Sex differences in razorbill Alca torda parentoffspring vocal recognition
1
Hubbs-SeaWorld Research Institute, 2595 Ingraham Street, San Diego, CA
92109, USA
2
Department of Biology, Memorial University of Newfoundland, St Johns,
Newfoundland, Canada A1B 3X9
* Author for correspondence (e-mail: sinsley{at}hswri.org)
Accepted 15 October 2002
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Summary |
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Key words: razorbill, Alca torda, parentoffspring vocal recognition, sex difference, behaviour, monogamous, seabird, auk, Alcidae
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Introduction |
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The auk family is a diverse group of long-lived and socially monogamous
seabirds that exhibit a high degree of natal philopatry and a variety of chick
developmental patterns (Bédard,
1985; Strauch,
1985
; Freison et al., 1996;
Gaston and Jones, 1998
). Most
species are very social and vocal communication is well developed
(Tschanz, 1968
;
Ingold, 1973
;
Birkhead, 1978
; Wagner,
1992
,
1997
;
Lefevre et al., 1998
). While
birds in most other families have a single developmental pattern, the auks
include species with three modes of chick rearing
(Sealy, 1973
;
Gaston, 1998
;
Ydenberg, 2001
). Guillemots
(Cepphus sp.), Brachyramphus murrelets, puffins
(Fratercula sp.), and auklets have semi-precocial young that are
cared for at the nest site until they are close to adult size, and then fledge
unaccompanied by their parents. Synthliboramphus murrelets have
precocial young that depart the colony at only 2 days of age accompanied by
both parents, who provide extended care at sea. Razorbills and murres
(Uria sp.) have `intermediate' young that receive biparental care at
the nest site until they are about 30% of adult body mass, followed by a
period of male only care at sea (Wanless
and Harris, 1986
; Gaston and
Jones, 1998
; Hipfner and
Chapdelaine, 2002
). For more detailed descriptions of fledging
behaviour and natural history, see Gaston and Jones
(1998
) and Hipfner and
Chapdelaine (2002
). These
different developmental patterns are likely to result in distinct selective
pressures acting on the ontogeny of parentoffspring recognition.
The development of parentoffspring recognition in various taxa is
usually related to the timing and probability of misidentification. For
example, in many species of birds, the onset of parental recognition coincides
with offspring mobility, i.e. fledging
(Beer, 1982;
Falls, 1982
;
Beecher, 1991
). Before chicks
are mobile they can often be reliably identified by geographic cues alone,
such as the nest site. Similar patterns have been reported for some mammal
species (Holmes, 1990
;
Charrier et al., 2001
). The
exceptions are those species that are colonial nesters with poorly defined
nest sites (e.g. murres and gulls), where chicks may be confused earlier in
life (Beer, 1982
;
Falls, 1982
). Razorbills,
although colonial, have distinct and separate nest sites (1-5 m apart) and
chicks generally do not move from these sites prior to fledging (Birkhead,
1977; Hipfner and Chapdelaine,
2002
). As a result, geographic cues alone should be sufficient for
identification of razorbill chicks while at the nest site. The crucial period
for parentoffspring individual recognition in razorbills is during the
chick's mobile stage at sea, when only the male parent is providing care. We
would then expect the onset of individual recognition to coincide with the
fledging period, and furthermore, if the pressure to recognize were restricted
to the male parent, parentoffspring recognition would be likely to
develop a paternal bias.
Aspects of individual vocal recognition between parents and offspring have
been investigated experimentally in four species of auk, each study providing
information about recognition onset. Common murre (Uria aalge) chicks
recognize their parent's calls that they have heard only from within the egg
(Tschanz, 1968). Thick-billed
murre (Uria lomvia) parentoffspring recognition is mutual,
with chicks recognizing their parent's calls as early as 3 days post-hatching
(Lefevre et al., 1998
).
Ancient murrelets (Synthliboramphus antiquus) also have mutual
parentoffspring recognition, developing within 2 days of hatching
(Jones et al., 1987
). In
razorbills, Ingold (1973
)
reported that parents (of unknown sex) recognized their chick's calls at 10
days but not 4 days after hatching (razorbill chicks fledge in approximately
15 days; Gaston and Jones,
1998
; Hipfner and Chapdelaine,
2002
). Ingold's
(1973
) findings are consistent
with the development of parentoffspring recognition in razorbills
coinciding with the transition to mobility, but whether there is a sex bias in
recognition remains untested. The primary goal of this study was to test
whether there is a paternal bias in razorbill vocal recognition by comparing
the responses of male and female parents to playback experiments of chick
calls.
