THE VOCAL BEHAVIOR OF THE AMERICAN CROW, CORVUS BRACHYRHYNCHOS
THESIS
Presented in Partial Fulfillment of the Requirements for the Degree Master of Sciences in
the Graduate School of The Ohio State University
By
Robin Tarter, B.S.
*****
The Ohio State University 2008
Masters Examination Committee Approved by
Dr. Douglas Nelson, Advisor
Dr. Mitch Masters ______
Dr. Jill Soha Advisor Evolution, Ecology and Organismal Biology Graduate Program ABSTRACT
The objective of this study was to provide an overview of the vocal behavior of the American crow, Corvus brachyrhynchos, and to thereby address questions about the evolutionary significance of crow behavior. I recorded the calls of 71 birds of known sex and age in a family context. Sorting calls by their acoustic characteristics and behavioral contexts, I identified and hypothesized functions for 7 adult and 2 juvenile call types, and in several cases found preferential use of a call type by birds of a particular sex or breeding status. My findings enrich our understanding of crow social behavior. I found that helpers and breeders played different roles in foraging and in protecting family territories from other crows and from predators. My findings may also be useful for human management of crow populations, particularly dispersal attempts using playbacks of crows’ own vocalizations.
ii ACKNOWLEDGEMENTS
I would like to thank Dr. Kevin McGowan of Cornell, Dr. Anne Clark of
Binghamton University, and Binghamton graduate student Rebecca Heiss for allowing me to work with their study animals. McGowan, Clark and Heiss shared their data with me, along with huge amounts of information and insight about crow behavior. None of my work would have been possible without their help. I would also like to thank Dr.
Douglas Nelson, Dr. Mitch Masters, Dr. Larry Phelan and Dr. Jill Soha of The Ohio State
University for their help at all the stages of my research. Finally, I owe a great deal of thanks to my husband, Anton Mates for all of his help – from accompanying me in the field, to programming help, to editing and revising my thesis.
iii VITA
May 29,1982 ...... Born – Walnut Creek, California
2000 ...... B.S. Integrative Biology, The University of California at Berkeley
2004 – present...... Graduate Teaching and Research Associate, The Ohio State University
FIELDS OF STUDY
Major Field: Evolution, Ecology and Organismal Biology
iv TABLE OF CONTENTS
Page
Abstract……………………………...…………………...... …….....……ii
Acknowledgements……………………………………...……...... ….....iii
Vita…………….…………………...... …...……………………….…….iv
List of Figures…………………………………………...... ………....…..vi
Introduction………………………………………………...... …….....…..1
Methods…………………………………………...... …………...... ……3
Results………………………………………………………...... …....9
Discussion……………………………………………...... …...... ………29
Bibliography……………………………...……………..…...... …..37
v LIST OF FIGURES
Figure Page
1. Spectrograms of short, rough, fading, and scream calls...... 11
2. Spectrograms of nasal, double short, and double rough calls...... 12
3. Spectrograms of coo and rattle calls...... 18
4. Fraction of adults that gave each call type by sex and breeding status...... 22
5. Call types shown separately by sex and breeding status...... 23
6. Spectrograms of begging and babble calls...... 25
7. Fraction of juveniles of each sex that gave each call type...... 28
vi INTRODUCTION
The American Crow, Corvus brachyrhincos, is a highly intelligent songbird, with an exceptionally large brain relative to its body size (Lefebvre et al. 2002). American crows display advanced problem solving skills and exceptional memories. They mature slowly and disperse late compared with other passerines (Caffrey 1992). They live in extended families, generally composed of juveniles, young from previous years, and one pair of breeding adults. Individuals may disperse as early as 2 months post fledging or stay in their natal group for 7 years or longer and different populations display either male or female biased dispersal (Marzluff & Angell 2005 and Caffrey 1992 respectively).
It is unknown whether non-dispersing individuals (referred to as helpers) gain fitness benefits from this cooperative breeding behavior; so far no studies have succeeded in finding reproductive benefits of cooperative breeding for either helpers or breeders
(Caffrey 2002).
There are several reasons to study American crows other than their ubiquity, intelligence and unusual social system. American crows have great economic impact on many industries, including agriculture and civic planning. California pistachio growers, for instance, suffer an average damage of over a hundred dollars per hectare annually, and growers of nuts and fruits lose 3-4% of their yield to crows (Delwiche et al. 2007).
1 Crow communal roosts inconvenience humans across the country. In the winter, crows form giant groups of as many as two million individuals (McGowan 2005), often within city limits due to the light, warmth and lack of predators in urban habitats, making noise and leaving waste where they gather. There has been considerable interest in using crows’ own calls to disperse these roosts (Delwiche et al. 2007, Frings and Frings 1957), and the relatively low auditory frequency cutoff (5.6 kHz) found in the closely related hooded crow suggests that these species are adapted to long-range communication, which would make them good targets for acoustic dispersal (Jensen and Klokker 2006).
