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Allopreening in the Black-browed Albatross
(Thalassarche melanophris): an exploration of
patterns and possible functions
NATASHA GILLIES,*
1
TIM GUILFORD
1
& PAULO CATRY
2
1
Department of Zoology, University of Oxford, Oxford, UK
2
MARE –Marine and Environmental Sciences Centre, ISPA –Instituto Universit
ario, Rua Jardim do Tabaco 34,
Lisbon, 1149-041, Portugal
The functions of display between breeding pairs of animals have been given little atten-
tion outside of sexual selection. Yet evidence suggests that display between partners is in
fact most commonly observed following mate choice, and is often just as elaborate. In
many bird species, allopreening, when one member of a pair preens the other, is a major
component of display both pre- and post-pair formation. Despite this, there has been lit-
tle investigation into its functions. Explanations that have been put forward tend to focus
on its role in feather hygiene, which has limited phylogenetic support, or its function in
the maintenance of the pair bond, though how this might occur or indeed what this
actually represents has not been adequately explained. Phylogenetic evidence reveals that
allopreening is most commonly observed in those species exhibiting high levels of part-
ner retention and biparental care, and it appears to be functional in maintaining coopera-
tion in parental behaviour in at least one species. In our observational study, we
explored the patterns and putative functions of allopreening during the nest-relief dis-
plays of breeding pairs of Black-browed Albatrosses Thalassarche melanophris during
incubation and chick-provisioning. Allopreening was an important feature of displays,
constituting 30% of display time. We found that the bird returning from its foraging trip
usually initiated allopreening, and preened more than its partner prior to change-over of
nesting duties. We further found a positive relationship between the amount of time the
pair spent in display and the duration of the subsequent foraging trip, providing tentative
support for a function in maintaining cooperative parental behaviour between the par-
ents. Although we cannot be conclusive as to its exact functions, we add to a limited lit-
erature the first exploration of functions for this conspicuous behaviour in albatrosses.
Keywords: display, foraging, negotiation, parental care.
Despite more than a hundred years having passed
since Huxley’sfirst observations that intra-pair dis-
play is more commonly observed after than before
pair formation (Huxley 1914), pair display often
remains viewed through the lens of sexual selection
(Griffith 2019). Consequently, the functions of dis-
plays occurring after mate choice has been made
(hereby post-pair formation display) remain poorly
understood. Post-pair formation displays can be
every bit as elaborate as those seen during mate
choosing, from the post-nuptial displays of Great
Crested Grebes Podiceps cristatus that initially
piqued Huxley’s interest, to the private duets of
Zebra Finches Taeniopygia guttata as they exchange
incubation duties (Elie et al. 2010). Although such
displays have historically been explained with ref-
erence to the intangible ‘maintenance of the pair
bond’(Harrison 1965), this in itself requires ulti-
mate explanation, and few authors have attempted
to explain exactly how display contributes to this
maintenance, or indeed what the bond actually
represents (Wachtmeister 2001).
*Corresponding author.
Email: gilliesne@gmail.com
Twitter: @tash_gillies
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
This is an open access article under the terms of the Creative Commons Attribution License, which permits use,
distribution and reproduction in any medium, provided the original work is properly cited.
Ibis (2021) doi: 10.1111/ibi.12960
In birds, one of the more common forms of
post-pair formation display is the nest-relief cere-
mony (Wachtmeister 2001), in which one parent
returns to the nest to relieve the other of its par-
enting duties. These displays are common in
socially monogamous, biparentally caring species.
For such species, in which pair bonds persist for
long time periods, the breeding success of parents
is largely interdependent, ultimately leading to
highly aligned lifetime reproductive output
(Griffith 2019). Consequently, parents may benefit
from coordinating their behaviour to maximize the
benefit to cost ratio of providing care from the
perspective of both parents (Mariette & Griffith
2015, Pilakouta et al. 2018). Intra-pair communi-
cation can help parents achieve this coordination
and may manifest in post-pair formation display.
Through such displays, parents may, for example,
signal their state to the partner to stimulate a
change in its behaviour. This appears to be the
case in Great Tits Parus major, where the incubat-
ing female vocally communicates her hunger to
the male to stimulate him to feed her more, so
that she can reduce her own foraging effort
(Boucaud et al. 2016a). Communication may also
facilitate direct negotiation: Blue-footed Boobies
Sula nebouxii ultimately come to a collaborative
decision on where to lay their eggs by negotiating
their nesting site preferences through ‘nest-point-
ing’displays (Drummond et al. 2002).
Allopreening, in which one individual preens
another, is often incorporated into displays both
pre- and post-mate selection (Wachtmeister
2001). Allopreening may play a hygienic role
through the removal of ectoparasites, as has been
experimentally investigated in some species (e.g.
Rock Pigeons Columba livea, Villa et al. 2016;
Eudyptid penguins, Brooke 1985), or may help
maintain feather condition by protecting against
breakage and facilitating the distribution of preen
oil (Clayton 1991). However, its restricted phylo-
genetic distribution suggests any such function
must be secondary to its ancestral purpose
(Harrison 1965). Furthermore, if allopreening ini-
tially evolved to serve a hygienic function, it might
be expected that its occurrence would be particu-
larly prevalent in highly gregarious species living in
close physical proximity, as a means to control the
spread of ectoparasites. However, phylogenetic
analysis (Kenny et al. 2017) reveals no association
between allopreening and colonial living. Both
allopreening and its mammalian counterpart,
allogrooming, have been found to reduce stress in
a variety of taxa, including Br€
unnich’s Guillemot
Uria lomvia (Kober & Gaston 2003), Common
Guillemots Uria aalge (Lewis et al. 2007), Ravens
Corvus corax (St€
owe et al. 2008), Horses Equus
caballus (Feh & de Mazier
es 1993) and Crested
Black Macaques Macaca nigra (Aureli & Yates
2010). However, it is not clear how or why allo-
preening would evolve to elicit such a response.
Social functions for allogrooming in mammals have
been well-explored, particularly in the primates
(Dunbar 1991), and increasing evidence is emerg-
ing for the importance in birds of its counterpart,
for example when forming and maintaining social
bonds (Morales Picard et al. 2020), establishing
dominance (e.g. Large-billed Crows Corvus macro-
rynchos, Miyazawa et al. 2020), forming pairs (e.g.
Eurasian Wrens Troglodytes troglodytes, Gill 2012),
and as an appeasement behaviour (e.g. Common
Guillemots, Birkhead 1978). However, the possi-
bility that allopreening functions in maintaining
cooperation in parental behaviour has been little
explored. A study of allopreening in Common
Guillemots revealed the first evidence that
allopreening may serve a cooperative function
(Takahashi et al. 2017). Parent Common Guille-
mots that return to the nest without food for the
chicks spent more time preening the partner, and
birds whose partners took longer to take over nest-
ing duties delayed allopreening, suggesting it may
serve a dual appeasement and punishment func-
tion. Allopreening has additionally been linked to
partner retention between breeding seasons
(Gill 2012) and high levels of parental cooperation
(Kenny et al. 2017), further hinting at a social and
potentially cooperative function of this behaviour.
Allopreening is a common behaviour in the
Black-browed Albatross Thalassarche melanophris
that can be observed during initial pair formation,
between paired individuals throughout the breed-
ing season, and between parents and offspring
(Tickell 1984). While allopreening albatrosses tend
to focus on the head and nape of their partners, as
is the case in other species (Harrison 1965), direct
observations conducted by Tickell (1984) did not
report any evidence of individuals removing lice or
ticks from their partners during allopreening, sug-
gesting this is not its primary function, though this
is yet to be experimentally tested. As is character-
istic of the Procellariiforms, Albatrosses are long-
lived, have stable, long-term pair bonds, and care
for their offspring cooperatively with their partner
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
2N. Gillies et al.
