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Allopreening in the Black‐browed Albatross (Thalassarche melanophris): an exploration of patterns and possible functions


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The functions of display between breeding pairs of animals have been given little attention 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 little 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 partner retention and biparental care, and it appears to be functional in maintaining cooperation 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 displays 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 parents. Although we cannot be conclusive as to its exact functions, we add to a limited literature the first exploration of functions for this conspicuous behaviour in albatrosses.
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Allopreening in the Black-browed Albatross
(Thalassarche melanophris): an exploration of
patterns and possible functions
Department of Zoology, University of Oxford, Oxford, UK
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 rst exploration of functions for this conspicuous behaviour in albatrosses.
Keywords: display, foraging, negotiation, parental care.
Despite more than a hundred years having passed
since Huxleysrst 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
(Grifth 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 Huxleys 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.
Twitter: @tash_gillies
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British OrnithologistsUnion.
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
(Grifth 2019). Consequently, parents may benet
from coordinating their behaviour to maximize the
benet to cost ratio of providing care from the
perspective of both parents (Mariette & Grifth
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-
ingdisplays (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
unnichs 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 rst 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 OrnithologistsUnion.
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 eld 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
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 (Grifth 2019). Specically, 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 planningof for-
aging trip duration has been reported for Manx
Shearwaters Pufnus pufnus (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 rst 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, parentswill-
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.
Study site
This study was carried out on New Island, Falk-
land Islands (51°4332’’S, 61°1755’’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 6871 and 120130 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 identication at a distance. The sex of
birds had been previously identied through the
observation of sex-specic 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 OrnithologistsUnion.
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.
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 ight 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 12 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 identied 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:
0.16.3 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.
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 ve 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 (Wakeeld
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 ight 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
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 OrnithologistsUnion.
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,showersor 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 tted 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 xed effects of sex,
age and breeding experience (in years), which we
identied as factors possibly inuencing beha-
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 inuenced the
amount of time they engaged in allopreening, we
tted 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 xed
effects of position(incoming vs. outgoing bird)
and timing(pre- or post-changeover).
Total allopreening timewas 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 edged per
breeding attempt) or sex of the outgoing bird by
tting an LMM (Table 1, Model 2) that included
these variables as xed 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
Response Fixed Random
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
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 incomingor outgoingfrom 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 edged 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 OrnithologistsUnion.
Allopreening in the Black-browed Albatross 5
provisioning, we additionally included breeding
stageas a xed effect. Finally, we included total
display time (in minutes) as a controlling variable,
as this dictates the amount of time available for
We investigated whether and which factors pre-
dicted the number of chick-directed allopreening
bouts instigated by each parent. We tted 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 timeas a xed
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 rst tted 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 xed 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 tted 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 xed effect of previous trip duration. Finally,
environmental conditions are known to affect for-
aging trip duration in Black-browed Albatrosses
(Wakeeld et al. 2009). To control for this, we
included the environmental variables of crosswind,
headwind and qualitative weather (see Methods,
Environmental data).
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: 3101 min). In the single
nest relief that did not involve display, the sitting
bird left the nest immediately following its part-
ners 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
0.2679.33%). 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 specically; parasites visible
by an observer at a distance of 12 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 rst in 64% of displays,
the outgoing bird resumed in 28% of displays, and
both birds simultaneously resumed in 8% of dis-
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
=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 OrnithologistsUnion.
6N. Gillies et al.
(female: 2.97 0.63%, male: 1.26 0.28%;
=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
=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 signi-
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 jitteredhorizontally for readability.
Figure 2. Total time spent preening by both parents in sec-
onds according to pair breeding experience (years). Shaded
area gives condence intervals.
Table 2. Test statistics and coefcient coordinates from a like-
lihood ratio test on LMM estimating predictors of total allo-
preening time (seconds).
Variable v
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
Signicant variables in bold. Experience =number of years
pair observed together; Success =historical breeding success,
chicks edged 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 OrnithologistsUnion.
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 =8.518.4%).
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 signicantly 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 signicant 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
signicantly 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).
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 coefcient coordinates from a like-
lihood ratio test to investigate the signicance of xed effects
on the number of chick-directed allopreening bouts.