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Materials and methods |
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Individual and sex identification of birds
Accurate individual and sex identification of razorbills Alca
torda L. was accomplished using existing metal/colour leg bands (numbers
visible by scope) or applied temporary marks. Additional banding of focal
birds was not feasible because capture sensitized subjects to our presence,
precluding close observation. Two methods were used for marking. A one-time
site-sweep was made soon after chicks hatched, at which time a small quantity
(approx. 50 ml) of brown or red hair dye was placed on each nest site. When
birds settled back into the nests (usually within 5-10 min), they were marked
by the dye. The second method used picric acid (non-toxic dye that turns
yellow upon contact with feathers) delivered via a 100 mm syringe.
The second method was delivered while hidden so that the target birds would
react as though they had been hit by falling guano (a constant occurrence).
Both of these methods resulted in unique individually identifiable shapes that
withstood daily diving behavior. The dye patterns, along with variations of
natural markings and life history information, were recorded on individual ID
cards.
Razorbills, as is the case for most auks, are sexually monomorphic, making
it difficult to determine the sex of birds observed in the field. Sexing birds
was accomplished by three on-site behavioral methods while a fourth laboratory
method was used for confirming the accuracy of the behavioral methods. First,
when copulations were observed, the mounting bird (i.e. dorsal position) is
reliably a male (Wagner,
1996). Although the bird being mounted is likely female, Wagner
(1996
) observed a number of
malemale mountings and so mounting was not used as a definitive method
for sexing the ventral bird. Second, when chicks fledge, they depart with the
male parent (Wanless and Harris,
1986
; Gaston and Jones,
1998
) and thus observation of a fledging event was sufficient to
identify the putative male. Third, despite male and chick having departed,
females would return to the empty nest site, usually at dawn with food for the
chick, and stay at the nest site. Although the third method is not entirely
independent of the second, together the three methods were sufficient to sex
all subjects. Accuracy of the behavioural sexing criteria was tested by
applying it to 10 subjects of a concurrent study (sex differences in parental
investment; R. Paredes, unpublished data) from which 0.5 ml blood samples were
taken and used for determination of sex using molecular markers
(Fridolfsson and Ellegrin,
1999
). We purposely avoided capturing the subjects of the study
reported here so that these birds would more readily habituate to our
presence. The sex for each of these 10 birds had been determined with at least
two of the three behavioural criteria. In each case the sex determined with
the behavioural criteria agreed with the molecular technique (R. Paredes,
unpublished data). The results of the current study indicate that vocal
behaviour, in addition to the behavioural methods listed above, can also be
used as a reliable indicator of sex for breeding adult razorbills.
Audio recordings
Audio recordings of razorbill vocal behavior were made with an AKG (AKG
Acoustics, Vienna, Austria) ultra-directional (shotgun) microphone, through a
Sennheiser (Wennebostel, Germany) power supply and into a Sony (Sony Corp.,
Tokyo, Japan) TCD D10 Pro II DAT recorder, a Sony Pro-Walkman cassette
recorder, or direct-to-disk. Direct-to-disk recording was converted at 16 bits
using Syrinx software (Burt,
1999) using a Fujitsu (Fujitsu Ltd., Tokyo, Japan) laptop platform
(600 MHz processor, 20 GB hard drive and 256 MB RAM). Playback experiments
were run from the same computer through an Acoustic Research (Lake Mary, FL,
USA) speaker-amplifier (±5 dB frequency response between 50 Hz-20 kHz).
All playback experiments were videotaped with a Sony Hi8 camcorder. Power for
all equipment was supplied by a portable (5 A) solar panel connected to two 12
V collection batteries, from which individual rechargeable batteries
(NiCd or Li) were recharged as needed.
Initially, all accessible razorbill nests (approximately 120) on the island
were scouted for recording, observation and playback potential. Focal nests
were chosen (60 nests in seven areas), adults were marked (see above), and a
rotation was established to record vocalizations from as many birds at
different sites as possible. Recording site selection was determined by
weather (i.e. wind and rain direction and severity) and background noise
(mostly surf and other birds, con- and heterospecific), in addition to what
recordings were needed. The vocalizations targeted and used for all playback
experiments were those between the chick and attending adult given while on or
near the nest. Examples of these chick and adult contact calls are provided in
Fig. 1. These calls correspond
to Bédard's (1969; from Hipfner and
Chapdelaine, 2002) `Lure Call' made by adult males and `Departure
Call' made by chicks.
|
Playback experiments
A total of 89 playback experiments were conducted to 42 individual birds at
19 different nests. Four different types of playbacks were conducted: (1)
chick calls played to male pair-members (i.e. putative fathers, herein
referred to as males or male parent; N=29 playbacks to 14 males); (2)
chick calls played to female pair-members (i.e. putative mothers, herein
referred to as females or female parent; N=28 playbacks to 13
females); (3) male calls played to chicks (N=15 playbacks to 12
chicks); and (4) male calls played to their female mates (N=17
playbacks to 10 females). Each subject was only sampled once during data
analysis for each type of playback experiment (i.e. samples are independent;
see below for criteria). The experiments tested whether (1) males and (2)
females recognize their chicks, and (3) whether chicks recognize their male
parent. The goal of the fourth playback experiment, testing whether females
recognize their mates, was to demonstrate that females would respond to the
procedure. It was not possible to playback female calls to their chicks and to
their mates because females rarely called, except when male and female parents
reunited on their nests, but these call sequences tended to be highly
overlapped and therefore unreliable to extract only female calls. Playback
experiments were serial presentations of control- and test-call treatments and
then repeated in opposite order (for a fuller treatment of playback design
issues, see McGregor, 1992).