(Tickell 2000). That paired individuals continue to
allopreen following their reunion at the beginning
of the season and throughout breeding raises the
prospect that allopreening may function to encour-
age or facilitate parental care. Whereas some evi-
dence from other species points to mechanistic
explanations for how this could operate, for exam-
ple by stimulating the production of hormones
such as oxytocin or prolactin (Keverne et al.
1989), or by reducing stress levels (Schino et al.
1988), functional hypotheses have been less well
explored, particularly in birds.
During incubation and brood guarding, parent
Black-browed Albatrosses engage in conspicuous
nest-relief displays as they exchange parenting
duties with the partner. While these displays com-
prise many other behaviours, such as vocalization
and ritualized dance postures, the predominant
behaviour is allopreening, on which this study is
focused. Using a field observation approach, we
describe the patterns of allopreening observed
between reuniting parent albatrosses during late
incubation and early brood guarding and consider
the potential drivers and functions of its observed
variation.
First, levels of allopreening have been found to
vary with sex (Zolnierowicz et al. 2016, Miyazawa
et al. 2020), have been linked to partner retention
(Gill 2012, Kenny et al. 2017), and may vary with
age and breeding experience (Lanctot et al. 2000,
Perrot et al. 2016). We therefore investigated
whether these factors predict the duration of allo-
preening bouts and nest-relief displays in the
Black-browed Albatross.
Secondly, based on previous phylogenetic analy-
ses that report that allopreening is associated with
cooperative parental care (Kenny et al. 2017), we
investigated the possibility that allopreening may
serve such a function in Black-browed Albatrosses,
which, as long-lived, socially monogamous birds,
should be selected to care cooperatively with their
partners (Griffith 2019). Specifically, we explored
whether allopreening might facilitate information
transfer that could be involved in the coordination
of parental care. For example, allopreening might
form part of an assessment or negotiation process
whereby the outgoing parent determines the con-
dition or state of its partner, and subsequently uses
this information to decide how long to spend at
sea. In this way, an outgoing bird that perceives its
partner to be in a poor state may spend less time
at sea so it can relieve it from nesting duties more
quickly. Evidence for such prior ‘planning’of for-
aging trip duration has been reported for Manx
Shearwaters Puffinus puffinus (Guilford et al.
2008), where parents that embarked on long for-
aging trips were already found further from the
colony than those on short trips on the first day of
foraging. To investigate the possibility that the
nest-relief ceremony could facilitate information
transfer in this way, we investigated whether a
relationship existed between display time and the
duration of the subsequent or previous forward
trip. Furthermore, when the egg hatches, allo-
preening between adults and chicks could present
an additional source of information for such deci-
sion-making processes. For example, parents’will-
ingness to engage in allopreening of chicks might
signal to their partner that they are in good condi-
tion and therefore ready to provide care. We
explored the possibility of a signalling role for
chick-directed allopreening by examining whether
there were qualitative differences in chick-directed
allopreening when it occurred during the nest-re-
lief display vs. when parents were alone with their
offspring. Such mechanisms of assessment could
allow parents to make optimal decisions about
their foraging trip durations from the perspective
of the pair as a whole, ultimately maximizing life-
time reproductive output for both parents.
METHODS
Study site
This study was carried out on New Island, Falk-
land Islands (51°43’32’’S, 61°17’55’’W), where
individually marked Black-browed Albatrosses
have been monitored since 2003. Between 6
December 2019 and 10 January 2020, encompass-
ing late incubation and early chick-rearing, which
in this species lasts 68–71 and 120–130 days,
respectively (Tickell 2000), adult attendance was
monitored daily in 114 nests in which both par-
ents were marked with a coloured plastic ring, per-
mitting identification at a distance. The sex of
birds had been previously identified through the
observation of sex-specific pre-incubation beha-
viours or through molecular techniques using
DNA from blood samples (Fridolfsson & Ellegren
1999). For 74 nests, pairs had been monitored for
multiple years and so their pair experience, taken
as the number of years both birds had been
observed breeding together, could be determined.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
Allopreening in the Black-browed Albatross 3
The age of eggs and chicks was taken as the num-
ber of days since laying and hatching, respectively.
Observations
A total of 99 nest-relief displays were observed.
Observations were conducted between the hours
of 09:00 and 20:00 (Falkland Islands Standard
Time) by a single observer. Approximately 6 h of
observation was conducted per day, usually split
into two shifts. A mean of 2.8 displays were
observed per day. Due to the small size of the col-
ony and its sloped topography, all nests could be
observed from a single viewpoint. Behavioural data
were collected during the nest-relief displays of
pairs, when the previously foraging parent returns
to the nest to relieve its partner from parenting
duties (incubating the egg or brooding the chick).
Data collection began from the moment the
incoming bird was sighted near the nest to the
moment its partner was deemed to have departed
from the colony, either because it had taken off
into flight or because it had walked out of sight.
The time between the arrival of the incoming bird
at the nest and the point at which the departing
bird ceased interaction with its partner was
recorded as ‘total display time’. Whenever the
incoming bird arrived at the colony, the observer
commenced data collection while simultaneously
changing position to be within 1–2 m of the target
nest for the duration of the recording period. At
this distance, pairs did not respond to observer
movements (N. Gillies pers. obs.). This movement
took less than 1 min and observation was possible
throughout, so important behaviours were unlikely
to be missed. Allopreening was identified as any
preening directed at either the partner or chick.
For any bout of allopreening, the duration and
recipient were manually recorded in real time
using a pencil and notepad, and a stopwatch to
record duration, for both parents simultaneously.
Any switch or pause in behaviour that lasted
longer than 1 s indicated the end of a single bout.
The time at which parents physically exchanged
duties (indicated by swapping positions on the
nest) was recorded and is henceforth referred to as
the ‘changeover’.
The duration of foraging trips was determined
as the number of days between sequential sightings
of an individual Black-browed Albatross at the
nest, i.e. the total number of consecutive days that
that individual was not seen on the nest. Mean
foraging trip duration is 5.2 days (range: 0.3–
11.3 days) during incubation and 1.9 days (range:
0.1–6.3 days) during chick provisioning (Grana-
deiro et al. 2018), and so while it is possible that
adults returned to the nest outside of the observa-
tion window, and so the duration of the trip in
hours would not be known, number of days is a
valid proxy for trip duration (Weimerskirch et al.
1994).
Allopreening between adults and offspring was
observed during nest-relief displays and sporadi-
cally when parents were alone with the chick dur-
ing brooding. We investigated whether there were
qualitative differences in chick-directed allopreen-
ing between these contexts that may indicate a
role of this behaviour in the display. To this end,
we collected data on the number of chick-directed
allopreening bouts during nest-relief displays. We
additionally estimated the frequency at which
chick-directed allopreening occurs when parents
are alone during brooding. Between 1 and 10 Jan-
uary 2020, we scanned the entire colony oppor-
tunistically in three to five 5-min bouts per day
during the observation window, and counted the
number of brood-guarding parents that allo-
preened their chicks in this time. We converted
the resulting number of parents observed allo-
preening to a proportion of total nests in the col-
ony where the adult was brood guarding. These
frequency data were collected over 31 bouts.
