high individual variability in all parameters. Considering that all
individuals encountered the same conditions at departure with essentially no movement constraints in an entirely
unexplored environment, the low individual variability within long-range species that visit neritic waters (mollymawks, petrels) is particularly striking. Conversely, more oceanic species with shorter dispersal ranges tended to
show more individual variability. This is particularly true for wandering albatross where individual variability is
the highest. Those individual differences may be in part sex-specific7,50. However adults were similarly variable in
migratory behaviour7,51, suggesting that variability in movement strategy is driven not only by external conditions
but also by the traits and internal state of individuals (morphology, physiology, behaviour). In a relatively homogeneous landscape with few external movement constraints, internal factors may have a more pronounced effect
on the large-scale movement patterns of juveniles and lead to higher individual variability than in coastal waters
where a higher probability of interactions (due to topography, high bird density, fisheries) may affect movement
costs and foraging decisions. Accordingly, despite high within-population variability, individual Atlantic puffins
(Fratercula arctica) show high consistency among years in their own migratory routes52. The authors suggested
that juvenile puffins may make long exploratory trips to different areas acquiring the experience needed to navigate their environment and find appropriate foraging zones. Since juvenile wandering albatrosses travelled across
the whole Indian Ocean or further during their first year at sea, using mixed movement strategies, one might
wonder if this could correspond to an exploratory behaviour. Individuals might acquire knowledge and progressively reduce the range of areas they visit and associated movement patterns until they adopt a foraging strategy
that is consistent from year to year, as the adults do during sabbatical years throughout their life51.
Innate navigation programme.
While anatomy, physiology, competition and environmental conditions
may strongly affect seabird post-fledging movement strategies53, our findings suggest that juveniles may also
partly use an innate navigation programme when leaving their natal colony54. Unlike species for which juvenile
migratory capacities are enhanced by the presence of adults38, juvenile procellariiformes are left by their parents
before they fledge. However, we found that juvenile strategies were consistent from the start within species, and
were similar to those of adults outside of the breeding season in most species. This suggests that juveniles first
follow internal cues, especially for the timing and direction of departure, but also for their destination in the case
of mollymawks and white-chinned petrels. The latter are striking examples since, in order to reach the targeted
foraging ground west of their colony, all individuals first flew northwards to find favourable winds instead of
following the Westerly flow or flying against it to reach directly the destination. This likely genetically encoded
behaviour might have been selected to use the less expensive route in terms of energetics and cause the dispersion
of juveniles to more distant feeding grounds50,55. In contrast to this innate behaviour, it has been suggested that
young Atlantic puffins may rely more on a true learning process42. Overall, juvenile seabirds probably depend
on both innate and acquired skills in different proportion depending on the species. For example, young Cory’s
shearwaters innately follow the same general strategy as older birds, but progressively improve their migratory
route with age22. Orientating in the apparently featureless environment of the pelagic ocean seems challenging,
and the navigation cues, innate or acquired by experience and memory, are far from being clear16,56–58. This innate
programme that drives juveniles on very specific routes may be a disadvantage in a context of rapid global change
when birds may need to adapt to a shift in resources distribution, with unconditional fixed strategies probably
being inferior to condition-dependent strategies35. In migrating birds several populations have retained their
original route that has become sub-optimal in the context of climate change59. Interestingly, all these cases refer
to species where the juveniles migrate independently from the adults and rely on their genetic programme for the
first migration, such as our study species. There seems to be no such case of apparently sub-optimal routes among
species where the juveniles accompany the adults on migration59. Thus, populations with independent juveniles
may be less flexible in terms of migration or movement strategy, for example when facing long-term changes that
need strategy adjustments.
Link between dispersal strategies and life histories. The three main strategies used by juvenile alba-
trosses and petrels were found in three distinct groups: mollymawks and white chinned petrels, great and sooty
albatrosses and giant petrels respectively. The first two groups have contrasting life history strategies independent
of their size: mollymawks and white chinned petrels are shorter-lived species than the others, with annual breeding and high mortalities during the juvenile-immature stages, whereas great albatrosses and sooty albatrosses are
longer lived biennial species with high survival during juvenile and immature phase31–33,60. Thus, the migratory
strategy where juveniles and adults share the same winter zones over shelf areas may result in higher costs in
terms of survival than the large looping strategy over oceanic waters. Moreover, oceanic species are generally
longer lived than neritic species61. Giant petrels are particular in their dispersal strategies, they are shorter lived
for their size but demographic data about the survival of juveniles is lacking62. Although future research with
higher numbers of loggers is necessary to estimate the survival of juveniles during these first months, our results
suggest a more general link between movement strategies, juvenile survival and life history strategies.