The questions of how cooperative breeding behavior is maintained, and how humans can best disperse unwanted congregations of crows can both be partially resolved by examining the vocal behavior of individually tagged and human-habituated wild crows. The fact that my study population was almost entirely comprised of tagged, human-habituated animals sets it apart from all other studies of crow acoustics except one
(Yorzinski et al 2006). Untagged crows are not reliably identifiable as individuals by human observers, and since at a distance there are no known indicators of their age or sex, observations of untagged individuals usually cannot be classified accordingly. With this problem removed, I was better able to ascertain contexts for the call types that I observed, and in many cases describe the responses they evoked in other known individuals. The differences I observed between the vocalizations of breeders and helpers sheds light on the benefits of cooperative breeding in this species. Moreover, I hypothesize functions related to group movement and foraging for certain call types, raising the possibility of exploiting those calls to relocate nuisance birds. 2 METHODS
My study took place in Cayuga Heights, New York (42°N, 76°W) from the beginning of June to the end of August, 2006. At the beginning of my study, the young had just fledged and at the end they were beginning to become more active and some ventured away from their families. Beginning in 1989, the crow population in this area has been monitored and nestlings have been marked with unique combinations of leg bands and wing tags to facilitate individual recognition (Yorzinski 2006). The majority of the individuals in my study had had blood samples taken in the nest, which were used to determine their sex.
The first phase of my research was a general observation of the animals in the study area. I spent 2 weeks following the members of the Ithaca crow project learning about the habits of the animals in their study. After this period of observation, I choose
10 families to focus on for the rest of my study. My selection was based on several factors. First, I wanted to use families with multiple tagged individuals so that I could identify the animals I was recording. I also wanted families that were habituated enough to human activity on their territories that they would behave normally while I recorded them. It was also important for me to include individuals of varying age and reproductive status in my study to allow me to examine the ontogeny of crow acoustic
3 behavior and to compare the behavior of helpers and breeders. All of the families I chose had 2 breeders, from 0 to 5 adult nonbreeders (helpers), and from 2 to 5 juveniles (first year birds). Ages ranged from less than 1 to 13 years. I wanted to have as much variation in the composition of my study families as possible in order to examine the possible effects that different composition might have on behavior. Finally, because I decided to make all of my recordings from inside my car, it was necessary to choose families that frequented car accessible locations. I chose to do all of my focal watches from my car because I found that, when I approached the crows on foot, the only vocalizations I could record were alarm-associated. Parr (1997) made the same observation.
I was able not only to tell individuals apart and compare their behaviors with respect to their sexes and breeding conditions, but also to get closer to my study animals than have observers of other populations. The Ithaca, NY crow population has been under continuous study by Kevin McGowan and his associates since 1988. Most of the tagged individuals in this population stay in Ithaca year round, so they are exposed to close human contact throughout the year (McGowan 2005). Continuous censusing and provisioning with peanuts allows the members of the project to keep track of the life histories of the Ithaca crows and has resulted in little fear of humans on the part of the crows. Ithaca residents are in general exceptionally friendly towards crows, at least in part due to McGowan’s outreach and education projects.
4 Unlike the crows I have observed in Columbus, OH, who, even after months of daily feeding and watching flew away whenever I tried to approach them, the Ithaca crows allowed me to approach them without attempting to flee after a few days. When recording in Columbus, I have been able to record only 2 types of calls at close range
(less than 10m), both associated with alarm, but in Ithaca I was able to record many call types including several which did not seem to be associated with my presence.
I made recordings of 76 individuals, including 42 adults and 32 juveniles. Of the adults I recorded, 21 were male, 16 female, and 5 were of unknown sex. The juveniles displayed a similar sex ratio, with 20 males and 12 females. Once I had chosen the families for my study, I began focal watches. I made a list with the names of the families in random order and visited them in that order every day between the hours of 5am and
7pm. I spent a total of 52 days in the field, and had from 0 to 6 successful focal watches per day with a total of 120 focal watches. If a family was not present on its territory when I arrived, I moved on to the next family on my list. This occurred in 135 of my 255 attempted focal watches, and overall some families were sampled more times than others.
Every family was sampled at least 3 times, but one family was sampled 20 times.
Because of this, it is impossible for me to make any statistical comparisons between families. I did not observe any significant differences in the overall vocal behavior of the different families. The bias in my sampling was due to that fact that some families spent more time on their territories or had territories that were more accessible to me than other families. The family that I recorded 20 times was especially human-habituated, being
5 more willing to approach my car than other families, however every call type that I recorded in focal watches of that family was also recorded in other families.
If a family was present on its territory when I arrived, I began making recordings after a period of 5 minutes during which time the animals may have behaved unusually due to my arrival. During these 5 minutes, I identified all of the crows on the territory. If
I did not hear any vocalizations for 15 minutes after I arrived, I moved on to the next family on my list, but this was very rare. More commonly, I heard the family before I saw them. At the beginning of my study I used peanuts to draw families close enough to my car for me to read their tags and bands. As my field season went on, I became more proficient at identifying individuals and they became more habituated to my presence; I then stopped using peanuts for every focal watch, but continued to give peanuts intermittently. All of the recordings I used in my analysis were made from birds within
20 meters of my car, using a Marantz PMD-670 solid-state recorder and a Sennheiser
ME-67 directional microphone.