Environmental data
Wind conditions at sea are likely to affect the
duration of foraging trips in albatrosses (Wakefield
et al. 2009), and so we accounted for this in our
models of trip duration. Crosswind and tailwind
components were reasoned to be the most impor-
tant components of the wind, based on an a priori
expectation as to effects of the interaction
between wind and a shear-soaring flight mecha-
nism (Pennycuick 2002, Sachs 2004, Paiva et al.
2010, Ventura et al. 2020). Estimated wind data
for the colony location were downloaded from the
NOAA Global Forecast System at a spatial resolu-
tion of 0.5°and a temporal resolution of 3 h using
the R package rWind (Fern
andez-L
opez & Schliep
2019). For each bird, a probable crosswind and
tailwind component was calculated for its at-sea
duration assuming travel to the most likely feeding
locale around Staten Island (southern Argentina;
Catry et al. 2013). It was further hypothesized
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
4N. Gillies et al.
that weather conditions at the colony might affect
display behaviours. To this end, qualitative data on
weather were collected each morning and after-
noon of observations, using the simple categoriza-
tion of ‘overcast’,‘sunny’,‘showers’or ‘fog’.
Statistical analysis
Statistical analyses were completed in R version
3.51 (R Core Team 2018). The R package lme4
(Bates et al. 2015) was used to construct linear
mixed effects models (LMMs) and generalized lin-
ear mixed effects models (GLMMs), and P-values
were obtained by comparing full models contain-
ing all variables to null models without the effect
of interest, using a likelihood ratio test. For cate-
gorical variables, least squares means for each
level of the factor were calculated using the R
package emmeans (Lenth et al. 2018). Data are
presented as means standard deviation. For
brevity, model structures are presented in
Table 1. All models were fitted with a random
intercept for individual (Ring), pair identity (Pair)
or individual nested within pair identity (Pair:ring)
as appropriate, to control for repeated measures.
We additionally included the fixed effects of sex,
age and breeding experience (in years), which we
identified as factors possibly influencing beha-
viour.
We investigated which variables explain the
amount of time spent allopreening by individuals
(Table 1, Model 1), by the pair as a whole
(Table 1, Model 2), and between parents and off-
spring (Table 1, Model 3).
To investigate whether sex or the breeding
experience (in years) of individuals influenced the
amount of time they engaged in allopreening, we
fitted a binomial GLMM to the time an individual
spent allopreening its partner, calculated as a pro-
portion of the total allopreening time in the dis-
play, as a function of sex and breeding experience
(Table 1, Model 1). Allopreening time may differ
depending on whether the bird is arriving at or
departing from the nest and might additionally
vary before and after physical changeover on the
nest. We accounted for this by including the fixed
effects of ‘position’(incoming vs. outgoing bird)
and ‘timing’(pre- or post-changeover).
‘Total allopreening time’was taken as the
summed duration (in seconds) of all allopreening
bouts by both parents in a single display. We
investigated whether total allopreening time varied
with breeding experience of the pair (in years),
historical breeding success (chicks fledged per
breeding attempt) or sex of the outgoing bird by
fitting an LMM (Table 1, Model 2) that included
these variables as fixed effects. To account for
differences between incubation and chick
Table 1. Model structures used in the analysis. Model numbers are those in the text.
Type of
model Model
Parameters
Response Fixed Random
Binomial
GLMM
1 Individual proportion of
time spent allopreening
Position *timing +sex +breeding years Pair : ring
LMM 2 Total allopreening time
(in seconds (s))
Experience +success +stage +sex +total display time Pair
3 Number of chick-directed
preening bouts
Experience +position +age +sex +total display time Pair : obs.ID
LM 4 Total display time (min) Experience +success +stage *age +sex +previous trip
5 Foraging trip duration
(days)
Experience +success +stage *age +sex +total display time +total
allopreen time +previous trip +stage *total display time +
crosswind +headwind +qual
Position =whether the bird was ‘incoming’or ‘outgoing’from the nest; timing =timing in the display, either pre- or post-changeover;
sex =male or female; breeding years =years individual observed breeding; experience =years pair observed breeding together;
pair =pair identity; ring =bird identity; success =historical breeding success, number of chicks fledged per breeding attempt;
stage =breeding stage, incubation vs chick brooding; total display time =time from arrival of incoming bird to cessation of pair inter-
action; age =age of offspring relative to hatch date in days; obs.ID =unique identity for each changeover display; previous trip =du-
ration of foraging trip that ended in changeover; total allopreen time =total time spent preening during display; qual =qualitative
weather. Foraging trip duration refers to the trip immediately following the nest-relief display.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
Allopreening in the Black-browed Albatross 5
provisioning, we additionally included ’breeding
stage’as a fixed effect. Finally, we included total
display time (in minutes) as a controlling variable,
as this dictates the amount of time available for
allopreening.
We investigated whether and which factors pre-
dicted the number of chick-directed allopreening
bouts instigated by each parent. We fitted an
LMM to the number of bouts using the predictors
of sex and whether the bird was arriving at or
departing from the nest (‘position’; Table 1, Model
3). We included ‘total display time’as a fixed
effect to account for the amount of time available
to parents to allopreen their chicks.
We were further interested in what factors pre-
dict variation in total display time (Table 1,
Model 4) and foraging trip duration (Table 1,
Model 5). We hypothesized that if nest-relief dis-
plays facilitate information transfer between the
pair, then we would observe a relationship
between the duration of the display and the dura-
tion of either the preceding or the subsequent for-
aging trip.
For models 4 and 5, we included only those
nests for which previous trip duration was known.
As only 16 nests had more than one observation,
we randomly selected one observation from each
of these nests. We first fitted a linear model (LM)
to total display time (minutes) as a function of the
duration of the previous foraging trip in days (‘pre-
vious trip’; Table 1, Model 4). As display time
may also vary with breeding experience of the
pair, historical breeding success, breeding stage,
offspring age and sex of the outgoing bird, we
included these variables as fixed effects. The effect
of age may differ between eggs and chicks, and so
we included an interactive effect between age and
breeding stage. We then fitted an LM to subse-
quent foraging trip duration (days) as a function of
total display time (minutes) and total allopreening
time (seconds; Table 1, Model 5). As before, we
controlled for experience, breeding stage, historical
breeding success, offspring age and sex of the
outgoing bird. As consecutive foraging trips are
likely to be correlated in length, we also included
the fixed effect of previous trip duration. Finally,
environmental conditions are known to affect for-
aging trip duration in Black-browed Albatrosses
(Wakefield et al. 2009). To control for this, we
included the environmental variables of crosswind,
headwind and qualitative weather (see Methods,
Environmental data).
RESULTS
Displays in which the exact timings of changeover
were not known or where foraging trip duration
was unknown were excluded from the analyses,
leaving 91 displays across 63 nests. Across all dis-
plays, the incoming bird was female in 49% of
observations and male in 51% of observations.
Of the 91 nest reliefs observed, 90 involved dis-
play, which lasted for an average of
23.3 19.0 min (range: 3–101 min). In the single
nest relief that did not involve display, the sitting
bird left the nest immediately following its part-
ner’s arrival at the colony. Allopreening was
observed in all 90 of these displays and constituted
a mean of 26.7 16.2% of display time (range
0.26–79.33%). Anecdotally, it was observed that
this tended to focus on the head or neck of the
bird, but it was not clear that any birds attempted
to target ectoparasites specifically; parasites visible
by an observer at a distance of 1–2 m were on
occasion seemingly ignored by the allopreening
bird (N. Gillies pers. obs.). Individual bouts of
allopreening lasted 16.1 23.4 s, and each display
comprised 27.1 26.2 bouts.