The findings of this study may have major implications for understanding the evolutionary mechanisms
underlying the foraging behaviours of naïve individuals, and the link with the characteristics of energy and
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spatial landscapes. Similarly, our results emphasize the importance of linking movement strategies and population dynamics1,35. Thanks to the rapid development of new tagging technology, it is now possible to track multiple
life history stages to study marine predator ecology but also to better understand why juveniles suffer higher costs
during the early stage of their life.
Methods
Field work and telemetry. Field studies were carried out on the Crozet (46.2°S, 52.4° E), Kerguelen (49.4°S,
70.1°E) and Amsterdam (38.4°S, 77.3°E) islands, south western Indian Ocean (see map in Supplementary Fig. 1).
All field procedures were approved by The Ethics Committee of IPEV and Comité de l′Environnement Polaire
and were carried out in accordance with the approved guidelines. We tracked nine species of albatrosses and
petrels belonging to different taxa: two species of great albatrosses (Amsterdam albatross Diomedea amsterdamensis, wandering albatross D. exulans), two species of Mollymawks albatrosses (Indian yellow-nosed albatross Thalassarche carteri and black-browed albatross T. melanophris), two species of sooty albatrosses (sooty
albatross Phoebetria fusca and light-mantled sooty albatross P. palpebrata), two species of giant petrels (northern
giant petrel Macronectes halli and southern giant petrel M. giganteus), and one species of petrel (white-chinned
petrel Procellaria aequinoctialis) (Table 1). Instead of complete species names, species codes are used in tables and
figures, as detailed in Table 1.
Juveniles. Between 2001 and 2014, 98 chicks (Table 1) were fitted with Argos satellite transmitters (Platform
Terminal Transmitter, PTT 100, Microwave Telemetry, Columbia, USA) just before fledging. Units were fixed
on the birds’ back feathers using adhesive tape and glue. The mass of devices (20–50 g) was always below the
3% of the body mass limit recommended for flying birds (Phillips et al. 2003). Transmitters were powered with
solar panels and worked with duty cycle mode, 10 hON-24 hOFF, 18 hON- 54OFF or 12 hON-60 hOFF. Some of
the juveniles were sexed using a molecular sexing method, others are of unknown sex. After data filtering and
homogenization (Supplementary Methods 1) we obtained a total of 83 tracks, with 53 lasting at least 3 months
and with an average of 0.65 ± 0.12 (SD) locations per day.
Adults. Adults from the same nine species and same sites were tracked during the non-breeding season, when
they are no longer central place foragers. Birds were fitted with light-recording geolocators (GLS) weighting less
than 3 g and attached to a leg band, beginning in 2000. GLS give positions twice per day with a low accuracy
(median error of 180 km)63. To compare the overall large-scale movement patterns of juveniles and adults we
randomly chose 10 complete adult tracks per species starting at the end of a breeding season and ending at the
beginning of the next one. To compensate for the low accuracy of locations given by the GLS system we smoothed
the trajectories by averaging locations on a 3-days’ time scale. Due to the low accuracy and low frequency of
sampling we used adult data only for the comparative analysis of overall displacements and a global assessment of
habitats used but not for the detailed trajectory analysis.
Movement Analysis. We used two types of approach for analysing the movement data, both implemented
using the R Software Environment64. 1: The squared displacement method was used to identify and compare
movement types within and between age classes and species36. 2: Movement statistics commonly used for animal
trajectory analysis were calculated to quantify detailed juvenile movement parameters and test the innate navigation hypothesis65.
To identify and compare movement types within and between
age classes and species, we used the squared displacement method36. The net squared displacement distance
(NSD) is the squared beeline distance (calculated using Haversine formula) between the starting point (here,
the natal colony of the birds) and each location of the trajectory. It is a fundamental statistic for movement studies66,67. We used the NSD method36 to identify and compare different broad movement types such as sedentary
(“home range”), migratory and nomadic movement modes (Supplementary Methods 2-Fig. 1), and concurrently
estimate general movement statistics such as distance covered (Supplementary Table 1). The approach is continuous time based and allows for the efficient analysis of unequally and irregularly sampled movement trajectories.
Following36 we fitted the movement mode models (Supplementary Methods 2-Equation 1) using nonlinear mixed
effects models (nlme in ‘nlme’ R library) and evaluated the support from the data for the different movement
modes using the concordance criterion68. Before applying the goodness-of-fit measure we also checked that the
estimated parameters (e.g. timing or distance of dispersal) were consistent with the spatio-temporal scales of the
trajectory and discarded models that were inconsistent (Supplementary Table 1).
Comparative analysis of displacement.