Variable v
df P-value Estimate se
Experience 1.23 1 0.26 0.052 0.048
106.49 1 <0.0001 5.36 0.49
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
Signicant 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 coefcient coordinates from
ANOVA to investigate the signicance of xed 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
Signicant variables in bold. Experience =years pair
observed breeding together; Success =historical breeding
success, chicks edged 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 coefcient coordinates from
ANOVA to investigate the signicance of xed 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
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
Signicant variables in bold. Experience =number of years
pair observed together; Success =historical breeding success,
chicks edged 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
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British OrnithologistsUnion.
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 specically 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 (Grifth 2019). Consequently, the
benet 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
partners condition is reduced substantially. As
such, conict between the parents is reduced, and
so optimal foraging trip duration is likely to reect
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-
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 condence
Figure 4. Relationship between total display time (minutes)
and foraging trip duration (days) for incubating (orange) and
chick-brooding (blue) birds. Shaded area gives condence
© 2021 The Authors. Ibis published by John Wiley & Sons Ltd on behalf of British OrnithologistsUnion.
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 partners ability or willingness to allo-
preen, is key to assessing partner state, as a physi-
cal assessment would probably be reected 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 conr-
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
partners 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 signicant. 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-
anceof 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 persuasivefunction for allopreening
may be seen in the nding 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 OrnithologistsUnion.
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 signicance 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 reects 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 reunication,
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
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
reects 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 OrnithologistsUnion.
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 convincetheir partner to allow them to
take over parenting duties, or alternatively might
allow the departing parent to assess its partners
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 benets 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 ndings suggest for the rst
time that in this species, it may serve a cooperative
This work received nancial 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 eld 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
eld and the ofce, 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.
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).
Data Availability Statement
The data that support the ndings of this study
are available from the corresponding author upon
reasonable request.
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Received 10 December 2020;
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Associate Editor: Rosemarie Kentie
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14 N. Gillies et al.
... Perhaps because of the need to communicate, the returning parent took longer to start incubation when it approached the nest when its partner was still incubating than when the partner had already left for its incubation recess, i.e. when the nest was empty (Fig. 2). The intense vocalizations during nest relief may play a role in communication, and may be similar to the more elaborate nest relief rituals, including allopreening, observed in other avian species (Glutz von Blotzheim 1999, Wachtmeister 2001, Deeming 2002b, Rodewald 2015, Kenny et al. 2017, Gillies et al. 2021. ...
... Perhaps such vocalizations honestly signal the incubating bird's needs, as suggested by both observations and experiments in some uniparentally incubating females, which show that females signal to their mate their need to be fed (Boucaud et al. 2016b, 2016c, reviewed in Amy et al. 2018. Vocalizations during nest reliefs, along with other aspects of nest relief rituals, such as allopreening (Gillies et al. 2021), may be crucial for coordination of parental care (Griffith 2019). ...
In species with biparental care, coordination of parental behaviour between pair members increases reproductive success. Coordination is difficult if opportunities to communicate are scarce, which might have led to the evolution of elaborate nest relief rituals in species facing a low predation risk. However, whether such conspicuous rituals also evolved in species that avoid predation by relying on crypsis remains unclear. Here, we used a continuous monitoring‐system to describe nest relief behaviour during incubation in an Arctic‐breeding shorebird with passive nest defence, the Semipalmated Sandpiper Calidris pusilla. We also explored whether behaviour of exchanging parents informs about parental coordination and predicts incubation effort. We found that incubating parents vocalized twice as much before the arrival of their partner than during other times of incubation. In at least 75% of exchanges, the incubating parent left the nest only after its partner had returned and initiated the nest relief. In these cases, exchanges were quick (25 s, median) and shortened over the incubation period by 0.1–1.4 s/day (95%CI), suggesting that parents became more synchronized. However, nest reliefs were not cryptic. In 90% of exchanges, at least one parent vocalized, and in 20% of nest reliefs the incubating parent left the nest only after its returning partner called incessantly. In 27% of cases, the returning parent initiated the nest relief with a call; in 39% of these cases, the incubating partner replied. If the partner replied, its following off‐nest bout was 1–4 hr (95%CI) longer than when the partner did not reply, which corresponds to an 8–45% increase. Our results indicate that incubating Semipalmated Sandpipers, which rely on crypsis to avoid nest predation, have quick but acoustically conspicuous nest reliefs. Our results also suggest that vocalizations during nest reliefs may be important for the coordination and division of parental duties.