In 62% of displays, the incoming bird initiated
allopreening, in 26% the outgoing bird initiated,
and in 12% both birds began allopreening simulta-
neously. Following the changeover, the incoming
bird resumed allopreening first in 64% of displays,
the outgoing bird resumed in 28% of displays, and
both birds simultaneously resumed in 8% of dis-
plays.
Model 1 –Individual allopreening time
The proportion of time individuals spent allo-
preening their partners during the display was best
predicted by an interaction of whether the bird
was incoming to or outgoing from the nest, and
whether allopreening occurred before or after
changeover (v
2
=12475.05, df =1, P<0.0001;
Fig. 1). Prior to changeover, incoming birds spent
a greater percentage of the display allopreening
compared with departing birds (incoming:
5.27 0.84%, outgoing: 0.24 0.042%). This
reversed following changeover, when outgoing
birds were found to spend more time allopreening
compared with incoming birds (incoming:
2.41 0.39%, outgoing: 4.44 0.72%). Females
spent a greater percentage of their display time
engaged in allopreening compared with males
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
6N. Gillies et al.
(female: 2.97 0.63%, male: 1.26 0.28%;
v
2
=8.3, df =1, P=0.0040). The number of
years an individual had been observed breeding
had no effect on the time they spent allopreening
(v
2
=0.92, df =1, P=0.34), and allopreening
times were not repeatable at the level of individual
(104 observations across 44 individuals,
r=0.0087 0.019, P=0.41).
Model 2 –Total allopreening time
The amount of time pairs spent allopreening
decreased by 12.13 5.73 s for each year that
the pair had been together, though there was no
effect of historical breeding success (Fig. 2;
Table 2). There was no effect of the sex of the
outgoing bird or breeding stage on allopreening
time (Table 2). As expected, there was a strong
correlation between total allopreening time and
total display time, with the amount of time spent
preening increasing by 0.30 0.032 s for each 1-s
increase in display time (Table 2), suggesting that
when controlling for other variables, the percent-
age of time spent allopreening during display was
approximately 30%.
Model 3 –Chick-directed preening
Of the 68 displays that took place during chick-
rearing, 83.3% involved some allopreening of the
chick. The amount of allopreening varied signifi-
cantly depending on whether it was provided by
the incoming, outgoing or both parents (Table 3),
with incoming birds providing more bouts of allo-
preening compared with outgoing parents (incom-
ing: 5.68 0.37 bouts, outgoing: 0.35 0.37
bouts) and simultaneous preening by both parents
making up the fewest number of bouts
(0.32 0.37 bouts). There was no effect of sex,
age, breeding experience or total display time on
the number of bouts (Table 5).
Parents were frequently observed to preen
chicks when alone during brood guarding. During
our daily preening observations, the number of
nests in which the chick was being brood-guarded
varied between 19 and 79, with a median of 43.
Figure 1. Proportion of total display time spent allopreening
prior to changeover and following it for the incoming (orange)
and outgoing (green) parents. Black crosses indicate mean
(horizontal line) and standard error (vertical line). Data points
are ‘jittered’horizontally for readability.
Figure 2. Total time spent preening by both parents in sec-
onds according to pair breeding experience (years). Shaded
area gives confidence intervals.
Table 2. Test statistics and coefficient coordinates from a like-
lihood ratio test on LMM estimating predictors of total allo-
preening time (seconds).
Variable v
2
df P-value Estimate se
Experience 4.76 1 0.029 –12.13 5.73
success 0.53 1 0.47 –90.29 134.00
stage (egg) 1.57 1 0.21 104.70 87.85
outgoing sex (M) 3.38 1 0.066 –104.96 57.89
Total display time 59.75 1 <0.0001 18.13 2.00
Significant variables in bold. Experience =number of years
pair observed together; Success =historical breeding success,
chicks fledged per breeding attempt; Stage =breeding stage,
incubation vs. brood guard; outgoing Sex =sex of departing
parent; Total display time =total duration of display in minutes.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
Allopreening in the Black-browed Albatross 7
On each day in any 5-min interval, a median of
14.1% of adults could be observed to preen their
offspring (range =8.5–18.4%).
Model 4 –Display duration
There was no effect of sex of the outgoing bird,
previous foraging trip duration, pair experience, or
the interaction of breeding stage and offspring age
on display duration (Table 4). Displays during
incubation were significantly longer than during
chick-rearing, at 59.61 20.8 min vs. 15.98
2.69 min for chick-rearing.
Model 5 –Foraging trip duration
There was a significant effect of the interaction
between offspring age and breeding stage on the
duration of foraging trips (Table 5). Mean trip
duration for incubating birds was 4.17 1.89 days
vs. 1.68 0.39 days for brood-guarding birds
(Fig. 3a). For each day increase in age, trip dura-
tion decreased by 0.58 0.14 days for incubating
birds and increased by 0.0016 0.030 days for
brood-guarding birds (Fig. 3b). Total display time
significantly predicted foraging trip duration during
incubation (Fig. 4, Table 5), with trip duration
decreasing by 0.085 0.025 days for each 1-min
increase in display time for incubating birds. There
was no effect of sex, pair experience, previous trip
duration, total allopreening time or any of the
three weather variables on trip duration (Table 5).
DISCUSSION
We report tentative evidence that allopreening,
which was observed to be a conspicuous feature of
nest-relief displays in Black-browed Albatrosses,
Table 3. Test statistics and coefficient coordinates from a like-
lihood ratio test to investigate the significance of fixed effects
on the number of chick-directed allopreening bouts.
Variable v
2
df P-value Estimate se
Experience 1.23 1 0.26 –0.052 0.048
Position
(incoming)
106.49 1 <0.0001 5.36 0.49
Position
(outgoing)
0.033 0.49
Sex (M) 0.22 1 0.64 –0.18 0.40
Age 3.61 1 0.057 0.070 0.037
Total display time 0.43 1 0.51 0.015 0.023
Significant variables in bold. Experience =years pair
observed breeding together; Position =driver of chick allo-
preening, either incoming, outgoing, or both parents;
Sex =male or female, for simultaneous preening represents
sex of incoming bird; Age =offspring age; Total display
time =total duration of display in minutes.
Table 4. Test statistics and coefficient coordinates from
ANOVA to investigate the significance of fixed effects on total
display time.
Variable tP-value Estimate se
Experience 0.057 1.0 0.027 0.47
Success 0.92 0.37 9.39 10.27
Stage (egg) 3.38 0.0016 36.16 10.71
Age –0.50 0.62 -0.19 0.38
Stage*age 0.61 0.55 0.92 1.52
Outgoing sex (M) 1.88 0.067 8.82 4.69
Previous trip –0.71 0.48 -0.89 1.25
Significant variables in bold. Experience =years pair
observed breeding together; Success =historical breeding
success, chicks fledged per breeding attempt; Stage =breed-
ing stage, incubation vs. brood guard; Age =offspring age;
outgoing Sex =sex of departing parent; Previous trip =dura-
tion of preceding foraging trip.
Table 5. Test statistics and coefficient coordinates from
ANOVA to investigate the significance of fixed effects on for-
aging trip duration (days).