During my focal watches I directed the microphone towards the closest bird that was vocalizing. After every vocalization, I said the name of the individual, or if the bird could not be identified I said “unknown”. For my analysis, I used recordings only from birds that I saw clearly while they were vocalizing. Since I chose families with mostly tagged birds I knew the age, sex and breeding status of the majority of the birds I recorded. Several of the unbanded birds had also been sexed by their breeding behaviors and were recognizable by their size or other physical characteristics (several birds were 6 missing feet). While recording, I also made notes about the behavior of the family using opportunistic sampling and focusing on whichever bird was vocalizing. I noted the locations of different individuals in the territory and documented behaviors such as feeding, allopreening, playing, mobbing, begging and territorial behaviors. I watched body postures carefully, noting that specific feather positions and head and tail movements corresponded with certain behaviors. I paid special attention to the vocalizing bird and tried to record the behavioral context of every vocalization I recorded.
Once I returned from the field, I transcribed and codified my written data. I listened to all of my audio recordings and separated out those for which the identification of the vocalizing birds was known and for which I had behavioral observations associated with each vocalization. I then removed from this set all of the recordings where the background noise was too loud or the signal too weak to be useful for acoustic analysis.
This eliminated the majority of my recordings but I was left with a sample of recordings which included all of the major call types I had observed.
Next I cut the remaining recordings into pieces, separating out call bouts from different individuals. I further subdivided these recordings into smaller sections, each containing one call series. I made spectrograms of all of these cuts using the program
Amadeus II(v3.8.7, 2006, HairerSoft on a 2005 MacBook). I listened to all of these and put them in three categories: adult sounds that consisted of series of “caws”: high amplitude, broadband, low frequency sounds characteristic of corvids; “non-caw” 7 sounds; and juvenile sounds, which I found I could separate from adult sounds by ear with 100% reliability. Within the two categories of adult vocalizations, I sorted the recordings based on how they sounded to my ear and on the visual properties of their spectrograms.
Representative spectrograms for this paper were generated in MATLAB 7.4.0, using the “spectrogram” routine in the Signal toolbox, slightly modified for greater frequency resolution. To measure the significance of correlations between use of call types and sex/breeding status, I used Fisher’s exact test, since sample sizes and expected values were often small. Calculations were done in MATLAB 7.4.0, using the
“Fisherextest” function, written by Dr. Antonio Trujillo-Ortiz at the Facultad de
Ciencias Marinas, Universidad Autonoma de Baja California, Mexico; and the
“myfisher” function, written by Dr. Giuseppe Cardillo at CEINGE (Centro di
Ingegneria Genetica e Biotecnologia Avanzate), Italy.
8 RESULTS
I found 5 distinct categories of “caw” sounds, 2 categories of non-caw sounds and
2 categories of juvenile sounds. Eighty-two percent of the cuts (296 of 361 sounds) that I selected for acoustic analysis fell into one of these categories. I sorted the juvenile vocalizations into two categories, begs – short sounds given singularly, or in long bouts with high interbout similarity, and babble – irregular sounds always given in long strings and sometimes resembling adult sounds. The remaining recordings sounded and looked too different from any of the categories I created to place in any of these categories, but didn’t exhibit enough similarities between them to indicate that additional categories would be useful. I have no doubt that there are call types that I did not observe or record with sufficient frequency to analyze. All of my recordings were made on territories during the fledgling season and it is likely that crows use other vocalizations in other contexts.
“Caw” Calls
The following call types are characteristically repeated in bouts lasting from a few seconds to 15 minutes or more and have a characteristic “caw” sound.
9 Short call (Figure 1A):
The Short call can be distinguished from other call types by its short duration
(roughly 200 msec) and its nearly symmetrical frequency contour. The majority of the acoustic energy in this call is contained in the second harmonic, but the first and third harmonics are always visible on spectrograms as well. The call is delivered in bouts, generally of between 3 and 10 calls. The calls are sometimes given at regular intervals and sometimes irregularly spaced, but always in rapid succession, with inter-call intervals less than 400 msec. Inter-bout intervals can range from 1.5 to 3 seconds. The wobble, an extremely fast sinusoidal frequency modulation, which is present in many corvid vocalizations (Laiolo & Rolando, 2004) is rarely visible in the short call – the frequency contour of this call is much smoother than that of other “caw” calls.
The short call was the most commonly recorded call in my study. I made usable recordings of short calls in 39% (47) of my focal watches. I recorded short calls from 18 individuals: 6 females, 11 males and 1 bird of unknown sex from 7 families. I never recorded a short call when all family members were visibly present in one location.
