senescence

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I have had a lot to say about male loons and their experience. Indeed, the fact that the male decides where to place the nest means that he develops a tight bond to his familiar territory and fights hard — harder than his mate — to keep it.

But females too play a vital role in breeding success (like the pictured female photographed by Linda Grenzer on Bear Lake). How might female experience affect the outcome of a nesting attempt? Now that I have begun a detailed analysis of causes of breeding success and failure, I have started to ferret out the difference that female experience makes. I am only halfway done, but I can already see that the number of years a female has spent on her territory strongly affects the date her chicks hatch. As the graph below shows, females that have just arrived on a new territory — because they have evicted the previous female owner or replaced a dead one — have an average hatching

date of 22 June. In contrast, 4-year veterans on territories hatch their eggs, on average, 5 days earlier — June 17th. Now this might not sound like much of a difference in hatching date. But when you are tasked with stuffing your voracious chicks with fish, watching them grow rapidly to adult size, and hoping they get proficient enough at foraging, flying, and avoiding trouble to eke out a successful migratory flight to Florida, you take every extra day you can get!

You might ask: “Does this delay occur because of female inexperience with breeding in general or does it come about because of lack of experience on a specific territory?” The delay seems to be associated with lack of familiarity with a specific territory, because females that pick up stakes and move to new territories show delays in hatching date just like the ones they suffered on their first territories.

The cause of the improvement in nesting schedule with experience is likely to be energetic. That is, a female that knows how and where to find food on a lake is able to recover from spring migration quickly and begin the lengthy and arduous process of raising chicks. A female that is still learning where to find food on her new lake spends extra time before she reaches a suitable body condition to commence breeding.

Don’t male loons have just as big a problem restoring their body condition and thus readying themselves for a nesting attempt? Perhaps. But males experience minimal breeding costs until they begin joint incubation duties with females. Apparently males’ energetic deficit from migration does not hinder the breeding schedule.

You probably noticed that the graph depicts a curve, not a line. Older age-classes of females — those that have spent 5 or more years on a territory — actually begin to nest later than females that have spent 4 or fewer years there. What on Earth could explain this peculiar pattern?

Since it makes little sense that a female’s experience on a territory could begin to work against her after several years, we must look beyond experience for an explanation. The later hatching dates of more experienced females probably arise from reproductive senescence — a decline in reproductive performance that occurs with advancing age. Senescence is well-known in mammals and also many birds. We should not be surprised to see such a pattern in loons.

It is exciting to discover and ponder the reproductive quirks of female loons. Like many of our findings, this one only became visible because we studied thousands of nests, by hundreds of marked loons, across decades of their breeding lives. That, of course, is our bread and butter.

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The Nose Lake male I observed today had a conspicuous scar on his head. This particular scar, which I dutifully sketched on my datasheet, was located on the right side of his head, behind and beneath the eye. In comparison, the head of the Nose Lake female was sleek and without blemish. Scarred males paired with pristinely-plumaged females are a common sight. In fact, the scar I recorded today was the 72nd of the study – and the 63rd seen on a male. Moreover, this scar has persisted for a month; Linda photographed this bird on May 6th, and the scar was obvious then.

Scars on heads of males, which occur when they grasp each others’ heads and necks in a territorial battle, bring to mind the short, violent lives that many males lead. Slowly and surely, we are beginning to understand why male battles are fiercer than female battles. Part of the explanation for this pattern has to do with nesting behavior. We know from analysis of nesting behavior among color-marked breeding pairs that male loons control the placement of the nest. While we do not know why males control nestsite placement, we can see that male control of nest placement cranks up the stakes for male territorial battles. Why? Because male loons learn by trial and error where to place the nest. Once a male has nested successfully on a territory, he reuses that good nest location again and again, boosting his hatching success. Therefore, once established on a territory where he has nested successfully, a male has a large stake in holding that familiar territory. If evicted from there, the male must relearn where to nest and where not to nest on a new territory, which costs him precious time and energy. In contrast, females, which do not control nest placement, can freely move from one territory to another without paying a penalty in lost familiarity and, hence, breeding success. Since one territory is, in effect, as good as another to them, females should fight less hard than males to remain on a territory – and they behave as predicted.