Variable tP-value Estimate se
Experience 0.72 0.48 0.031 0.043
Success 0.86 0.40 0.74 0.86
Stage (egg) 4.06 0.00040 4.46 1.10
Age 0.045 0.96 0.0016 0.035
Stage*age –4.24 0.00025 –0.58 0.14
Outgoing sex (M) 1.14 0.27 0.49 0.43
Total allopreen time 1.18 0.25 0.00091 0.00077
Previous trip 1.78 0.086 0.21 0.12
Total display time –0.32 0.75 –0.0087 0.027
Stage*total display
time
–3.0 0.0061 –0.076 0.025
Headwind 1.79 0.087 0.0034 0.0019
Crosswind 0.63 0.54 0.00082 0.0013
Qual (showers) –2.0 0.060 –1.6 0.81
Qual (sunny) –1.41 0.17 –0.79 0.56
Significant variables in bold. Experience =number of years
pair observed together; Success =historical breeding success,
chicks fledged per breeding attempt; Stage =breeding stage,
incubation vs. brood guard; Age =offspring age; Outgoing
sex =sex of departing parent; Total allopreen time =total time
spent preening during display; Previous trip =duration of pre-
ceding foraging trip; Total display time =time from arrival of
incoming bird to cessation of pair interaction; qual =qualitative
weather.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
8N. Gillies et al.
may facilitate parental cooperation over care. For
incubating birds, the amount of time spent in dis-
play was negatively correlated with the duration of
the subsequent foraging trip, but was not related
to the duration of the foraging trip preceding the
changeover. This relationship might indicate that
this behaviour facilitates information transfer that
may relate to subsequent decisions about foraging
trip duration. Both parents directed bouts of allo-
preening of one-another, sometimes simultane-
ously, for variable amounts of time. The parent
returning from its foraging trip tended to initiate
allopreening both during the display and following
the switching of parents (‘changeover’) on the
nest. Furthermore, this incoming bird allopreened
its partner the most overall, though there was a
divide between the pre- and post-changeover peri-
ods: following changeover, the outgoing bird allo-
preened relatively more than its now-sitting
partner. Most allopreening focused on the head
and neck of the partner, areas that are inaccessible
during self-directed preening (autopreening). How-
ever, this did not seem to be specifically targeted
at ectoparasites, matching previous observational
accounts of allopreening in Black-browed Alba-
trosses (Tickell 1984).
As albatrosses are long-lived and highly socially
monogamous (Bried et al. 2003, Burg & Croxall
2006), pairs are expected to share a large propor-
tion of their reproductive output over their breed-
ing lifespan (Griffith 2019). Consequently, the
benefit to either bird of exploiting its partner by
reducing its own care, for example by taking an
excessively long foraging trip, is limited, as any
costs imposed on the partner are likely to be sub-
sequently shared with the foraging bird. Such costs
may be incurred either when the partner takes its
own long foraging trip, which in extremis could
lead to an increased risk of desertion (Weimer-
skirch 1995), or in future breeding attempts, if the
partner’s condition is reduced substantially. As
such, conflict between the parents is reduced, and
so optimal foraging trip duration is likely to reflect
a compromise between the needs of both parents,
as has been previously reported for Antarctic Pet-
rels Thalassoica antarctica (Tveraa et al. 1997).
However, establishing such a compromise requires
exchange of information between the two part-
ners.
Recent evidence suggests that nest-relief dis-
plays may facilitate such a process in other species.
In Common Guillemots, long nest-relief cere-
monies, which are largely made up of bouts of
allopreening, are associated with poor body condi-
tion of the incoming bird (Takahashi et al. 2017).
Conversely, Zebra Finches that are delayed in their
return to the nest engage in shorter changeover
duets with the partner and shorter subsequent for-
aging trips (Boucaud et al. 2016b). Nest-relief dis-
plays may serve a similar function in Black-browed
Figure 3. (a) Frequency of foraging trip durations for incubat-
ing (orange) and chick-brooding (blue) birds. Colours are
transparent to make all bars visible; darker colours indicate
overlapping bars. (b) Relationship between foraging trip dura-
tion (days) and offspring age (days) for incubating (orange)
and chick-brooding (blue) birds. Shaded areas give confidence
intervals.
Figure 4. Relationship between total display time (minutes)
and foraging trip duration (days) for incubating (orange) and
chick-brooding (blue) birds. Shaded area gives confidence
intervals.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
Allopreening in the Black-browed Albatross 9
Albatrosses, allowing the outgoing parent to decide
on its optimal foraging trip duration by assessing
the state of its partner. That most allopreening
observed was delivered by the incoming bird may
suggest that behavioural information, such as the
incoming partner’s ability or willingness to allo-
preen, is key to assessing partner state, as a physi-
cal assessment would probably be reflected in
more preening by the outgoing bird. Furthermore,
it is unclear how allopreening directed at the head
or neck would facilitate physical assessment of
condition; if this were the function, then it might
be more logical for the outgoing bird to focus on
the body of its partner, which might allow assess-
ment of, for example, fat reserves. Instead, allo-
preening by the incoming bird may be explained
as a mechanism of ‘reassurance’, whereby the
arriving bird signals to its partner a strong confir-
mation that it is motivated and able to take over
incubation duties, reducing the risk of egg aban-
donment and therefore nest failure. Through this,
the outgoing parent can make an assessment of its
partner’s commitment to engage in parental care.
This could additionally provide an explanation
for the fact that, following hatching, allopreening
of the chicks by either or both parents became a
common component of the nest-relief display.
Bouts of chick-directed allopreening were most
commonly observed by incoming birds, which
were reuniting with the chick (and partner). An
assessment function for allopreening might explain
this behaviour, which could in theory provide
information to displaying parents, for example by
indicating willingness of the allopreening bird to
engage in parental care. However, while the ten-
dency of incoming birds to preen the chick the
most during displays supports this, that parents
continued to allopreen when alone with the chick
means the evidence that this plays a role in display
is limited. Indeed, for brood-guarding birds, the
effect size of the relationship between foraging trip
duration and allopreening time was slightly posi-
tive, but small and not statistically significant. For-
aging trip durations were considerably shorter
during chick-rearing, a common strategy observed
in seabirds that can help to balance the costs of
commuting and the risks of chick starvation when
delivering food (Cuthill & Kacelnik 1990). This
may consequently mean less time is available to
the parents for display and, by extension, allo-
preening. Brood-guarding albatrosses experience
higher energetic expenditure than incubating
adults (Bevan et al. 1995), and so despite their
shorter spells on the nest they are probably subject
to similar constraints as during incubation. Fur-
thermore, if the returning adult arrives with little
food available for the chick, it is important that its
partner does not subsequently spend long at sea.
As such, trip duration may be more constrained
due to the competing demands of self-maintenance
and chick-provisioning, meaning that both ‘reassur-
ance’of a commitment to caring by the partner
and assessment of partner condition are probably
less important. Indeed, displays were considerably
shorter during chick-rearing than during incuba-
tion, suggesting limited value of an information
transfer function, if it exists.
An assessment function for allopreening during
incubation may explain the observed inverse rela-
tionship between display duration and the length
of the subsequent foraging trip. Long-lived species
are expected to prioritize future survival and
reproduction (Stearns 1992) and so outgoing par-
ents that are in poor condition would be expected
to make decisions that favour their own condition,
even at the expense of the current breeding
attempt. Consequently, such poor condition par-
ents might have less to gain from assessing the
condition of their partner and will spend less time
displaying so they can leave to forage more
quickly. These birds will subsequently spend more
time at sea while they replenish their lost mass
reserves. Conversely, sitting birds that are in good
condition are less constrained by this resource
trade-off and so might be less motivated to leave
the nest without strong persuasion from the part-
ner that it is ready to take over caring duties. This
might manifest in a longer period of display as the
incoming bird attempts to convince its partner to
exchange places on the nest, followed by a shorter
foraging trip as the departing parent does not need
to spend as much time at sea to regain mass.