Usually the calls were given when individuals were first appearing on their territory after an absence or convening on a feeding spot. The most common response that I observed family members giving to the short call was to fly toward the position of the caller. I often heard this vocalization when I provisioned the animals with peanuts when not all of the family members were present. I also heard this call during territorial disputes, coming from the family that was outnumbered. Callers usually pointed their heads up when making this vocalization. 10 Figure 1: Spectrograms of short (A), rough (B), fading (C), and scream (D) calls
11 Figure 2: Spectrograms of nasal (A), double rough (B), and double short (C) calls
Doubled short call (Figure 2C):
The doubled short call or double call consists of pairs of very short calls given in bouts of 2 to 8 pairs. The interval between the short calls in each pair (usually about 1 second) is very consistent within a bout, but the intervals between pairs can vary between
12 1.75 and 2.5 seconds. I recorded the double call from 3 females, 5 males and 1 bird of unknown sex from 4 families. When a territorial dispute was ending, and birds were returning to their respective territories, the call was given by the first bird to reach the home territory. It seems to be associated with the dispersal of multiple-family assemblages and the reaffirmation of intra-family connections. This call is functionally similar to the short call (Figure 1A) in that receivers respond to it by approaching the caller but, unlike the short call, it always displays a paired temporal pattern.
Rough call (Figure 1B):
The rough call is the most broadband of the “caw” calls and one of the longest, usually lasting about 300 msec. The acoustic energy is primarily found in the third harmonic, but the second harmonic also has a strong energy signature at the beginning of the call. The frequency contour has a roughly fusiform shape, trailing off at the end. The call has a strong wobble, which can easily be seen on the spectrogram. The call is sometimes given singly, but is usually delivered as an irregular series, with shorter inter- call intervals towards the end of the bout.
I made useable recordings of the rough call on 22% (26) of my successful focal watches, from 11 females, 4 males and 1 bird of unknown sex from 6 families. The majority of the callers were female breeders, but some were male breeders or helpers of either sex. In every recorded instance, it was directed at a begging juvenile. Often the caller was being followed and harassed by one or more juveniles when the rough calls began, and then attempted to flee from this harassment while continuing to call. Every 13 bout of rough calling that I observed ended with the caller moving away from other individuals. Sometimes juveniles stopped begging after a harassed adult gave this call, but often they continued to beg after a short pause. When this was the case, their begging was often directed at a new adult. Adults did not respond to this call, either vocally or by changing position.
Double rough call (Figure 2B):
The doubled rough call, or long-short call, has the same acoustic properties as the rough call, except for its temporal patterning. It always consists of a long rough call followed by one or more very short rough call (100 – 150 msec). I recorded the long- short call from 3 males and 1 female from 3 families. This call type was always given by a bird that was moving away from its group when unrelated crows were present, such as during mobbing or a territorial encounter. I never observed this vocalization when a bird was perched; rather callers were on the ground or in the air. Flying callers were always departing the main group at the time. The acoustic qualities of the long-short call are similar to those of the rough call, and like the latter, the long-short call is associated with movement away from other family members. However, the members avoided were not invariably juveniles, as they were in the case of the irregular rough call.
Fading call (Figure 1C):
The fading call has a shape and length similar to the rough call, but its energy structure is very different. At the beginning of the call, most of the energy is in the second harmonic, but towards the middle of the call, the energy switches to the third 14 harmonic. The calls are given in short bouts of 3 to 5 calls with even spacing of roughly
250 msec. Different bouts recorded during the same period of observation usually had the same number of calls, for instance, a bout with 3 calls was usually followed by another 3 call bout.
This call appeared in 21% (25) of focal watches, coming from 4 females, 6 males and 3 birds of unknown sex from 7 families. This call was always given when multiple families were in close proximity, usually in the context of a territorial dispute. Generally the calls were given antiphonally, with individuals from different groups alternating. The calling bird was always stationary, but nearby birds were often chasing others or feeding.
Scream call (Figure 1D):
Most of the energy in the scream call is in the second harmonic, but it has strong harmonic structure overall. This call is usually shorter than the rough or fading calls, but is also the most variable in length, ranging from 100 to almost 400 msec. It is given in bouts of variable length with short intercall intervals. The length of the bout may be associated with the duration of the perceived threat.
I recorded scream calls in 14% (17) of focal watches from 6 females and 4 males from 6 families. Usually this call was associated with some kind of danger, real or perceived. I never observed this call directed at a living crow, although in one case several crows from a single family gave it while facing a recently dead juvenile family member. In all other cases, the call was directed at a possible predator (red-tailed hawks, 15 Buteo jamaicensis or cats, Felis silvestris catus) or an animal (skunks, Mephitis mephitis,
Eastern grey squirrels, Sciurus carolinensis or myself) about which the caller gave other indications of alarm. The calls of crows mobbing raptors in flight were invariably scream calls, but many were too noisy to analysis and the individuals were never identifiable. Crows also regularly mobbed and gave scream calls when human researchers from the Ithaca Crow Project climbed nest trees to band and tag the young.
Individuals from other territories often joined aerial mobs, often starting from over a mile away, but I did not observe them to approach when crows perched and gave scream calls within their own territory.
Nasal call (Figure 2A):
The distinctive sound of the nasal call is obvious from its very unusual spectrogram. The frequency contour is inflected at the beginning and then flattens out.