Juveniles. We applied NSD models to juvenile movement data covering the first 3 months after departure from
the natal colony (see details in Supplementary Methods 2.1). Figure 1 shows typical juvenile trajectories along
with the corresponding NSD curve and model fit. We identified a new movement type that we named “large-scale
looping” (Fig. 1c, details in Supplementary Methods 2.2). To complete the information given by the NSD method,
we calculated the distance from the colony reached at 3 months for an index of dispersion distance and classified species as follows: (1) small scale movements – birds which remained in the Indian Ocean, at a range
shorter than 3000 km from the colony; (2) medium scale movements - birds which dispersed to the Australian or
South-African coasts, i.e. between 3000 and 6000 km; and (3) large scale movements - birds which left the Indian
Ocean and ranged farther than 6000 km.
Adults. For adult birds we applied the NSD method on the whole inter-breeding period, i.e. 5 to 12 months
depending on the species. All adult trajectories were best fitted by the migratory model as adults always returned
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to the colony to breed. As for juveniles, we compared inter-breeding migration distances and displacements
scale in the wintering areas along with the type of habitat used (neritic or oceanic) as detailed in Supplementary
Methods 2.3.
Trajectory parameters analyses. To quantify detailed juvenile movement parameters and test the innate
navigation hypothesis, we calculated movement statistics commonly used for animal trajectory analysis65, i.e. orientation, daily distance travelled, sinuosity and range. For consistency, all parameters were averaged over 15 day
time periods for the three first months of the trips for each individual. To aid visualization, however, we present
only the first 15 days of each month in our figures, i.e. values for three periods of 15 days. Circular statistics for
orientation analyses were computed with the R package “circular”69. For other parameters, we used linear mixed
effect models (lme within ‘nlme’ R package70) with individual as random factor to take into account individual
variability, followed by post-hoc Tukey tests (‘multcomp’ R package71) to test for temporal and interspecific differences (see lme & Tukey test results in Supplementary Results 1 & 2 and Supplementary Table 2). Differences
between time periods or between species were considered significant at the P < 0.05 level in Tukey pair-wise comparison tests. For all models we visually checked that model assumptions were met. For Yellow-nosed albatrosses
and other species after a certain amount of time, small sample sizes lead to unsatisfactory residual distribution
and thus the tests for these species are to be considered with care (see supplementary Method 3 for details).
Parameters calculated for each track were: the bearing taken at departure, the directionality of the bird with
respect to the colony after two and three months, the sinuosity of tracks, the daily distance travelled and the mean
latitude attained. Details for parameter calculations and statistics can be found in Supplementary Methods 3.
Habitats used. To determine the conditions where juveniles settled in specific areas we examined the bathy-
metric characteristics of their last locations (neritic waters when depth >−3000 m, i.e. from lower continental
slope to continental shelf, or oceanic area when over deeper waters), and compared this with adults’ broad habitat
types (Supplementary Methods 2.3). Although it was not possible here to obtain accurate information on adult
habitat, we extracted bathymetry, daily sea surface temperature (SST) and monthly chlorophyll a (CHLa) values
for all juveniles’ trajectories. Environmental data were downloaded from the NOAA coast watch website (http://
coastwatch.pfeg.noaa.gov/erddap/index.html). To allow comparison between species, bathymetry, SST and CHLa
values have been summarised in Supplementary Fig. 2. As for trajectory parameters, differences between species
have been tested with linear mixed models and Tukey post-hoc tests in order to take individual variability into
account. We used all locations with environmental data available and took autocorrelation into account in the
models. Conversely, the large inaccuracy of GLS locations did not permit to reach any conclusions about adult
habitat characteristics.
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Acknowledgements
The study at Crozet, Amsterdam and Kerguelen Islands was supported by IPEV (programme N° 109), with
additional funding from the Prince Albert II de Monaco Foundation. We thank the many field workers involved
in the field programmes, and Dominique Besson, Karine Delord and Maud Berlincourt for help with data
management as well as Rory Wilson, Tim Coulson and E.J. Milner-Gulland for helpful comments on earlier
version of the manuscript and Emily Shepard for English language corrections. We thank the two anonymous
referees for extensive comments and suggestions on earlier version of the manuscript. The study is a contribution
to the Programme EARLYLIFE funded by a European Research Council Advanced Grant under the European
Community’s Seven Framework Programme FP7/2007–2013 (Grant Agreement ERC-2012-ADG_20120314 to
Henri Weimerskirch). Sophie de Grissac was funded by the ERC Grant.
Author Contributions
H.W. designed research and corrected the manuscript; S.d.G. collected field data, analysed data and wrote the
manuscript; L.B. helped for NSD analyses and manuscript writing, A.G. did preliminary statistical analyses. All
authors gave final approval for publication.
Additional Information
Supplementary information accompanies this paper at http://www.nature.com/srep
Competing financial interests: The authors declare no competing financial interests.
How to cite this article: Grissac, S. et al. Contrasting movement strategies among juvenile albatrosses and
petrels. Sci. Rep. 6, 26103; doi: 10.1038/srep26103 (2016).
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Scientific RepoRts | 6:26103 | DOI: 10.1038/srep26103
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