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Friday, July 10, 2009

Death, visitations, and dance of "solidarity"

---For July 2 photos on Christy Yuncker Photo Journal, click here.

On July 2, 2009, we were aroused at 7 AM by unison calling of Roy and Millie. 

Twin colts, Jacques and Phyl, had trailed their parents around our cranberry bog for almost three weeks since hatch on June 10th and 11th

When we glanced at Cattail Point on that morning of July 2, we saw only Jacques running back and forth between his parents, begging for food. The adults flapped their wings twice, peered down at a tawny mass half-hidden in the grass, preened, and shuffled around. After careful examination through a spotting scope, we saw that the object of their gaze was Phyl's motionless body. The photo to the left shows Millie looking down at Phyl.

In the following hour, the three cranes foraged for insects in the grass. Then at 8 AM, the adults exchanged unison calls with a part of cranes across the valley while Jacques watched (below).

At 10 PM on the previous evening, both colts went to sleep as usual, snuggled under Millie's wings at the habitual family roosting site. 

Phyl's immobility was not a total surprise to us. The temperature on the first of July was almost 80º F, hot for Interior Alaska. All day Phyl lagged 10-15 meters behind the rest as they foraged and when they paused, she sat down. Jacques followed close upon the heels of his parents and thus garnered most of the insects. Periodically, Millie carried a dragonfly back to Phyl and she ate (pictured below). We don't know whether these tidbits provided sufficient nourishment for her needs, but later Jacques, Phyl and their parents shared a hearty supper of fresh duckling provided by Roy (another duck feast was described in the previous blogpost) before all repaired to Cattail Point. Jacques pecked very gently at Millie's shoulder; she sat down in the tall grass, and both colts slipped under her wings. 

Phyl did not arise to forage with Jacques in the morning, and we could not tell whether Phyl was alive or dead.The events of July 2 reminded us of behavior we saw in 2004 on the day before the colt named Woodstock died. At that time in 2004, the twin colts were 2.5 months old. On Woodstock's next-to-last day, he often huddled on the ground with head under wing. At least once, Peter Pan, the stronger colt, went over to Woodstock, settled down next to him, and spent many minutes looking at his twin, as seen in the picture below. We saw no full-blown agonistic displays or serious fighting between healthy and failing colts in 2004 or 2009. [Note added: No antagonism between healthy and dying colt in 2010 either.]  After Woodstock's death, our notes show that the parents carefully examined the corpse, but we do not have extended observations like those for Phyl's death in 2009. Phyl's death (or incapacity followed by death) profoundly affected the behavior of Millie and Roy. It evoked memories of the poignant PBS Nature depictions of an obsessive female chimpanzee who carried the corpse of her deceased infant for many days. Unusual behaviors associated with dying or death have been reported for many species, including primates1 and elephants2.
[See also the Comment below from Roger Payne, who describes the behavior of two helper whales when another whale is ill or dying. As to what emotion underlies such behavior, Roger prudently notes: "I think that the only answer is that we still don't know what emotions species experience..."]
We can't put ourselves inside the head of another species, but behavior reflects physiology.  The cranes' behavior on July 2nd indisputably reflected their arousal and is consistent with a distressed emotional state. Repeatedly, Roy and Millie interrupted their foraging to return to the Cattail Point and to linger near Phyl in what we term a "visitation". At the end of the day, all three cranes danced with fierce intensity.

Five minutes after the family had begun their first morning dragonfly safari, Roy returned alone to Cattail Point to stand next to Phyl. Once there, he craned his neck and peered at the fluffy
colt for about five minutes. He appeared to offer an insect to the ground; then he rejoined the hunt in the deep grass. Six minutes later, all three cranes stopped harvesting insects and came back to Phyl. Roy and Jacques stayed briefly but Millie spent 28 minutes preening.