Test treatments consisted of four different calls (to control for
psuedoreplication; Kroodsma,
1989
) from the focal individual's parent or offspring. Control
treatments were four different calls from a non-parent or non-offspring from
the same area (i.e. within audible range) except for two subjects that had
isolated nests. Starting orders (control or test treatment) were randomly
determined by a coin toss and then alternated for all subsequent playbacks
during that session (i.e. until the equipment was moved to a different
location).
Experiments began by setting up speakers within 5 m of each nest. Playbacks followed shortly thereafter if this had been accomplished without being detected by the birds. If the birds were disturbed (i.e. moved off their nests), the area was vacated for 1-4 h to allow normal behaviour to resume before initiating a playback. All playbacks occurred when chicks were between 11-18 days old. Although adults and chicks were vocal prior to fledging, clear counter-calling (i.e. bidirectional, repeated calling) between parent and chick only began once the chick began showing signs of mobility. It was only after this point in time that parents and chicks clearly responded to the playbacks of each other's calls. At the same time, the amplitude of chick calls increased substantially, which greatly facilitated recording. Consequently, most of the playback experiments (i.e. 57 of 89) occurred within 48 h of fledging and we were thus able to restrict the comparative analyses to this time period (see below). Finally, because the playbacks occurred in situ, the chick was usually with one parent during most experiments. In order to control for the problem of response interference by a non-focal bird, any such overt response (i.e. calling or movement) during the playback sequence terminated the experiment.
Responses to playbacks were measured in situ based on the number of calls given, orientation behavior (presence/absence), and phonotaxis (i.e. movement towards the broadcast sound source; presence/absence and distance). Subjective accounts of response strength and any additional information were also made at the same time. Videotaped accounts of playbacks were used to verify scores in the laboratory. If a subject gave no apparent response to a playback using the in situ criteria then the experiment was repeated at a later time. Analyses of response frequencies include all responses to all playback data (i.e. test or control conditions) and any repeated measures on the same subject were averaged before combining data across subjects. The analyses involving treatment comparisons (i.e. test versus control) used only the data from within 48 h of fledging (with the exception of playbacks to two males that gave clear responses 72 h prior to fledging), to ensure that femalechick tests were not conducted systematically earlier than malechick tests. If a subject had received multiple playbacks for these tests, the analyses included only the first playbacks to which subjects gave any category of response. The final analyses summarized the playbacks with two methods: (1) the mean number of calls or distance moved (the best indicators for most conditions being ratio data and unambiguous in nature) and (2) a composite score combining measurements of the three categories of bivariate data: Call?, Orient? and Taxis? (ordinal data). Untransformed ratio data (i.e. number of calls; distance moved) were tested with parametric statistics after being screened for departures from normality. Ordinal (i.e. the composite response) and bivariate data (i.e. response rates) were analyzed using nonparametric comparisons. All comparisons were two-tailed and paired within individuals. Sample sizes (N or degrees of freedom, d.f.) always refer to different individual birds and are given as subscripts with the test statistic.
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Results |
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Males (putative fathers) responded more to the calls of their chicks than to those of strange chicks, indicating paternal vocal recognition (Fig. 3A,B). Both call and the composite assay indicated significant differences between test and control treatments (paired t-test for variable calls: t13=4.38, P=0.0008; Wilcoxon signed-ranks test for composite score variable: T=4, N=14, P=0.0166).
|
Females (putative mothers) did not respond more to the calls of their chicks than to those of strange chicks (Fig. 3C,D). Neither calling or movement responses analyzed separately nor the composite assay indicated significant differences between test and control treatments (paired t-test for variable calls: t12=0, P=1.0; paired t-test for variable distance moved: t12=0.955, P=0.3613; Wilcoxon signed-ranks test for composite score variable: T=9, N=13, P=0.753).
Chicks responded more to the calls of their male parent than to those of strange adult males, indicating mutual paternal vocal recognition (Fig. 3E,F). Both call and the composite assay indicated significant differences between test and control treatments (paired t-test for variable calls: t11=4.33, P=0.0012; Wilcoxon signed-ranks test for composite score variable: T=0, N=12, P=0.0431).