... On the one hand, allopreening improves birds' plumage condition by reducing ectoparasites (Brooke, 1985;Villa et al., 2016). On the other hand, allopreening maintains pair bonds between mated pairs (Gill, 2012;Kenny et al., 2017), improves cooperation during parental care (Gillies et al., 2021;Takahashi et al., 2017), and reduces aggression between conspecifics (Lewis et al., 2007;Radford & Du Plessis, 2006). The hygienic and social benefits are not mutually exclusive (Kober & Gaston, 2003;Radford & Du Plessis, 2006). ...
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Allopreening occurs in many species of birds and is known for providing hygienic and social benefits. While this behavior has been extensively studied among conspecifics, its occurrence among different species remains little known. Outside of captive environments, only a few records of interspecific allopreening exist. In this study, we describe our observations of the interspecific allopreening behavior between Spot-necked (Stachyris strialata) and Nonggang Babblers (S. nonggangensis) in a non-captive environment in southern China. To our knowledge, these observations represent the first record of interspecific allopreening in the family Timaliidae. We suggest that this understudied behavior is most likely related to the dominant–subordinate relationship between these two species: either the dominant species preening the subordinate species to assert dominance or the subordinate species preening the dominant species to reduce tensions by appeasement. We also suggest interspecific allopreening may not be as rare as we thought if we study this behavior under circumstances where different species are close to each other. This study contributes to our understanding of not only the potential mechanism(s) behind interspecific allopreening but also the behavioral ecology of the vulnerable Nonggang Babbler.
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Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in maintaining strong affiliative bonds between group members, which in turn, underpin the emergence of cooperative behavior. In contrast, although allopreening occurs in many avian species, we know little about its social functions. Our study addresses this issue by investigating allopreening in a broad comparative data set including six corvid and nine parrot species. We assessed whether rates of allopreening initiations, proportion of time spent allopreening, and the number of grooming partners in captive group‐housed birds were comparable to patterns observed in captive chimpanzees and bonobos. While parrots and corvids were found to have similar rates of social grooming to bonobos and chimpanzees, Pan species dedicated significantly more time to social grooming. Animals in larger groups had more grooming partners, but when controlling for the number of potential partners, birds tended to have fewer grooming interaction partners than Pan species. We then investigated whether allopreening in parrots and corvids was predicted by behavioral markers of affiliative social bonds (close physical proximity, active feeding, and low levels of agonistic behavior). Results revealed that providing allopreening to a partner was significantly predicted by often being in close proximity, but not engagement in active feeding or agonistic behavior. We examined the region allopreened in a subset of species and found that preening a partner's head was predicted by both close physical proximity and active feeding, while body allopreening was only predicted by close physical proximity. Head preening may confer more hygienic benefits to recipients, and thus, may be more selectively provided to valued partners. Results support the hypothesis that allopreening in corvids and parrots helps maintain social bonds with an individual's most important social partners, showing some similarities to allogrooming in primates. Parrots and corvids were more likely to allopreen partners that they chose to maintain close physical proximity with. When examining the region allopreened, we found that preening a partner's head was predicted by frequent close proximity and active feeding, indicating this might be a more valuable service reserved for highly valued social partners. Compared to Pan species, parrots and corvids initiated grooming bouts at similar rates, but invested less time in grooming and engaged with fewer partners. The figure illustrates the probability of dyadic allopreening being observed within a given dyad, as a function of their proximity score. Data illustrated derives from the model testing if occurrence of allopreening in a dyad could be predicted by proximity and active feeding (N = 118 individuals from nine species). Each dot shows the average probability per bin of the proximity score, whereby the area of the dots depicts the number of dyads per dot (N = 1 to 1,005). The dashed and dotted lines depict the fitted model and its confidence interval (with all other predictors in the model being at their average and assuming an observation effort of 4 hr, which roughly equals the average observation effort). Allopreening was more likely to occur in dyads that spent a higher proportion of their time in close physical proximity.