Diverse authors have recounted behavioral disruption after the death of a related crane.  One of the earliest dates from about 500 BC. The Ramayana, one of the great Sanskrit epic poems of India, describes similar behavior after the death of a Sarus Crane. In this classic, the Hindu sage Valmiki recounts the anguish of a female Sarus who wailed interminably after her mate had been killed by a hunter3. Likewise after the death of his mate a few decades ago, a Red-crowned Crane stood vigil for days over her frozen corpse in the demilitarized zone between North and South Korea (see George Archibald's comment below). Finally, Eugenia Bragina (comment below) reports that Siberian Crane parents were attentive to the corpses of colts at the Oka Crane Breeding Center.

Were these visitations of Roy and Millie in 2009 merely to check Phyl's status? Perhaps she was still alive but incapacitated and they were waiting for Phyl to revive?  During their many visits to Phyl's body, there was no hint of scavenging nor any behavior remotely resembling the savage butchering of the duckling on the previous evening. 

Roy visited Cattail Point briefly three more times (2, 7, and 15 minutes) in the morning, sometimes uttering low vocalizations that were just audible to us one hundred meters away. Shortly after he rejoined the others in foraging, it became Millie's turn to visit Cattail Point. She preened, walked around Phyl, examined her closely, and bent down so that the underside of her beak was close to the immobile mass of feathers. She made two more visitations (2 and 7 minutes). At noon, the whole family walked over to the roost site. In the picture above, the adults are preening. Phyl is in the grass to Jacques' left.

In the early afternoon, the family hunted. At 3:15 PM, Roy spent 45 minutes in Phyl's vicinity, looking, preening, stepping around her body, and then somewhat curiously, going through ritualized slow head movements: turning left, bending down and picking up something (perhaps a piece of grass, a twig or blade of cattail), and then turning right, bending down, and apparently dropping the object.
The motor pattern was indistinguishable from nest-building that we have watched each May. He repeated the sequence as if he was starting to make a pile of grass beside the body. Then Roy shifted slightly to one side and made another "pile" in a new place. In the picture below, Phyl is barely distinguishable in the grass at lower right corner. Roy stands on guard and Millie is bending down in a typical nest building stance as she holds a brownish bit of cattail blade in her beak.
In her Master's thesis written over thirty years ago, Karen Voss described repetitive ritualized placement of twigs and grass when Greater Sandhill Cranes built their nests in Wisconsin. She also observed ritualized nest-building in 6-month-old cranes, even though these young birds had no actual nest site.4 But for this July 2 episode, we haven't seen nest building behaviors except in early May.

There were more visitations in
late afternoon and early evening. Four more times, Millie or Roy initiated grass-piling bouts. In three cases, the pile, had it been visible, would be located beside Phyl and once on top of her body. Just before roosting time, all three cranes walked to bog central and foraged.
The sun was sinking behind the west ridge, creating long shadows like that produced by Roy's neck (above) and broad bright and dull stripes across the grass (below).

At 9:52 PM, Roy stepped into a stripe of sunlight, jumped, and all three cranes began to dance explosively. They danced and danced and danced on the dramatically side-lit grassy stage. Even Jacques, barely three weeks old, joined in with gusto. Fortuitously, Christy's cameras were focused on bog central when the dance erupted for three minutes and 107 photographs. After the dance coda, Roy walked forward into shadow and stood for a minute or more. Then all three cranes returned to roost at Cattail Point. Roy slept standing on one leg; Millie settled down next to Phyl's body, and Jacques climbed under her wing. For more images go to Christy Yuncker Photo Journal.
The memorable dance was neither frenetic nor flailing. It was extended in duration, intense, and very fast, but the moves were controlled, fluid, graceful, and balanced. Each bird exhibited with high energy, and yet all three were attuned. The photo above shows Roy as he dashed from the right in front of Millie who is at the apex of a spectacular Run-flap-glide with wings held straight out. As she landed, Roy wheeled to face her and bowed in a Wing-spread-forward-tilt display (see Quicktime movie below). Then he spread his wings, jumped, and turned left to engage Jacques in a Wing-spread-hold face-off. The movie below shows a 4 second segment of the overall dance that lasted 160 seconds. See also the link to our Photo Gallery.