Most of the energy is in the third harmonic, but some is in the second at the beginning.
At the point where the frequency flattens out, all of the energy disappears from the fourth and fifth harmonics, showing very strong filtering in the animal’s vocal tract. The call is also exceptionally long, lasting over 500 msec in most cases. Nasal calls are delivered in bouts of two or three, with a consistent delay of about 750 msec between individual calls; bouts are separated by several seconds of silence.
I often heard the nasal call in the field, but I was able to record it and identify the vocalizing bird in only 4 focal watches (3%), from 2 individuals who were both male from 2 families. This is because the caller was usually in a group of birds flying high in 16 the air and because the call usually overlapped the calls of other birds, making it difficult to determine which bird was producing which call type. I frequently observed this call being made when an animal was approaching its territory or a foraging location. In all four of my successful recordings, the call was delivered while other group members were vocalizing (usually short or fading call types), with the different callers overlapping.
When given simultaneously with another bird giving short calls, family members converged on the location of the callers more quickly than when the short calls were given alone leading me to hypothesize that this call functions to strengthen the signals of other callers.
Other Adult Vocalizations
The following call types differ from the typical “caw” vocalizations of crows in their acoustic features and their comparatively low amplitude.
Coo (Figure 3A):
The coo call of the crow is the only purely tonal call I recorded in the field. This call is short (100-200 msec) and very low amplitude. There is no frequency modulation and virtually all of the energy is in the second harmonic. It is given in bouts of 2 to 4 calls with even spacing.
17 Figure 3: Spectrograms of coo (A) and rattle (B) calls
The coo call can be heard only from a short distance, but since birds generally make it from a conspicuous location, I was able to record it on 7 of the 15 focal watches where I observed it. I recorded 1 female and 3 males cooing, along with 2 birds of unknown sex from 4 families. The coo always came after a period of arousal in the group
18 – intense begging, intra-family hostility over a desirable food item or a territorial dispute.
When juveniles persist in begging after feeding, the closest adult may coo. Cooing by adults leads to an abrupt stop in juvenile babbling behavior as well. In all observed instances where adults cooed to other adults, the callers were family members who had engaged in agonistic behavior immediately beforehand leading me to hypothesize that the coo is an appeasement behavior.
I observed coos only from perched birds on their territories, with at least one group member, usually a juvenile, within a half a meter of the caller. The coo was always paired with a visual display; with the head and throat feathers ruffled, the caller vertically bobbed its head, while pointing the bill down and into the chest. The display looked like a choking movement, as if the bird had swallowed a large object and was trying to force it down its esophagus.
Rattle (Figure 3B):
The rattle generally lasts between 1.5 and 2.5 seconds. Each consists of a series of rapid clicks, which in the second half of the call acquire a resonant decay and produce a bell-like ringing. Both the click rate and the resonant frequency are roughly constant within a rattle; the example shown is typical, with a click rate of about 12.5 Hz.
I recorded the rattle in 13% (16) of focal watches, from 4 females and 6 birds of unknown sex from 5 families. The call was almost always given from a location that was not directly visible to me, usually from deep within the foliage of a perch tree or in a 19 clump of other crows, and frequently it was given when humans approached other family members who were foraging on the ground. When family members were dispersed over their territory and this call was given, the whole family would assemble, followed by allopreening, cooing and head bobbing, all familial bonding behaviors. Other calls causing families to congregate such as the short and double call types were typically given when some family members were off-territory, and resulted in members arriving but sitting in moderately dispersed groups (e.g. multiple, adjacent trees.) The rattle, however, resulted in families compacting themselves more tightly, for instance in a single tree or on a single roof. The caller continued rattling until all nearby members were gathered.
Similar in temporal structure to this rattle, but quieter and less tonal, was a short, conflict- associated rattle (which I call the conflict rattle). It has been recorded and described in previous research (Laiolo and Rolando 2003), but I observed it very infrequently. In crows, physical contact is extremely rare during territorial disputes and other agonistic interactions. In the 52 days I spent in the field, I observed contests which reached the level of physical impact only 5 times. In all 5 cases I observed the aggressor bird making a short rattle call, but I was able to record this rattle only 2 times, from one female and one bird of unknown sex, and neither of these recordings yielded useful spectrograms due to background noise. The call was especially difficult to record because it was so quiet, and because the caller was moving quickly. The callers in these situations were being mobbed by birds of other species and about to be pecked, having food taken from them
20 by a non-family member and fighting back or physically displacing another crow on a food patch. I never saw any crow suffer physical injury from impact.
Analysis of Adult Vocalizations
I examined the correlation between adults’ sex and breeding status, and their use of given call types (Figures 4, 5A-B). I did not include the nasal call, coo or conflict rattle in this analysis, as each call type was recorded from fewer than five birds of known sex and breeding status. The included call types were recorded from between six and twenty-three such birds. Double rough calls were included in the rough category, and double short calls were included in the short category, since acoustically the individual caws of each were indistinguishable from those in the corresponding category.