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Allogrooming, where an individual grooms another, has been extensively studied in various social animals to understand its role in the evolution of cooperation/proso-ciality. In existing studies in mammals, allogrooming has been suggested to exhibit not only a hygiene but also a social function. Allopreening, a topic of increasing interest in mammals but recently also in birds, has been studied mostly with mature animals. However, in some species immature individuals also show allopreening and its function remains poorly understood. Crows, Corvus spp., are an ideal model to study this phenomenon, because juveniles form year-round aggregates during their long juvenile stage (e.g., throughout 3-4 years). Here, we investigated the function of allopreening in juvenile groups of wild-caught large-billed crows (C. macrorhynchos). Allopreening frequency and duration for three groups of wild-caught juveniles were analysed to determine whether there was a symmetrical (i.e., reciprocal) or asymmetrical allopreening pattern, and if sex composition of the dyad and/or relative dominance of donor and recipient had an effect. We found that both the frequency and duration of male allopreening correlated with frequency of aggression. Allopreening between both males and females occurred unidirectionally from dominants to subordinates but not in the opposite direction. On the contrary, allopreening between a male and a female was found to be reciprocated, though the absolute frequency and duration were both greater in males than in females. These results suggest that the social function of allopreening in juvenile crows differs depending on the sex composition of the dyad, functioning as a dominance signal for same-sex dyads, and serving a social bonding function for opposite-sex dyads. These findings may reflect the potentially crucial roles of allopreening in within-sex competition and opposite-sex attraction during the 3 year-long juvenile stage affecting future mate choice in lifelong monogamy.
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Socially monogamous birds have provided a major focus of research in the field of sexual selection, providing insight into the evolution of ornaments, sexual dimorphism and sex roles. Following important theoretical work in the 1970's, there has been a continued emphasis on elements of the sexual conflict between socially monogamous partners. The application of molecular tools enabled a significant research investment into the conflict over paternity. The differential allocation hypothesis, has been another well-worked area, focusing attention on the conflict over investment with a current or future partner, and being at the forefront of high-profile work on maternal effects. Whilst the conflict between the sexes has been a fascinating area of evolutionary biology over the past four decades, I will argue that the level of conflict between partners is often overstated, and our understanding of social monogamy is biased by taking the perspective of conflict rather than cooperation. For example, differential allocation in socially monogamous birds can be explained from an entirely cooperative perspective, as can much behavior that is currently associated with sperm competition and the conflict over paternity. With over 80% of avian species forming socially monogamous bonds that are often life-long and can last for many decades, we need to redress the balance, and focus more attention on the benefits that both males and females gain from establishing, and maintaining socially monogamous partnerships. I highlight behavioral and morphological adaptations that feature strongly in socially monogamous birds, and that are deserving of more attention from the perspective of the high level of inter-individual cooperation and coordination that undoubtedly exists in many species. Whilst the focus of research has begun to shift recently, it will take many years to redress the bias toward sexual conflict that has taken the major share of empirical attention to this point.
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1. Wind connectivity has been identified as a key factor driving many biological processes. 2. Existing software available for managing wind data are often overly complex for studying many ecological processes and cannot be incorporated into a broad framework. 3. Here we present rWind, an R langauge package to download and manage surface wind data from the Global Forecasting System and to compute wind connectivity between locations. 4. Data obtained with rWind can be used in a general framework for analysis of biological processes to develop hypotheses about the role of wind in driving ecological and evolutionary patterns. This article is protected by copyright. All rights reserved.
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Despite an extensive body of theoretical and empirical literature on biparental cooperation, it is still unclear whether offspring fare equally, better or worse when receiving care by two parents versus a single parent. Some models predict that parents should withhold the amount of care they provide due to sexual conflict, thereby shifting as much of the workload as possible to their partner. This conflict should lead to offspring faring worse with two parents. Yet, other models predict that when parents care for their offspring together, their individual contributions can have synergistic (more than additive) effects on offspring fitness. Under this scenario, biparental cooperation should lead to offspring faring better with two parents. We address this fundamental question using a unique experimental design where we compared offspring fitness when the two parents worked together (biparental treatment) and when they worked separately (uniparental treatment), while keeping constant the amount of resources and number of offspring per parent across treatments. This made it possible to directly compare the biparental treatment to the sum of the male and female contributions in the uniparental treatment. Our main finding was that offspring grew larger and were more likely to survive to adulthood when reared by both parents than a single parent. This is the first empirical evidence for a synergistic effect of biparental cooperation on offspring fitness and could provide novel insights into the conditions favouring the evolution of biparental cooperation.