The intensity and duration of the dancing after the death of Phyl strongly suggests that dancing provides emotional release for cranes. It is widely recognized that dancing strengthens and reaffirms the pair-bond, and in this instance, dancing probably reinforced family solidarity and and promoted continuity.

All summer from May into August, Roy replaces his flight feathers, one-by-one. During the vigorous dancing, several old feathers fell out and floated to the grass. The photo below was taken just after the finale of the solidarity dance. Roy is walking toward us. A loose whitish primary feather that is dropping from his left wing has been highlighted by the sunlight.
In the days since, Roy and Millie carry on as characteristically attentive crane parents, feeding and guarding Jacques as they guide his progress through core subjects of Foraging and Display/Dance.

When we first posted this blog, it had been a week since Phyl died. We had seen no dancing during that entire week. We monitored the pond all day; Phyl's body was not scavenged nor did the crane family returned to Cattail Point. After July 2, the cranes began to roost 50 meters to the east.

The photo to the right shows Phyl's skeletonized corpse on August 10 - 6 weeks after her death. Insects and bacteria have cleaned away flesh, but the body is still not scavenged.

For us, July 2 is unforgettable - repeated visitations to Phyl's body climaxed by what we call the Dance of Solidarity.

There are so many aspects of such behavior that need further study and explanation. For example, what is the adaptive significance of the ritualized grass-piling behavior?
    1. For re-nesting? The grass-piling could be tentative restarting of nest-building in response to death of an offspring. In this context, "death of a colt" (reproductive failure) leads cranes to initiate another reproductive cycle. When eggs fail to hatch, a second nesting is common at lower latitudes where summer seasons are longer than Alaska.
    2. For concealing the body? The grass-piling might be like a motor behavior module, a sequence of postures and movements driven by neural circuitry (a fixed-action pattern in classical ethology). Such a piling module could be used to build a nest or to hide a corpse that might otherwise atttract predators to the nest territory.
    3. For grieving? Piling could be part of animal version of grieving behavior. Marc Bekoff has reported similar "funeral" incidents, in magpies (standing vigil for several minutes and piling grasses near a dead magpie at the side of a road)5 and in a fox (piling dirt on the corpse of a fox killed by a cougar).6 Perhaps ritualized piling behavior has deep evolutionary roots and is somehow hard-wired in the nervous systems of birds and mammals?
    4. Merely a general expression of stress? In classical ethological terminology, piling might be displacement behavior, as suggested by the comment below from Eugenia Bragina. George Archibald notes below that cranes dance when they are upset by some event, such as the approach of a predator. Perhaps grass-piling and the intense dance simply reflect emotional stress.
Emotions have physiological bases. In humans, grief behaviors include lethargy, subdued responsiveness, and bouts of wild emotional release. When medical researchers image the brains of people in bereavement, they see localized brain centers light-up in MRI scans and proinflammatory cytokines increase as well.7,8 Since both birds and mammals descended from primitive reptiles, their brains have similar basic architectures, but the final placements of cognitive brain centers evolved along different trajectories. Facile generalization from human data to bird neuroscience is not legitimate since similarities in detailed function of the higher cognitive centers are unproven. But from a behavioral perspective, the visitation bouts and solidarity dancing in cranes show parallels with human grieving - in some senses, reminiscent of an Irish wake. Putative parallels in physiological correlates, such as inflammation and activation of brain nuclei, are intriguing starting points for further comparative research.
In the words of Peter Marler9:

"...emotion-based displays can of course convey a lot of information."
We suspect that both emotional and cognitive factors contributed to the displays and other behaviors we witnessed after the death of Phyl.