The rattle appeared to be an exclusively female vocalization. Forty percent of recorded females gave it at some point, but none of the males did, despite a larger male sample population. The fraction of female helpers who gave it was larger than that of breeding females, but not significantly so (Fisher exact test: p=0.39). The rough call was predominantly given by breeding females (p=0.0007); the scream call was given by significantly more breeders than helpers (p=.0087).
The short and fading calls were predominantly given by male helpers (p=0.020 and 0.022, respectively), but the fading call was given the least by breeding males
(p=0.024). 21 Fraction of Adults Who Made Each Call Type 1 Breeding Females (10) 0.9 Breeding Males (10) 0.8 Helping Females (6)
0.7 Helping Males (11)
0.6
0.5
0.4
0.3
0.2
0.1
0 Short Rough Scream Fading Rattle
Figure 4: Proportion of individuals of a given sex and breeding status, that gave a particular call type.
22 Fraction of Adults, By Sex 0.9 Females (16) 0.8 Males (21) 0.7
0.6
0.5
0.4
0.3
0.2
0.1
0 Short Rough Scream Fading Rattle
Figure 5A. Proportion of individuals of each sex, that gave a particular call type.
Fraction of Adults, By Breeding Status 0.9 Breeders (20) 0.8 Helpers (17) 0.7
0.6
0.5
0.4
0.3
0.2
0.1
0 Short Rough Scream Fading Rattle
Figure 5B. Proportion of individuals of each breeding status, that gave a particular call type.
23 The rattle appeared to be an exclusively female vocalization. Forty percent of recorded females gave it at some point, but none of the males did, despite a larger male sample population. The fraction of female helpers who gave it was larger than that of breeding females, but not significantly so (Fisher exact test: p=0.39). The rough call was predominantly given by breeding females (p=0.0007); the scream call was given by significantly more breeders than helpers (p=.0087).
The short and fading calls were predominantly given by male helpers (p=0.020 and 0.022, respectively), but the fading call was given the least by breeding males
(p=0.024)
Juvenile Vocalizations
Begging (Figure 6a):
Begging vocalizations are short, broadband calls with energy localized in alternating harmonics (second, fourth, sixth, etc). They vary in length from under a second to almost 3 seconds and are given singly or in long, irregular bouts.
During the time that I was in the field, begging was by far the most common and conspicuous vocalization produced by juveniles. I recorded begging vocalizations in
85% (102) of the focal watches, from 27 individuals: 8 females, 17 males and 2 birds of unknown sex from all 10 families.
24 Figure 6: Spectrograms of begging (A) and babble (B, C, D) calls
Although the bias towards males in my recording could be explained by the skew in the sex ratio of the population as a whole, I did observe that males I recorded begged considerably more loudly and often than did females. Although I was able to record begging only in juvenile (first year) birds, I observed but did not record adult birds
25 begging, although they did so much less readily than juveniles, and only when the object of their attention was in possession of an especially desirable food item. When begging, juveniles lower their bodies and flutter their wings and open their beaks wide to expose the bright pink of their mouths. The rate of begs is inversely proportional to the caller’s distance from a target bird and directly proportional to their general level of arousal.
When alone or when no food is present, juveniles beg intermittently, but as an adult carrying food approaches, begs become more frequent until they run together into a gargling squall. As the juvenile takes the food, it continues to make choked begging vocalizations. These sounds seem to attract other juveniles more than any other sound, and all the nest mates approach to share in the feeding.
Begging vocalizations can be heard in a variety of contexts, but are most frequent when other group members are feeding. Juveniles also beg when no food is present and direct their begging in inappropriate directions (towards nest mates or when no other bird is present). Many juveniles persist in begging long after they can feed independently.
When juveniles first begin to feed on their own, they frequently pick up edible (and sometimes inedible) objects, drop them in front of an adult, and beg until the adult puts the food object in their mouths.
Babble (Figure 6b, c, d):
Babble vocalizations consist of long strings of calls with varying acoustic structure, some resembling adult vocalizations and some unlike any other crow sounds. I observed sounds similar to every adult call type described here except the coo during 26 juvenile babble bouts. When making an adult-like sound, the babbling juvenile often made appropriate body movements. I saw juveniles assuming the posture characteristic of cooing adults during babble bouts, but the sounds that these juveniles made while in this position were always too quiet to record. It is possible that they were attempting to coo, but were unable to do so at that stage in development.
I recorded juveniles babbling in 38% (45) of focal watches, from 4 females, 11 males and one bird of unknown sex from 8 families. Babbling behavior began when birds were between 3 and 4 months of age, and bouts generally took place when juveniles were apart from adults and nest mates. Juveniles ceased to babble at the same age that they stopped begging and began to use more characteristically adult vocalizations.
Analysis of Juvenile Vocalizations
Among juveniles, I recorded a higher proportion of males than females begging and babbling, but not significantly so (Fisher exact test p=0.22 and 0.21, respectively).
27 Fraction of Juveniles Who Made Each Call Type 0.9 Females (12) 0.8 Males (20) 0.7
0.6
0.5
0.4
0.3
0.2
0.1
0 Begging Babbling
Figure 7: Proportion of juveniles of each sex, that gave a particular call type.