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Individuals of many species form bonds with their breeding partners, yet the mechanisms maintaining these bonds are poorly understood. In birds, allopreening is a conspicuous feature of interactions between breeding partners and has been hypothesized to play a role in strengthening and maintaining pair bonds within and across breeding attempts. Many avian species, however, do not allopreen and the relationship between allopreening and pair bonding across species remains unexplored. In a comparative analysis of allopreening and pair bond behavior, we found that allopreening between breeding partners was more common among species where parents cooperate to rear offspring. The occurrence of allopreening was also associated with an increased likelihood that partners would remain together over successive breeding seasons. However, there was no strong evidence for an association between allopreening and sexual fidelity within seasons or time spent together outside the breeding season. Allopreening between partners was also no more common in colonial or cooperatively breeding species than in solitary species. Analyses of evolutionary transitions indicated that allopreening evolved from an ancestral state of either high parental cooperation or high partner retention, and we discuss possible explanations for this. Overall, our results are consistent with an important role for allopreening in the maintenance of avian pair bonds.
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In species with biparental care, pairs share a cooperative interest in offspring survival but may be in conflict over their relative investments, as reported in recent turn-taking studies of chick-provisioning birds. Turn-taking in Common Murres (Uria aalge) involves the foraging bird returning to the colony to provision the chick and the brooding parent departing. We examined whether Common Murres in poor condition had slower or more irregular turn-taking behavior, as has been documented in Common Murres equipped with geologgers. Irregularities include the brooding bird not trading parental roles with its returning mate or a bird returning to the colony without a fish. Irregular turn-taking sequences generally took longer than normal turn-taking sequences and differed in the rate and synchrony of allopreening, the main interactive behavior between mates. There was a delayed onset of allopreening when nest reliefs were protracted, whereas returners that did not bring a fish started allopreening sooner than either their brooding partners or other returners that brought a fish. Common Murres in better condition (higher body mass and lower lipid metabolite levels) left the colony sooner after their returning mates fed the chick compared to Common Murres in worse condition. Birds with higher chick-feeding rates brought fish back in more visits, which suggests that these were higher-quality birds. When birds vary in their turn-taking ceremonial behaviors, they may be negotiating by providing their partners with cues about their condition. Since Common Murres have long-term pair bonds and both parents are necessary to raise offspring, mates should respond to information from their partners if they can do so without compromising their own condition beyond a critical threshold.
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Tracking studies of seabirds have generally focused in identifying areas used for foraging, in the hope of highlighting regions of energy transfer which may be important for seabird and general ecosystem conservation and special management. However, some sea areas may serve functions other than providing nutritional resources, which may be equally relevant, particularly if used by large numbers of individuals. In this paper, based on a study of 4 breeding colonies in the Falkland Islands and on 314 individuals tracked, we show that virtually all (97.8%) black-browed albatrosses Thalassarche melanophris (BBA) bathe in the close vicinity of the colony, remaining in the area for nearly an hour, before departing on a foraging trip. This compares with only 20 to 40% of the individuals landing close to the colony at the end of a foraging trip. The observed utilization of marine areas by BBA in a radius of 1 to 5 km around the nesting colony is one order of magnitude higher than elsewhere, including foraging hotspots. Clearly, even long-range flying birds such as albatrosses can make an intensive use of the sea-surface in the immediate vicinity of the colonies, and therefore any threats to seabirds in these areas (disturbance, pollutants, collision with artificial structures and light attraction) can potentially have a major impact at the population level. As such, the close neighbourhood of seabird colonies are potentially highly sensitive areas, and this needs to be taken into account when carrying out risk assessments or during marine spatial planning exercises.
Seabirds must often travel vast distances to exploit heterogeneously distributed oceanic resources, but how routes and destinations of foraging trips are optimized remains poorly understood. Among the seabirds, gadfly petrels (Pterodroma spp.) are supremely adapted for making efficient use of wind energy in dynamic soaring flight. We used GPS tracking data to investigate the role of wind in the flight behaviour and foraging strategy of the Desertas petrel, Pterodroma deserta. We found that rather than visiting foraging hotspots, Desertas petrels maximize prey encounter by covering some of the longest distances known in any animal in a single foraging trip (up to 12 000 km) over deep, pelagic waters. Petrels flew with consistent crosswind (relative wind angle 60°), close to that which maximizes their groundspeed. By combining state-space modelling with a series of comparisons to simulated foraging trips (reshuffled-random, rotated, time-shifted, reversed), we show that this resulted in trajectories that were close to the fastest possible, given the location and time. This wind use is thus consistent both with birds using current winds to fine-tune their routes and, impressively, with an a priori knowledge of predictable regional-scale wind regimes, facilitating efficient flight over great distances before returning to the home colony.