We know that Phyl expired sometime on July 2, but we can't determine the exact hour or minute. The parent visitations over the day might have been for monitoring a dying colt (the behavioral expression of crane solicitude) or grieving at her death. The prolonged dance at day's end certainly reflects arousal that stems from heightened intensity in the crane version of emotion. Some may contend that it is presumptuous to apply a term like grieving with its subjective overtones, because we cannot precisely specify the underlying physiological correlates. But passing off these striking behaviors as mere "displacement" flies in the face of the evidence. 

We welcome your reactions to our blog. If you have relevant interpretations or observations that you are willing to share with others, either click on the word "Comment" at the bottom of this blog or email us directly. With your permission, we will paste your email as a Comment below. 

August 2013 addendum

Recent publications on vertebrate reactions to death should be considered: 

Corvid funerals - In 2012, T I Iglesias10 and her colleagues at UC-Davis investigated the crowds of scrub jays  that collect briefly and emit noisy calls at the site of a dead bird of the same species. The animals gather, scream at the body, and then disperse.  These aggregations, often called "funerals" (of jays, crows, or ravens) have been reported many times11.  There need be no close prior association between the dead individual and the noisy living screamers.  Dr. Iglesias' group concluded:
"Our results show that without witnessing the struggle and manner of death, the sight of a dead conspecific is used as public information and that this information is actively shared with conspecifics and used to reduce exposure to risk."
So it appears that the widely cited "corvid funerals" are a mobbing reaction to danger and do not reflect "social grieving". 

Animal Mourning - In 2013, Barbara King, an anthropologist at the College of William and Mary has published a very nice little book entitled How Animals Grieve12 and also an article in the July 2013 Scientific American13 which discussed grief and mourning in mammals and birds. She suggests that two criteria distinguish animal grief:
  1. A distinct change in behavior in response to the death of an individual, and 
  2. A close prior association between the dead animal/bird and the mourner.
In the Scientific American article, she further states:   .
"Love in the animal world often entwines with grief in an acute mutuality. Perhaps even more than the degree of social cohesion within a species, it is love between individuals that predicts when grief will be expressed."
We believe that the Sandhill Crane behaviors that followed the demise of Phyl reflect grief, since they fit Dr. King's criteria.

December 2015 addendum

Whale response to death of a calf - offered on Youtube by Rodrigo Friscione Wyssmann in December 2015.

Wyssmann notes: "The whale on the left is an adult female. The one on the right is her male escort. We were on our way to Roca Partida when we heard that the female's calf had been attacked by a few killer whales. When we got there, the mother was inconsolable. The male was trying to comfort her by touching her gently, but it was useless. Some of you may already know this, but it's only the male whales who sing (while mating), so this was obviously a devastating and silent moment. The man holding the camera is my father." 

References cited:
1. Citations in LiveScience column entitled "Grief: the price of love" by Meridith F. Small.
2. Citations on Elephant information website.
3. Hammer N 2009. Why Sarus Cranes epitomize Karunarasa in the Ramayana. Journal of the Royal Asiatic Society, Ser 3 19:187-211. See also Ali S, Ripley SR 1983. Handbook of the Birds of India and Pakistan, Compact Edition, II. Delhi, Oxford University Press.
4. Voss KS 1976. Behavior of the greater sandhill crane. Thesis for Master of Science in Zoology, University of Wisconsin-Madison.
4. Bekoff M. 2007. Are you feeling what I'm feeling? New Scientist. 26 May 2007, p. 44 (Grief).
6. Bekoff M. 2009. A fox, a cougar, and a funeral. Psychology Today blog
7. O'Connor MF, Irwin MR, Wellisch DK 2009. When grief heats up: Pro-inflammatory cytokines predict regional brain activation. Neuroimage May 29 Epub.
8. O'Connor MF, Wellisch DK, Stanton AL, Eisenberger NI, Irwin MR, Lieberman MD, 2008. Craving love? Enduring grief activates brain's reward center. Neuroimage 42:969-72.
9. Marler P 2004. Bird songs: a cornucopia for communication. In Nature's Music: The Science of Bird Song, P. Marler & H Slabbenkoorn (eds.),132-177. Elsevier, Amsterdam, p. 172.
10. Iglesias TL, McElreath R, Patricelli GL 2012. Western scrub-jay funerals: cacophonous aggregations in response to dead conspecifics. Animal Behaviour 84:1103-1111.
11. Beckhoff M 2008. The Emotional Lives of Animals: A Leading Scientist Explores Animal Joy, Sorrow, and Empathy - and Why They Matter. Ne World Library
12. King BJ 2013. How Animals Grieve. University of Chicago Press
13. King BJ 2013 When animals mourn. Scientific American. July  308(7):62-67.