A second part of the explanation for violent male battles is rapid senescence. Again, while we do not yet understand why males should age so badly, compared to females, the contrast in senescence has strong implications for male behavior. A male reaches a point – in his mid-teens typically —  where he is in rapid decline. That is, he is losing body condition and is at great risk for losing his territory. With the future offering little reproductive promise, many males in their mid-teens increase their aggressiveness and territory defense so that they can squeeze another year or two of breeding out of their territory. This, of course, is the terminal investment finding that I have been blogging about for the past months. (By the way, that paper has just been published online.)

With two factors – male nestsite selection and senescence – at play, we can begin to understand why males might be so violent. The factors are additive. A fifteen year-old male on a familiar territory is both falling into decline and facing a steep loss in breeding success, if evicted. So he has two good reasons to fight like hell to hang on.

 

 

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I have always loved working in the field. While others remain indoors, chained to their desks and computers, much of my work requires paddling canoes on beautiful lakes to record behavior of loons. It is a dream job. Recent findings, though, are forcing us back into the laboratory.

Why must we return to the lab? Most of you know already from recent posts that male loons senesce dramatically in their mid teens and that they also become aggressive at that age. But the fact that males decline, whereas females do not, raises vexing questions about underlying physiological causes of male decline. Does male health hit the skids because of the cumulative impact of blood parasites? Does the greater body size of males make it more difficult for them to maintain good health throughout their lives? Is male decline linked in some fashion to conditions faced during the chick phase? As always happens in science, one finding, even a very clear one, raises a legion of related questions.

Fortunately, we can answer many such questions by taking small blood samples from our loons at the time of capture. Jeremy Spool, a soon-to-be-Ph.D. from University of Wisconsin-Madison, supervised the taking of these samples, which can tell us about hormone levels, parasites, and genetic patterns. Jeremy also completed a preliminary wave of analyses and has made an interesting discovery with regards to telomeres.

First some background. Telomeres are “end caps” on chromosomes — composed of many repeated DNA sequences — that protect chromosomes when they are replicated during cell division. In both humans and loons, the sequence of repeated DNA building blocks (nucleotides) that comprise telomeres is the same: TTAGGG. Telomeres grow shorter with age and with illness in humans and many other animals. Human babies have chromosomes capped with about 2,500 repeats of TTAGGG; older humans have only about 800 such repeats. A number of researchers have found that shortening of telomeres is related to stressful conditions faced by non-human animals. For example, one study reported that cormorants and albatrosses hatched late in the breeding season showed greater shortening of telomeres — possibly indicating more rapid aging — than did individuals born early in the breeding season. A good deal of work remains to be done on telomeres to determine if they can predict patterns of aging and body condition, but there are some promising signs that they can do so.

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Jeremy analyzed telomere length in loon blood samples from 2017 to see if: 1) telomere length was correlated with age, and 2) males and females differed in telomere length. He noted a weak tendency for male telomeres to shorten with age. We will have to add more data to see if the pattern holds up. On the other hand, Jeremy also found that females had telomeres significantly longer than those of males (see figure, above). Since we know that female loons live longer than males and do not experience a sudden decline in condition in their mid teens, this pattern is as we might have predicted.

What does the telomere pattern tell us? While it is vaguely comforting to find a physiological correlate to confirm the difference in aging pattern between male and female loons, telomere shortening is still a mystery in animals generally — and most certainly in loons. We can draw no immediate link between short telomeres and any other aspect of physiology, like parasite load, immunological capacity, or even age. But the male/female difference gives us hope that telomeres might predict body condition, disease resistance, and/or life expectancy, within each sex. If so, then measuring of males’ telomeres might permit us to predict if and when they are near death and should begin behaving aggressively — to allow themselves one last desperate reproductive gasp. Moreover, if young loons, like cormorants, pay a price by losing some of their telomeres from the stress of being hatched late in a breeding season, then differences in hatching date might help us solve the enduring mystery of why some male loons cannot survive past their mid teens, while others thrive well into their 20s.