Finally, male calls were played back to their female mates as a supplemental test of whether or not females would respond to the procedure. The problem being confronted was whether the lack of discrimination shown by females to their chick's calls truly indicated a lack of recognition (Fig. 3C,D) or if females were simply not responding to the experimental procedure. Females, as previously, did not respond vocally, but they approached the speaker only during playbacks of their mates' calls and did not respond to the calls of other males. However, the data only bordered statistical significance at the 5% level using a two-tailed test (paired t-test for variable distance moved: t8=1.58, P=0.1529; Wilcoxon signed-ranks test for composite score variable: T=0, N=10, P=0.1088), probably because of low statistical power caused by an unavoidably small sample size (i.e. 18.2 and 18.5% for the two tests, respectively). As a result, the test is suggestive of mate recognition but not conclusive. The main reason for conducting the mate recognition playbacks, however, was to ascertain whether females would respond to the procedure and clearly they did respond.
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Discussion |
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In this study, the pattern of parental care of razorbills appears to
interact with the ontogeny of individual recognition, resulting in a male
gender bias in parentoffspring recognition. Our results agree with
those of Ingold (1973),
supporting the prediction that recognition onset in razorbills develops during
the end of the nestling stage as the chick becomes increasingly mobile and
ready to fledge. Our results also agree with several studies that show
parentoffspring vocal recognition can be bi-directional or mutual with
alcids (Tschanz, 1968
;
Ingold, 1973
;
Jones et al., 1987
;
Lefevre et al., 1998
). Our
results are unique, however, in that we show that mutual
parentoffspring recognition in razorbills appears to be limited to the
male parent, despite a significant period of biparental care. Specifically,
males responded preferentially to their own chick's calls and chicks responded
preferentially to the calls of their male parent. In contrast, the playback
experiments were not able to show any evidence of recognition between
razorbill female parents and their offspring. Females responded infrequently
to their chick's calls and indifferently to the calls of strange chicks.
Finally, we found that females only rarely vocalized to their chicks,
hampering our efforts to test the chick's ability to recognize their female
parents (this vocal bias did, however, prove to be a reliable means of sexing
breeding razorbills). Our attempts to test whether chicks recognized the calls
made by their female parent that were relatively infrequent and directed
elsewhere (e.g. mate counter-calls) were not successful. Thus, chicks may
recognize their female parents via these less frequent vocal cues or
via other modalities (e.g. visually). These possibilities remain to
be tested.
While our data suggest that female razorbill parents do not recognize their
chicks' calls, a lack of response cannot be equated to a lack of vocal
recognition. Our observations are strengthened by additional non-vocal
behavioural assays (i.e. orienting and phonotaxis) that similarly showed a
lack of discrimination between control and test treatments by females. In
addition, playback experiments between mates (i.e. adult male to adult female)
demonstrate that females respond to the procedure but not selectively to their
chick's calls, supporting the conclusion that femalechick vocal
recognition is nonfunctional and possibly absent. It remains possible,
however, that females recognize their chicks using vocalizations or another
sensory mechanism, but do not respond to them at the nest because it is
inappropriate or unnecessary. Male parents gave their strongest responses to
playbacks close to the time of fledging, when they were off the nest
attempting to counter-call with their chick. In contrast, females were never
observed counter-calling with their chicks either on or off the nest. Because
females rarely interact vocally with their chicks, there is little opportunity
for chicks to learn their female parents' calls. It would thus appear that
regardless of whether or not female parents recognize their chicks' calls,
their lack of functional response to their chicks would decrease if not negate
any future benefit (e.g. nepotism) that vocal recognition might provide
(Holmes, 1990;
Sherman et al., 1997
).
Ultimately, this needs to be tested by observing interactions between adult
females and their mature offspring (e.g.
Insley, 2000
).
To sum, evolutionary pressures do not act solely on the finished product
(the breeding adult) but also upon every stage of an animal's life history. In
the present study with razorbills, a particular behavioural phenotype (i.e.
male biased parentoffspring vocal recognition) appears to result from
the interaction of two primary factors. First, razorbills follow a life
history strategy of biparental care until chick mobility, after which a period
of paternal-only care ensues (Sealy,
1973; Wanless and Harris,
1986
; Gaston,
1998
; Gaston and Jones
1998
; Ydenberg,
2001
). Second, the developmental onset pattern of vocal
recognition commonly occurs during a neonate's transition to mobility when
other cues such as location are no longer available
(Beer, 1982
;
Falls, 1982
;
Beecher, 1991
). The final
result is a sex-bias in recognition behaviour, an ability that is fundamental
to many social interactions. Such a result in the context of a long life span
combined with natal philopatry could play a decisive role in driving other
higher order social phenomena within this species.
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Acknowledgments |
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