Revised April 16, 2010, August 30, 2013, and December 11, 2015.
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  1. Dear Christy and George,

    Thanks for your wonderful blog and web site. The story about the loss of Phyl and the visitations and dancing that followed is quite remarkable. Your photos and behavior descriptions are excellent. Thanks for sharing!

    You might enjoy reading "The Music of Wild Birds" illustrated by Judy Pelikan, adapted from the "Field Book of Wild Birds and Their Music", by F. Schuyler Mathews (1904). This lovely book was published by Algonquin Books in 2004. Mathews was a naturalist/musician who wrote musical notations for the individual songs of many birds. His account about the song sparrow describes a male singer that changed his song from major to minor key, after his mate disappeared. Mathews was convinced that the male was grieving the loss of mate, as the song was a sad tune compared to the usual cheerful song that he was very familiar with. He provides musical notations for each song.

    Regards to Roy, Millie and Jacque.

    Debbie S. Miller

  2. This comment is pasted from an email written by George Archibald.

    Dear George and Christy,

    Thank you very much for sharing this remarkable story with me.

    Inspecting the corpse happened once with Red-crowned Cranes on the Korean DMZ. The female of a pair died from unknown causes and the male remained for many days beside the frozen corpse. When it was obviously weakening from starvation, the soldiers captured, force fed and revived the living crane and sent the mummified carcass of the mate to me with the question, “Why did this crane die?” By the time the rescued bird recovered it was late spring and the other cranes had migrated. Fearing the captured crane’s flight strength would be inadequate, the army asked Lufthansa Airline to take the crane to Russia and have it released on the breeding grounds in southeastern Siberia. The bird arrived safely in Moscow and today lives at the Moscow Zoo.

    There are a number of reports of a survivor remaining for extended periods near the corpse of the mate. Perhaps the evolutionary gain from a super-strong bond with a mate (that is they produce many offspring) outweighs the loss of perishing from starvation if the mate dies. This is also the reasoning behind the reason birds sometimes incubate addled eggs for weeks beyond the hatch date. The evolutionary gain of being a tight and persistent incubator outweighs the loss of incubating until the eggs explode!

    Cranes dance intensively when they are developing a relationship with a new mate, when they are synchronizing hormonal and behavioral states prior to copulating, and when they are nervous. Perhaps the latter was the primary motivator for the remarkable dance you witnessed. I have seen cranes dance intensively when approached by humans and predators. Your cranes definitely were upset and they expressed that emotion by dancing. So being upset over the death of their colt is perhaps a type of mourning.

    Warm wishes and hoping for a successful fledging of Jacques.

    Warm wishes,

    Dr. George Archibald
    International Crane Foundation
    E 11376 Shady Lane Road
    Baraboo, WI 53913.