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It is a bit unseemly, I suppose, to pile on Russia now. Having been caught meddling with our election and cheating during past Olympics, their reputation could hardly get worse. Yet the metaphor of the Russian judge — meaning a person who brings a strong bias to a process that is supposed to be marked by disinterested fairness and good judgment – is almost irresistible to me at this juncture. Indeed, the metaphor has been throbbing in my brain these past weeks as I have marveled at the scores awarded to figure skaters and Big Air snowboarders.

Let me explain. I recently completed a revision of our paper on terminal investment by male loons: the most remarkable finding we have made in 25 years of research. (This is the paper showing that males become highly aggressive and territorial at the same time that their health, survival, and territory defense is declining.) Praised by three reviewers at a prestigious journal, our paper was blocked from acceptance by a fourth reviewer who insisted that we complete a complex statistical analysis to check our results. Review of scientific articles is almost always anonymous, as in this case, so we cannot know the reviewer’s identity or the reason for his/her objection. But my study of his/her statistical point convinced me that it was mistaken. Yet, the editor disregarded my carefully-crafted refutation and chose to support the reviewer. Of course, it is immensely frustrating for an author when an editor sides with a stubborn reviewer. This outcome forced us into a difficult decision: 1) kowtow to the reviewer by reworking our statistical analysis needlessly, which would have entailed a lengthy delay in publication and cost us perhaps $2000 to hire a statistical consultant, or 2) pull the plug on the submission that seemed on the brink of acceptance, pending completion of that difficult statistical revision. I hope I made the right call by withdrawing the paper and sending it to a new journal.

Two factors played a role in my decision to withdraw the paper that, perhaps, should not have. First, I have spent many months polishing this paper and am reaching the end of my rope with it. I am certain that it is sound statistically and likely to be impactful in my field, if I can just navigate the stormy seas of reviewer opinion. Second, I must soon turn my attention to acquiring new research funding and must have this paper in print in order to demonstrate to funding agencies that the past funds they have sent to me have been well spent. Thus, I have chosen to send the paper to a solid – but not highly prestigious – journal in my field, hoping to find a fast track to publication.

I am not the first person to make a decision to publish a great paper in a low-impact journal in order to keep the wheels of research turning. Each paper, in my experience, follows its own journey. A pedestrian paper sometimes catches a wave and ends up in a lofty journal, only to be scoffed at and forgotten in short order. And cool papers sometimes fall into low‑impact journals, are discovered by many scientists, and become classics. Let’s hope the terminal investment paper falls into the latter category.

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I have just completed my paper on black flies. The paper presents evidence that black flies cause nest abandonment, which was lacking in the literature before. The evidence is pretty convincing, I believe. (We shall see what my scientific colleagues think when I submit the work for publication in the next week.)

In the course of looking at black fly impacts on nesting, I stumbled into two  interesting findings. These findings were serendipitous, like much of what scientists report. That is, I was keenly focused on one topic — black flies and nest abandonment — when I made a finding related to another topic — other causes of abandonment. In fact, I analyzed statistically a whole set of factors, some seemingly unrelated to black flies, that might have predicted nest abandonment. Among these were age of the male, age of the female, duration of the pair bond between them, exposure to wind (which might have kept the flies at bay), size of breeding lake, and distance from the nest to the nearest flowing water (from which black flies emerge as adults).

I was excited, but also baffled, to discover two new predictors of nest abandonment. First, pairs on large lakes are less prone to nest abandonment than pairs on small lakes. Second, pairs containing an old female are far more likely to abandon a nest owing to black flies than are pairs containing young females.

Now, I like to think that I know everything about loons. When I am visiting a study lake and someone asks an easy one like, “Do loons mate for life?”, I puff myself up, lower my voice an octave, affect a mild British accent, and pontificate on the serially monogamous breeding system of Gavia immer. But I was wholly wrong-footed by these two new findings. I had been so laser-focused on black flies as the prime movers in nest abandonment that I had included age and lake size in the analysis almost as an afterthought. I had not even considered what it would mean to learn that age and lake size were significant predictors.