Indeed, incubating, and to a lesser extent brood-
ing, adults were often observed to be extremely
reluctant to leave the nest, with changeovers occa-
sionally being initiated when the incoming bird
physically pushed its partner off the nest (in our
study, such behaviour was observed in 11 of 99
displays). Data on adult body condition were not
available in our study, but support for a condition-
dependent ‘persuasive’function for allopreening
may be seen in the finding that females tended to
allopreen more than males. Males are larger than
females (Ferrer et al. 2016) and probably in better
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
10 N. Gillies et al.
overall condition as they have not borne the cost
of producing the egg (Astheimer et al. 1985). Con-
sequently, they are more likely to be capable of
sustaining incubation for longer, which could man-
ifest in greater reluctance to leave the nest. Males
and females did not differ in their foraging trip
durations and so would be likely to experience dif-
ferential costs of incubating that could manifest in
such differences in motivation.
Besides behaviour, outgoing birds may make an
assessment of their partner using their well-devel-
oped olfactory sense, which is an important part of
the sensory system of seabirds (Hagelin et al.
2003, Nevitt 2008). Outgoing birds may use olfac-
tory cues gathered from the head and neck of their
partners to detect cues that may indicate foraging
success, such as the type or quality of food, and
therefore its probable condition. One hypothesis
for the functional significance of signal repetition is
that it serves to reduce error in the assessment of
the receiver (Enquist & Leimar 1983, Mowles &
Ord 2012). It is possible that the inverse correla-
tion between trip duration and total display time
observed here reflects the outgoing bird taking
longer to assess the partner when it is in poor con-
dition, and therefore soliciting further allopreening
from the partner. If the outgoing bird determines
that the partner is in a worse state than normal,
then this may encourage it to spend less time at
sea and thus to return and relieve its partner ear-
lier, reducing the risk of egg abandonment, which
condemns the breeding attempt to failure due to
predation in this species (Warham 1990, N. Gillies
pers. obs.). However, it is probable that if allo-
preening functioned in this way, more allopreening
would be observed by the outgoing bird. Further
research is needed to determine whether beha-
vioural or olfactory cues actually relate to body
condition, which would provide the necessary evi-
dence that such a role for allopreening could exist.
For parents visiting lone chicks, several minutes
of chick-directed allopreening were observed
before the parent either began brooding or com-
menced feeding. This may suggest chick allopreen-
ing has an alternative role in reunification,
evidence for which has been observed in primates,
where temporary separation of mothers and off-
spring leads to a subsequent increase in grooming
behaviour following reunion in a wide range of
species (Anderson & Chamove 1979, Gunnar et al.
1981, Taylor et al. 2015). However, the function
of this sort of behaviour is not clear, and further-
more, brood-guarding parents regularly preened
their chicks sporadically during the day, with no
obvious initiating cue. The functions of offspring-
directed allopreening in birds have not been well
explored. Possible functions include assessing chick
need to ensure optimal food delivery (Weimer-
skirch et al. 1997), reducing tick load (Bergstr€
om
et al. 1999), though the evidence for this in Black-
browed Albatrosses is limited (Tickell 1984; P.
Catry pers. comm.) or stress reduction (Taylor
et al. 2015). Future work should examine how
patterns of offspring-directed allopreening change
as the chick ages, whether allopreening reduces
measures of stress, and whether it correlates with
reduced tick load.
Finally, the total amount of allopreening
observed during the nest-relief display decreased
with each year that a pair had been observed
breeding together. In many bird species, reproduc-
tive success is seen to increase with duration of
the pair bond, even when controlling for possible
confounding variables such as age (Emslie et al.
1992, Pyle et al. 2001, van de Pol et al. 2006).
However, the mechanistic basis of this is not well
known. Earlier laying (van de Pol et al. 2006),
reduced time spent courting (Sanchez-Macouzet
et al. 2014) and improved behavioural coordina-
tion (Griggio & Hoi 2011) of more experienced
pairs have all been used to explain this improve-
ment in breeding success over successive years of
mating. It is possible that the reduced amount of
preening observed in more experienced pairs
reflects an improvement in the coordination of
care. For example, birds may take less time to
assess the condition of their partners with
increased experience, or require less stimulation to
leave the nest. However, the effect observed here
was small. If there is indeed no relationship, this
would suggest that ‘maintenance of the pair bond’,
which would be expected to precipitate some rela-
tionship between pair duration and allopreening,
would not be a satisfactory explanation for the
function of this behaviour. Further research is nec-
essary to determine whether the observed relation-
ship is real and, if so, what is its driver.
Alternatively, a relationship may exist between
allopreening and the amount of time parents
remain together in the future. To this end, future
studies could consider whether pairs that allopreen
more are less likely to divorce in subsequent years.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
Allopreening in the Black-browed Albatross 11
Our observations provide tentative evidence
that intra-pair displays between parent Black-bro-
wed Albatrosses, in which allopreening behaviour
is a key component, may facilitate cooperation
over parental care. Allopreening by incoming par-
ents may be a mechanism by which arriving birds
try to ‘convince’their partner to allow them to
take over parenting duties, or alternatively might
allow the departing parent to assess its partner’s
condition or success at sea, so it can adjust its for-
aging trip duration accordingly. To determine
which, if either, hypothesis is more likely, future
work should investigate how body condition of the
parents relates to the amount and patterns of allo-
preening observed. The phylogenetic distribution
of allopreening, as well as previous observations of
Black-browed Albatrosses (Tickell 1984), do not
support an ancestral role in plumage maintenance,
and so we do not suspect this to be its primary
role. However, we did not investigate this directly
and so further experimental work would be
needed to draw conclusions on the putative hygie-
nic or feather maintenance benefits of this beha-
viour. The function of other facets of the nest-
relief display not investigated here such as vocal-
ization and dance postures have not been
explored. These aspects of display may supple-
ment the reassurance or assessment functions of
allopreening suggested here, or may serve alto-
gether different purposes. Many aspects of the
nest-relief display incorporate elements seen also
in displays between newly forming pairs. Ulti-
mately, allopreening is likely to be multi-func-
tional; however, our findings suggest for the first
time that in this species, it may serve a cooperative
function.
This work received financial support from the Falkland
Islands Government (Environmental Studies Budget); by
FCT –Portugal through UIDB/04292/2020 and UIDP/
04292/2020, granted to MARE; and from the Biotech-
nology and Biological Sciences Research Council
(BBSRC) through grant BB/M011224/1. We thank the
New Island Conservation Trust for permitting and sup-
porting field studies on their reserve, and the South
Atlantic Environmental Research Institute (SAERI) for
logistical support. Finally, thanks go to Francesco Ven-
tura and Amanda Kuepfer for generous help in both the
field and the office, to OxNav members for helpful dis-
cussion, and to two anonymous referees and the Associ-
ate Editor, Ruedi Nager, for thoughtful comments and
suggestions on the manuscript.
AUTHOR CONTRIBUTION
Natasha Gillies: Conceptualization (lead); Formal
analysis (lead); Methodology (lead); Writing-origi-
nal draft (lead); Writing-review & editing (lead).
Tim Guilford: Conceptualization (equal); Formal
analysis (supporting); Methodology (equal); Writ-
ing-original draft (supporting); Writing-review &
editing (equal). Paulo Catry: Conceptualization
(equal); Formal analysis (supporting); Methodol-
ogy (equal); Writing-original draft (supporting);
Writing-review & editing (equal).
DISCLOSURE OF INTERESTS
None.
Data Availability Statement
The data that support the findings of this study
are available from the corresponding author upon
reasonable request.
REFERENCES
Anderson, J.R. & Chamove, A.S. 1979. Contact and
separation in adult monkeys. South Afr. J. Psychol. 9:49–
53.