28 DISCUSSION
I identified a number of call types used by American crows to coordinate group movement. They share this characteristic with several other social species that depend on patchy and ephemeral resources, including White-faced Capuchins, Cebus capucinus
(Boinski 1991) and Green Woodhoopoes, Phoeniculus purpureus (Radford 2004).
Many American crow researchers have described “assembly” and “dispersal” vocalizations, which cause receivers to, respectively, assemble at the position of the signaler or leave that position (Frings 1957, Parr 1997, Marzluff 2005). The observers differ in their hypotheses about the ultimate function of these vocalizations, but all agree that the proximate functions of the vocalizations are to attract crows to a location or to send them away from that location. Although many of my call types equate to those defined in previous research, I found no call types that function simply as universal
“assembly” or “dispersal” calls. Instead, the effect of each call depends on the familial relationship between caller and listener, as well as on their positions relative to their home territories.
The short call appears to function as a familial assembly call, recruiting distant family members to the general vicinity of the caller. This type probably includes both the
“Short Caw” and “Ko” of Verbeek and Caffrey (2002). Short calls vary considerably in 29 temporal patterning of the caws, and I did not attempt to subdivide the type based on such patterns, save for the simple case of the double call. The short call is heard more frequently than any other, reflecting the typical pattern of American crow foraging; each individual explores on its own, then short-calls to assemble the family if it comes upon a food bonanza or promising foraging site. Crows, as generalists, compete for food with a wide variety of other species as well as with conspecifics. They also cooperate to exploit food sources otherwise inaccessible to individual birds; Kilham (1989) reports crows shaking insects out of plants while others wait to catch them below, and working in groups to harass non-threatening predators such as herons and otters into giving up their catch. Both factors make the strategy of rapidly assembling the family at a good foraging site a rewarding one.
Chamberlain and Cornwell (1971) report a “dispersal” call type, based on field observations and playback experiments. The two spectrograms Chamberlain and
Cornwell associate with this category are quite dissimilar, and Parr (1997) doubts that it represents a coherent call type (Verbeek & Caffrey 2002). Verbeek and Caffrey consider at least one of these calls to be properly included in their “Short Caw,” which is supported by the first spectrogram’s close resemblance to a short call. I think this is behaviorally plausible; because the short call is often used to rally families within or near their home territory, playback may cause unrelated crows off their territory to retreat, lest they come into conflict with the resident family.
30 The doubled variant of the short call is primarily associated with territorial disputes, and seems to serve as a familial recruitment call. It is equivalent to Verbeek and Caffrey’s (2002) “Double Short Caw,” and is included in the “Alert” call of
Chamberlain & Cornwell (1971).
The rough call is always given by individuals moving away from a group. It may serve to discourage further interaction by other group members with the caller; when given toward begging juveniles, they end their begging or change its focus to another adult. Rough calls given in temporally unstructured sequences are directed at juveniles, while structured calls—such as the long-short variant—may also be given to adults. It is probably included in Verbeek and Caffrey’s “Harsh Caw.” I suggest that other such calls
Chamberlain and Cornwell classed as “dispersal” were in fact structured or unstructured rough calls. Not only does the initial caw of their second spectrogram closely resemble a rough call, but I commonly observed individual crows rough-calling while fleeing a group of begging juveniles; often the juveniles briefly pursued them on the wing. In the absence of individual identification, this might readily be interpreted as one crow leading others away from the group with a “dispersal” call.
The fading call is equivalent to the “Medium Caw” of Verbeek and Caffrey, who report the same antiphonal “counter-cawing” between neighboring families that I observed. It is given when families approach one another at the edges of their respective territories; the callers are perched, while other crows may feed or chase members of the neighboring family. Counter-cawing may temporarily define the boundary between 31 territories more clearly and precisely, so that there is less chance of an accidental trespass triggering a serious conflict while families are foraging in close proximity to one another.
The scream call is the typical mobbing call of the American crow, corresponding to Chamberlain and Cornwell’s (1971) “Assembly Call,” and to Verbeek and Caffrey’s
“Harsh Caw.” It is given almost exclusively toward predators or apparent threats, ranging from hawks and skunks to humans who pursue the crows on foot for an extended period of time. It is the only call I recorded that was frequently followed by the approach of crows unrelated to the caller. However, in the cases where there was no mob in flight, as when perching crows screamed at a human or skunk on the ground, I did not observe unrelated crows to enter the family territory of the callers. Interestingly, on one occasion when a juvenile died of disease, several family members gave the scream call for hours, while perched and facing the body.
The nasal call is probably included in Verbeek and Caffrey’s “Long Caw,” although its unusual length exceeds even that reported for the latter. Usually given in flight, its function is unclear, but it may serve to strengthen the message of family members’ overlapping calls. This hypothesis is based on the fact that, when it was given simultaneously with the short call, family members approached the callers more quickly than when the short call was given alone. Another possible message of the nasal call is a signal of arrival on the territory in response to the short call.