  3. This comment is posted from an email to us (July 25, 2009) of Eugenia Bragina, Biological Faculty, Department of Vertebrate Zoology, Moscow State University.
    Hi George...,
    Cranes also pay much attention to such accident. We worked in Oka Crane Breeding Center where captive cranes breed every year. When staff take out a chick (for example, for release to nature), the poor parents call some days very intensively; they emit sounds every some minutes. You can imagine an energetic cost of such behavior. If the body of a dead chick remains in the enclosure of its parents they often bent forward and touched it. Usually the staff quickly takes out corpses so I don't know how much time parents would stay near it. Building of new nests may be connected with new reproduction. As I know about the South of USA, Sandhill Cranes have time to repeat a breeding after death of hatch/chicks. It may be displacement activity too because you describe many attempts on different places.
    I forwarded your letter to Tatiana Kashensteva, Head of Oka Crane Breeding Center, maybe she will add some comments.
    Best regards,

  4. From: Payne Roger []

    Hi George,
    Thank you for your interesting blogs. I read all that I found on line and looked at the pictures. Having not been present myself I have no faith in my ability to form an opinion about the activities you saw or their possible meaning. The trouble, of course, is that there are many interpretations that might fit what you saw, grief being just one of them, and there is danger in trying because there are terrible exceptions to one's preconceptions. Here's one of them and it concerns whales (which you ask about).

    Only a few whale species undergo mass strandings and those that do it and that have been studied in any detail show that there is usually a large adult (female or male) who is in obvious distress, and is often flanked by two other adults who help lift its head high enough above the water so it can breathe. All the other members of the pod wait patiently next to the trio that includes the sick individual until the sick one recovers or dies. This can go on for hours, even days which means that when the tide goes out everyone strands and most pod members die from overheating. However, nowadays lucky pods of mass-stranded whales get found by whale lovers who baste them with water and pile on wet towels to keep them cool through the low tides. So when the tide returns the healthy individuals are still alive. At that point they move around slowly, and re-strand in some other new position very close by (a position that also strands them at low tide). When the sick individual dies everybody leaves. There are two obvious interpretations: 1) that they love the dying individual, are grieving for it, and will not leave it to die alone. 2) (And it is this I find more likely) they are afraid to leave the dying individual because it has enforced its dominance by attacking or biting them whenever they tried to avoid it (evidenced by tooth marks which appear to come from the same large individual and that are present on almost everyone in the pod. Most species that strand are harem species. Harem masters of many species enforce their dominance with violence. In a word: they are monsters. One way that harem bulls in male furseal harems punish females who attempt to leave their harem is that they kill them. At the very least they bite her viciously if they can catch her. My suspicion is that no one in the pod of whales with the dying leader dares to leave the dying tyrant until they are damn sure that he's dead and won't come after them. I would prefer to think that it was grieving that kept the whales around a dying companion, but fear fits all the totality of observations better. I have described it here because I think it points out how hard it is to know what any behavior really indicates.

    I think that the only answer is that we still don't know what emotions species experience, even though we would all love to, and although we all probably believe at some level in our private thoughts that whales experience major emotions such as grieving. But I am reminded about the exchange between William Randolf Hearst and Arthur C. Clarke. Hearst cabled Clarke: "Is their life on Mars? Cable thousand words." Clarke responded: "Nobody knows. Repeat 500 times." So I suggest that when it come to guessing what an animal is feeling that we all repeat 500 times: "Nobody knows."

    Thanks for bringing your story to my attention.

    Best wishes,


  5. I followed Karin Franzen's link to your journal and blog. I very much enjoyed your photos and your account of Roy and Millie's activities. Over the last year or so I have become more interested in the sandhill cranes. Last fall we had a family of three visit our neighborhood every morning. I am hoping they will visit again this year. I'll be back again to hear more about Roy and Millie and the little one.

  6. It was elucidating to read this journal of this sandhill crane family. The reason I even happened on your sight was a dream. I had a sandhill crane nestle down next to me in my dream and contentedly sleep. Of course, I awoke wondering what sort of bird it was. I kept searching pictures and discovered that is was the sandhill crane. Your blog was very touching. I love animals and especially birds. Thank you.