Astheimer, L.B., Prince, P.A. & Grau, C.R. 1985. Egg
formation and the pre-laying period of Black-browed and
Grey-headed Albatrosses Diomedea melanophris and D.
chrysostoma at Bird Island, South Georgia. Ibis 127: 523–
529.
Aureli, F. & Yates, K. 2010. Distress prevention by grooming
others in Crested Black Macaques. Biol. Lett. 6:27–29.
Bates, D., M€
achler, M., Bolker, B.M. & Walker, S.C. 2015.
Fitting linear mixed-effects models using lme4. J. Stat.
Softw. 67:1–48.
Bergstr€
om, S., Haemig, P.D. & Olsen, B. 1999. Increased
mortality of Black-browed Albatross chicks at a colony
heavily-infested with the tick Ixodes uriae.Int. J. Parasitol.
29: 1359–1361.
Bevan, R.M., Butler, P.J., Woakes, A.J. & Prince, E.A.
1995. The energy expenditure of free-ranging Black-browed
Albatrosses. Philos. Trans. R. Soc. B Biol. Sci. 350: 119–
131.
Birkhead, T.R. 1978. Behavioural adaptations to high density
nesting in the Common Guillemot Uria aalge.Anim. Behav.
26: 321–331.
Boucaud, I.C.A., Aguirre Smith, M.L.N., Val
ere, P.A. &
Vignal, C. 2016a. Incubating females signal their needs
during intrapair vocal communication at the nest: a feeding
experiment in Great Tits. Anim. Behav. 122:77–86.
Boucaud, I.C.A., Mariette, M.M., Villain, A.S. & Vignal, C.
2016b. Vocal negotiation over parental care? Acoustic
communication at the nest predicts partners’incubation
share. Biol. J. Linn. Soc. 117: 322–336.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
12 N. Gillies et al.
Bried, J., Pontier, D. & Jouventin, P. 2003. Mate fidelity in
monogamous birds: a re-examination of the
Procellariiformes. Anim. Behav. 65: 235–246.
Brooke, M. 1985. The effect of allopreening on tick burdens of
molting eudyptid penguins. Auk 102: 893–895.
Burg, T.M. & Croxall, J.P. 2006. Extrapair paternities in
Black-browed Thalassarche melanophris, Grey-headed T.
chrysostoma and Wandering Albatrosses Diomedea exulans
at South Georgia. J. Avian Biol. 37: 331–338.
Catry, P., Lemos, R.T., Brickle, P., Phillips, R.A., Matias, R.
& Granadeiro, J.P. 2013. Predicting the distribution of a
threatened albatross: The importance of competition,
fisheries and annual variability. Prog. Oceanogr. 110:1–10.
Clayton, D.H. 1991. Coevolution of avian grooming and
ectoparasite avoidance. In Loye, J.E. & Zuk, M. (eds) Bird–
parasite Interactions: 258–290. Oxford: Oxford University
Press.
Cuthill, I. & Kacelnik, A. 1990. Central place foraging: a
reappraisal of the ‘loading effect’.Anim. Behav. 40: 1087–
1101.
Drummond, H., Calder
on-De Anda, M., Perez, C. & Stamps,
J. 2002. Collaborative tactics for nestsite selection by pairs
of Blue footed Boobies. Behaviour 139: 1383–1412.
Dunbar, R.I.M. 1991. Functional significance of social
grooming in primates. Folia Primatol. 57: 121–131.
Elie, J.E., Mariette, M.M., Soula, H.A., Griffith, S.C.,
Mathevon, N. & Vignal, C. 2010. Vocal communication at
the nest between mates in wild Zebra Finches: a private
vocal duet? Anim. Behav. 80: 597–605.
Emslie, S.D., Sydeman, W.J. & Pyle, P. 1992. The
importance of mate retention and experience on breeding
success in Cassin’s Auklet (Ptychoramphus aleuticus).
Behav. Ecol. 3: 189–195.
Enquist, M. & Leimar, O. 1983. Evolution of fighting
behaviour: Decision rules and assessment of relative
strength. J. Theor. Biol. 102: 387–410.
Feh, C. & de Mazier
es, J. 1993. Grooming at a preferred site
reduces heart rate in horses. Anim. Behav. 46: 1191–1194.
Fern
andez-L
opez, J. & Schliep, K. 2019. rWind: download,
edit and include wind data in ecological and evolutionary
analysis. Ecography 42: 804–810.
Ferrer, M., Morandini, V., Perry, L. & Bechard, M. 2016. Sex
determination by morphological measurements of Black-
browed Albatrosses (Thalassarche melanophrys) Using
discriminant analysis. Waterbirds 39: 295–299.
Fridolfsson, A.-K. & Ellegren, H. 1999. A simple and
universal method for molecular sexing of non-ratite birds. J.
Avian Biol. 30: 116.
Gill, S.A. 2012. Strategic use of allopreening in family-living
wrens. Behav. Ecol. Sociobiol. 66: 757–763.
Granadeiro, J.P., Campioni, L. & Catry, P. 2018.
Albatrosses bathe before departing on a foraging trip:
implications for risk assessments and marine spatial
planning. Bird Conserv. Int. 28: 208–215.
Griffith, S.C. 2019. Cooperation and coordination in socially
monogamous birds: moving away from a focus on sexual
conflict. Front. Ecol. Evol. 7: https://doi.org/10.3389/fevo.
2019.00455
Griggio, M. & Hoi, H. 2011. An experiment on the function of
the long-term pair bond period in the socially monogamous
Bearded Reedling. Anim. Behav. 82: 1329–1335.
Guilford, T., Meade, J., Freeman, R., Biro, D., Evans, T.,
Bonadonna, F., Boyle, D., Roberts, S. & Perrins, C.M.
2008. GPS tracking of the foraging movements of Manx
Shearwaters Puffinus puffinus breeding on Skomer Island,
Wales. Ibis 150: 462–473.
Gunnar, M.R., Gonzalez, C.A., Goodlin, B.L. & Levine, S.
1981. Behavioral and pituitary-adrenal responses during a
prolonged separation period in infant Rhesus macaques.
Psychoneuroendocrinology 6:65–75.
Hagelin, J.C., Jones, I.L. & Rasmussen, L.E.L. 2003. A
tangerine-scented social odour in a monogamous seabird.
Proc. R. Soc. Lond. Ser. B Biol. Sci. 270: 1323–1329.
Harrison, A.C.J.O. 1965. Allopreening as agonistic behaviour.
Behaviour 24: 161–209.
Huxley, J.S. 1914. 33. The courtship-habits of the Great
Crested Grebe (Podiceps cristatus); with an addition to the
Theory of Sexual Selection. Proc. Zool. Soc. Lond. 84: 491–
562.
Kenny, E., Birkhead, T.R. & Green, J.P. 2017. Allopreening
in birds is associated with parental cooperation over
offspring care and stable pair bonds across years. Behav.
Ecol. 28: 1142–1148.
Keverne, E.B., Martensz, N.D. & Tuite, B. 1989. Beta-
endorphin concentrations in cerebrospinal fluid of monkeys
are influenced by grooming relationships.
Psychoneuroendocrinology 14: 155–161.
Kober, K. & Gaston, A.J. 2003. Social interactions among
breeding Br€
unnich’s Guillemots Uria lomvia suggest
constraints in relation to offspring vulnerability. Ibis 145:
413–418.
Lanctot, R.B., Sandercock, B.K. & Kempenaers, B. 2000.