The statistical significance of lake size as a predictor of abandonment forced me to confront a complex variable. If numbers of black flies are correlated with nest abandonment (as they are), then it requires no great conceptual leap to infer that black fly harassment is causing loons to abandon their nests. But the fact that lake size predicts abandonment opens up a much broader range of explanations, because lake size is correlated with degree of human recreation, pH, wind exposure, wave action, available food, and numerous other factors. Having picked through the possibilities, an energetic explanation seems most likely to explain the lake size pattern. That is, large lakes provide more food than small lakes, so loon pairs on large lakes should be in better health and condition than those on small lakes. Well-fed, healthy adults with strong immune systems should be better able to cope with the blood loss and exposure to blood-borne pathogens (like Leucocytozoon protozoans, which cause a malaria-like disease in birds) than under-nourished individuals with weaker immune systems.

What about the higher abandonment rate of pairs that contain an old female? Here again, energetics might be the key. Old females senesce — they experience much lower survival and slightly higher vulnerability to eviction than young females. So it stands to reason that old females are in poorer body condition and are more likely to abandon nests when attacked viciously by black flies. Reproductive decline among old females is widespread in animals, and the tendency of old female loons to abandon nests more readily seems consistent with that pattern.

But what about males? As I have emphasized in recent blog posts, males senesce even more dramatically than females do. How is it possible that old males can continue to incubate eggs when being bitten mercilessly by black flies when old females cannot? Terminal investment appears to be the answer. Terminal investment — efforts to increase breeding output as death approaches — occurs only among male loons, even though both sexes senesce. As the months have passed, we have learned that male loons not only become hyper-aggressive when they reach old age (15 years) in an apparent attempt to hold their territory for another year or two of breeding, they also seem to show a more subtle willingness to try harder to hatch eggs and rear young to fledging. The new finding showing that old males do not abandon nests as readily as old females when beset by black flies is thus part of a growing pattern.

My tentative explanations for the impacts of lake size and sex on nest abandonment are not the end of the story, of course. Rather, they raise more vexing questions. Why on earth would a loon settle to breed on a small lake, when small lakes doom loons to poorer body condition, a higher rate of abandonment, and the likelihood of losing one or both chicks in the event they can hatch the eggs? And even if the higher rate abandonment of nests by old females fits a growing pattern, why do males and females differ so much in their life-history strategy? We do not know….and this is why I love my work!

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Our paper that describes basic features of senescence has been accepted for publication Journal of Avian Biology. With the lightning-fast turnarounds and early views that the public is now granted to scientific articles, you can search for the paper and read an advance copy…months before copy-editing and proofing of the final version is done. Let me know if you find any typos!Screen Shot 2017-03-10 at 12.47.06 PM

The paper describes findings that I have been blogging about for some months now. First, both sexes of loons senesce (begin to die at a high rate) once they reach their mid-20s. Second, at first blush it seems that the sexes do not differ substantially in the senescence pattern. Third, this paper looks only at territory holders, which are the creme de la creme of adult loons, because they have not only survived to adulthood, but also claimed a territory and produced chicks there. Thus, this group of birds analyzed does not include the many adults who tried but failed to settle on a territory or settled briefly but did not reproduce. Fourth, old males (but not females) suffer a decline in territory resettlement after being evicted from a territory. Finally, we present in the paper preliminary evidence that suggests male might increase or at least maintain high breeding success at advanced age, while it seems that females fall into reproductive decline. So there is a glimmer of possible terminal investment by males (increased investment by animals near death) at which this paper hints. If you have followed my blog, you know that we have data from a separate analysis that deals more directly with the possibility of terminal investment by males.

That is all I have for now. I have just finished hiring the four field staff members for this year. They are a strong bunch and include one of our seasoned hands from 2016. Since we are on the verge of ice-out already, I have gotten the crew hired none too soon. By the time most of us arrive in May, nesting will be well underway. No matter. We are accustomed to scrambling to keep up with the loons.

See you out on the lakes!