32 The coo functions as an appeasement signal, lowering the level of agitation of the bird to whom it is directed. It is typically directed at babbling juveniles, at begging juveniles by adults who are not carrying food, and from one adult to another after an intrafamilial conflict. The quietness of the call suggests that proximity of caller and receiver is linked to its function.
The rattle, apparently exclusive to females, is a close-range familial assembly call of exceptional urgency. It is given by perched birds, often when humans approach family members on the ground, and results in nearby family members quickly approaching the caller; only when these birds are all perched within a few yards of each other does the caller cease rattling. Unlike the short and double calls, the rattle does not seem to be associated with rallying the group to fight or feed; it seems to be important for compacting a group that may be already engaged in these activities.
The begging call solicits food from family members. I recorded it only from juveniles, but Verbeek and Caffrey (2002), McGowan and Clark (personal communication) report that it is also given by females on the nest, during the breeding season. Fledged juveniles sometimes bring adults various objects, drop them and then beg; if these objects are food items, the adults sometimes respond by picking them up and offering them to the juveniles. This behavior may help juveniles to learn to distinguish between safe and unsafe foods, a distinction that is extremely important for a generalist species like the crow.
33 Babble vocalizations are identified as “song” by E. D. Brown (1979), who suggests that they function in courtship or territorial defense. However, within my study population they were exclusively juvenile vocalizations. Moreover, Brown and
Farabaugh (1997) found that crows “sing” within about a week of fledging, and Parr
(1997) made field observations of such calls only in juvenile and yearling crows. Adult babbling has been primarily observed in captive animals (Brown 1979), whose vocal development may be delayed or incomplete.
Babbling is analogous to “subsong” in other songbirds, and to the babble of human infants. I base this judgment on four observed characteristics of these vocalizations which are used to define “babble” in the bioacoustics literature (Kroodsma
2005), and to identify babble in other species such as the sac-winged bat (Knörnschild et al. 2006). First, the vocalizations contain sounds that are similar to adult calls, but are concatenated into long strings with no apparent pattern. Second, the babble vocalization is usually given outside of the context normally associated with the adult calls. Third, juveniles often babble alone and out of the audible range of any conspecific receiver.
Finally, juveniles stop babbling when they develop an adult vocabulary.
The most marked difference between male and female vocal repertoires was the presence of the rattle in the latter. Rough calls were also predominantly recorded from females, but this may simply reflect the greater amount of time breeding females spend with foraging juveniles. Very few call types were recorded from breeding males. This may be because breeding males in fact use few call types, but it may also be due to 34 recording sample size, if such males were either less vocal or more frequently off- territory and hence less often recorded. My data do not allow me to distinguish between these possibilities.
A number of similarities can be drawn between the vocalizations of American crows and those of other corvids, particularly North American jays. A specifically female rattle has been previously identified in Steller’s and scrub jays (Hope 1980, Strahl
1987). Hope also reports a “bah” call made by juvenile Steller’s jays begging for food, which like the American crow begging call includes a choked gurgle made while actually feeding. Finally, a quiet, lengthy “song” has been described in Steller’s, scrub and blue jays (J.L. Brown 1964, Hope 1980, Kroodsma 2005). Structurally this call is analogous to American crow babble, with concatenated fragments resembling typical adult jay calls
(Kroodsma 2005 p. 187). And although this call has been hypothesized both to function in courtship and to recall juvenile birds to related adults, it is often observed being given by solitary birds and known juveniles (Hope 1980). These parallels suggest that, like that of crows, jay “song” may in fact be juvenile babble.
Male helpers were exceptionally likely to include fading and short calls in their recorded repertoire; in particular, they included fading calls more often than breeders of either sex. They were never observed to give scream calls. Female helpers were at least as likely (though not significantly more so) to include rattles in their repertoire, as were breeding females. This pattern suggests three benefits families may enjoy due to the presence of helpers: assistance in territorial disputes and interactions with other families; 35 increased ability to locate food bonanzas; and early warning of predators and other dangers.
Male helpers are particularly likely to assist in interfamily disputes, and may do so in ways other than vocalization; the single bird I observed to be most physically aggressive during interfamily conflicts was a helper male. Easily recognizable thanks to his wing tags and missing foot, he frequently dove on members of neighboring families.
Female helpers are particularly likely to serve as sentinels. Ward and Low (1997) showed that the time individual urban crows spend scanning for danger varies inversely with the size of their foraging group, suggesting that American crows take turns as sentinels. The presence of female helpers may therefore significantly increase the foraging time available to other adults in the family group.
Although I did not find a call type associated with dispersing a group of crows from a location, my work could be useful for dealing with the negative impact of crow roosts and other aggregations. Several of the call types I described function to attract crows to a location, and playback of these vocalizations could be used to direct crows to locations away from humans and agriculture. Based on my observations I find it unlikely that the “distress calls” that researches have proposed to use to disperse crows would cause them to leave a location. The only calls I recorded which would correspond to distress function to attract other crows to the caller, not disperse them.
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