Do male breeding displays function to attract mates or
defend territories? The explanatory role of mate and site
fidelity. Waterbirds 23: 155–164.
Lenth, R., Singmann, H., Love, J., Buerkner, P. & Herve, M.
2018. Package ’emmeans’. https://github.com/rvlenth/emmea
ns.
Lewis, S., Roberts, G., Harris, M.P., Prigmore, C. &
Wanless, S. 2007. Fitness increases with partner and
neighbour allopreening. Biol. Lett. 3: 386–389.
Mariette, M.M. & Griffith, S.C. 2015. The adaptive
significance of provisioning and foraging coordination
between breeding partners. Am. Nat. 185: 270–280.
Miyazawa, E., Seguchi, A., Takahashi, N., Motai, A. &
Izawa, E.I. 2020. Different patterns of allopreening in the
same-sex and opposite-sex interactions of juvenile Large-
billed Crows (Corvus macrorhynchos). Ethology 126: 195–
206.
Morales Picard, A., Mundry, R., Auersperg, A.M., Boeving,
E.R., Boucherie, P.H., Bugnyar, T., Dufour, V., Emery,
N.J., Federspiel, I.G., Gajdon, G.K., Gu
ery, J., Hegedi
c,
M., Horn, L., Kavanagh, E., Lambert, M.L., Massen,
J.J.M., Rodrigues, M.A., Schiestl, M., Schwing, R.,
Szabo, B., Taylor, A.H., Horik, J.O., Bayern, A.M.P.,
Seed, A. & Slocombe, K.E. 2020. Why preen others?
Predictors of allopreening in parrots and corvids and
comparisons to grooming in great apes. Ethology 126: 207–
228.
Mowles, S.L. & Ord, T.J. 2012. Repetitive signals and mate
choice: Insights from contest theory. Anim. Behav. 84: 295–
304.
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
Allopreening in the Black-browed Albatross 13
Nevitt, G.A. 2008. Sensory ecology on the high seas: The
odor world of the procellariiform seabirds. J. Exp. Biol. 211:
1706–1713.
Paiva, V.H., Guilford, T., Meade, J., Geraldes, P., Ramos,
J.A. & Garthe, S. 2010. Flight dynamics of Cory’s
Shearwater foraging in a coastal environment. Zoology 113:
47–56.
Pennycuick, C.J. 2002. Gust soaring as a basis for the flight
of petrels and albatrosses (Procellariiformes). Avian Sci. 2:
1–12.
Perrot, C., B
echet, A., Hanzen, C., Arnaud, A., Pradel, R. &
C
ezilly, F. 2016. Sexual display complexity varies non-
linearly with age and predicts breeding status in greater
flamingos. Sci. Rep. 6:1–10.
Pilakouta, N., Hanlon, E.J.H. & Smiseth, P.T. 2018.
Biparental care is more than the sum of its parts:
experimental evidence for synergistic effects on offspring
fitness. Proc. R. Soc. B Biol. Sci. 285: 20180875.
Pyle, P., Sydeman, W.J. & Hester, M. 2001. Effects of age,
breeding experience, mate fidelity and site fidelity on
breeding performance in a declining population of Cassin’s
Auklets. J. Anim. Ecol. 70: 1088–1097.
R Core Team 2018. R: A Language and Environment for
Statistical Computing. Vienna: R Foundation for Statistical
Computing.
Sachs, G. 2004. Minimum shear wind strength required for
dynamic soaring of albatrosses. Ibis 147:1–10.
Sanchez-Macouzet, O., Rodriguez, C. & Drummond, H.
2014. Better stay together: pair bond duration increases
individual fitness independent of age-related variation. Proc.
R. Soc. B Biol. Sci. 281: 20132843.
Schino, G., Scucchi, S., Maestripieri, D. & Turillazzi, P.G.
1988. Allogrooming as a tension-reduction mechanism: A
behavioral approach. Am. J. Primatol. 16:43–50.
Stearns, S.C. (1992). The Evolution of Life Histories. Oxford:
Oxford University Press.
St€
owe, M., Bugnyar, T., Schloegl, C., Heinrich, B.,
Kotrschal, K. & M€
ostl, E. 2008. Corticosterone excretion
patterns and affiliative behavior over development in Ravens
(Corvus corax). Horm. Behav. 53: 208–216.
Takahashi, L.S., Storey, A.E., Wilhelm, S.I. & Walsh, C.J.
2017. Turn-taking ceremonies in a colonial seabird: Does
behavioral variation signal individual condition? Auk 134:
530–541.
Taylor, J.H., Mustoe, A.C., Hochfelder, B. & French, J.A.
2015. Reunion behavior after social separation is associated
with enhanced HPA recovery in young marmoset monkeys.
Psychoneuroendocrinology 57:93–101.
Tickell, W.L.N. 1984. Behaviour of Blackbrowed and
Greyheaded Albatrosses at Bird Island, South Georgia.
Ostrich 55:64–85.
Tickell, W.L.N. 2000. Albatrosses. New Haven: Yale
University Press.
Tveraa, T., Lorensten, S.-H. & Sæther, B.-E. 1997.
Regulation of foraging trips and costs of incubation shifts in
the Antarctic petrel (Thalassoica antarctica). Behav. Ecol. 8:
465–469.
van de Pol, M., Heg, D., Bruinzeel, L.W., Kuijper, B. &
Verhulst, S. 2006. Experimental evidence for a causal
effect of pair-bond duration on reproductive performance in
Oystercatchers (Haematopus ostralegus). Behav. Ecol. 17:
982–991.
Ventura, F., Granadeiro, J.P., Padget, O. & Catry, P. 2020.
Gadfly Petrels use knowledge of the windscape, not
memorized foraging patches, to optimize foraging trips on
ocean-wide scales. Proc. R. Soc. B Biol. Sci. 287:
20191775.
Villa, S.M., Goodman, G.B., Ruff, J.S. & Clayton, D.H. 2016.
Does allopreening control avian ectoparasites? Biol. Lett.
12: 20160362.
Wachtmeister, C.-A. 2001. Display in monogamous pairs: a
review of empirical data and evolutionary explanations.
Anim. Behav. 61: 861–868.
Wakefield, E.D., Phillips, R.A., Jason, M., Akira, F.,
Hiroyoshi, H., Marshall, G.J. & Trathan, P.N. 2009. Wind
field and sex constrain the flight speeds of central-place
foraging albatrosses. Ecol. Monogr. 79: 663–679.
Warham, J. 1990. The Petrels: Their Ecology and Breeding
Systems. Cambridge, MA: Academic Press Ltd.
Weimerskirch, H. 1995. Regulation of foraging trips and
incubation routine in male and female Wandering
Albatrosses. Oecologia 102:37–43.
Weimerskirch, H., Chastel, O., Ackermann, L., Chaurand,
T., Cuenot-Chaillet, F., Hindermeyer, X. & Judas, J. 1994.
Alternate long and short foraging trips in pelagic seabird
parents. Anim. Behav. 47: 472–476.
Weimerskirch, H., Mougey, T. & Hindermeyer, X. 1997.
Foraging and provisioning strategies of Black-browed
Albatrosses in relation to the requirements of the chick:
natural variation and experimental study. Behav. Ecol. 8:
635–643.
Zolnierowicz, K.M., Nyklova-Ondrova, M. & Tobolka, M.
2016. Sex differences in preening behaviour in the White
Stork Ciconia ciconia.Polish J. Ecol. 64: 431–435.
Received 10 December 2020;
revision accepted 11 April 2021.
Associate Editor: Rosemarie Kentie
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British Ornithologists’Union.
14 N. Gillies et al.
