Plants Can’t Talk. But Some Fruits Say ‘Eat Me’ to Animals.

Two national parks in Uganda and Madagascar presented researchers with a

natural experiment to understand how plants have adapted to appeal to animals
that spread their seeds.

Image
Some plants in Madagascar may have evolved fruit colors so that they can be
seen by lemurs that are red-green colorblind.CreditCreditAndy Davies/Science
Source

By JoAnna Klein
 Oct. 9, 2018
o 5

As the sun rises over Kibale National Park in Uganda, red berries and orange
figs hang in the rain forest’s canopy. They’re waiting for monkeys, apes or birds
to scan the foliage, eat the ripe fruit and either spit or defecate seeds far from
their sources, spreading their next generation to a new location.

Nearly 2,000 miles away, in the similarly mountainous rain forests of

Madagascar’s Ranomafana National Park, yellow berries or fragrant, green figs
await lemurs, the frugivores of this jungle. They’ll search the forest all night for
their feast, later scattering the seeds.

Over millions of years of natural selection, these plants have developed ways to
communicate with animals through their fruits, new research suggests, saying
something like “choose me.” With traits evolved to match each animal’s
sensory capacities or physical abilities, fruits can signal dinner time in the
jungle, and further their plant’s survival as a species.
“When I first learned that plants, in a way, behaved — that they were actually
communicating information to animals — my mind exploded,” said Kim
Valenta, an evolutionary ecologist at Duke University and co-author of a study
published recently in Biology Letters investigating the relationship between
fruit color and animal vision.
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Dr. Valenta and her colleague Omer Nevo, an evolutionary ecologist at the
University of Ulm in Germany who published another paper about scent last
week in Science Advances, are working to understand how plants have adapted
to appeal to animals that spread their seeds. What they are revealing is that
plants deserve more credit — and that the intricate relationships between plants
and animals may be critical for understanding and preserving their shared
habitats.

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For more than a century, biologists have wondered why fruits from closely-
related plants have such different appearances, and how animals know which
ones to eat.

The prevailing hypothesis has been that animals could have influenced fruit
traits — like shape, location on a tree, presentation on a branch or odor and
color — through natural selection. The easier it is for fruit-eaters to identify ripe
fruits, the better the chance for both to survive. The animal eats, and the parent
plant reproduces — by using the animals as gardeners — without lifting a root.

In a similar way, many flowers tailor their petal shape, color, texture or nectar’s
scent or flavor to attract often a single pollinating species. Scientists accept that
these flower traits could result from coevolution, because the relationships are
so specific.

But they’ve had questions about plants reproducing through seed dispersal.
How can you pin a fruit’s particular traits to an animal when many different
animals, with their own evolutionary adaptations, interact with the same fruits?
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Though traits like shape are easier to study, without proper tools to measure
color and odor, much research has relied on human perceptions and may have
overlooked how other animals may experience the world.

Image
A chimpanzee feeding on figs in the Budongo Forest, Uganda.CreditLiran
Samuni

For the researchers, these parks in Uganda and Madagascar offered the perfect
natural experiment. With similar landscapes and related plants bearing different-
looking fruits that feed animals with very different sensory abilities, the
researchers could reveal how animal senses may have influenced the contrasting
colors of ripe fruits against foliage.

The monkeys and apes in Uganda have tricolor vision like humans, and the
birds have even better vision. But most lemurs in Madagascar can only see the
blue-yellow spectrum — they’re red-green colorblind, and rely more on their
strong senses of smell for many behaviors.

So the researchers collected ripe and unripe fruits and foliage and analyzed their
colors with a spectrometer. With a model based on the visual capacities of the
seed-dispersing animals, they also determined who was most likely to detect
different fruit colors contrasting against an assortment of backgrounds.

They found the colors of each fruit were optimized against their natural
backdrops to meet the demands of the visual systems of their primary seed
dispersers. In Uganda, fruits contrasting with foliage in colors on the red-green
spectrum — say that red berry in a green cluster — popped for birds and
monkeys whose eyes can see them.
But in Madagascar, fruit with blue-yellow contrasts — like those yellow berries
— could be best detected by red-green colorblind lemurs (and some birds, too).
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The researchers also know that lemurs dedicate large areas of the brain to
olfaction, helping them communicate with one another and pick mates — often
in the dark. To these excellent smellers, a fragrant brown fig might also stand
out.

In Dr. Nevo’s scent study, his team collected hundreds of ripe and unripe fruits
from Ranomafana — about a third dispersed solely by visually challenged
lemurs and the rest by other lemurs and the park’s few visually gifted birds. He
suspected the lemur-eaten fruits would have a greater difference in odor after
they ripened than the bird-eaten fruits.

To find out, he extracted their odors using the “semi-static headspace

technique.” Sealed in oven bags, chemical fruit odors built up and were then
pumped out, trapped and analyzed.

They confirmed that fruits dispersed solely by lemurs produced more chemicals
and a greater assortment of compounds upon ripening. And in the wild, lemurs
spent more time sniffing these same fruits with big differences in ripe versus
unripe odors. To the researchers, this suggested the differences could signal,
“I’m here. Eat me,” to creatures otherwise possibly unable to see them.
Image

A red-bellied lumur with figs in Ranomafana National Park in Madagascar. In

the experiment, the fruits eaten by lemurs were more sniffable. CreditConnie
Bransilver/Science Source

These results may only be extreme, localized cases supporting the hypothesis
that plants and seed-dispersers evolve together. But the researchers see
additional clues in a relationship between forest elephants in the Uganda park
and Balanites wilsoniana, a tree that might not be able to survive without them.
When ripe, Dr. Valenta said she could detect the “fermented gym sock” odor of
the tree’s large fruits for miles. Elephants — with huge noses and more
olfactory receptor genes than any other known animal on Earth — gobble up the
fallen fruits (they may make them feel tipsy too).

Only elephants can swallow the fruits and defecate the equally large seeds
whole. And this plant won’t reproduce unless it passes through an elephant’s
gut, Dr. Valenta said. This type of mutual dependence is seen in well-
established flower-pollinator relationships, but it’s rare to find in fruit-seed-
disperser relationships. Further study may offer additional evidence that animal
senses influence fruit traits.

The traveler’s palm in Madagascar highlights another plant advertisement

strategy targeted at animals.

In other parts of the world, related birds of paradise plants produce red or
yellow coated seeds easily detectable to birds. But in Madagascar, where
traveler’s palm is native, the seeds are brilliant blue and particularly detectable
to aye-ayes, a kind of rat-cat-bat-looking lemur with an enhanced capacity to
detect ultraviolet light, according to Dr. Valenta.

The seeds of many plants — the traveler’s palm likely included — also contain
a laxative, urging whatever eats them to hastily expel them, undigested, “with a
nice pile of runny fertilizer,” said Jonathan Drori, author of “Around the World
in 80 Trees.”

Aye-ayes and other lemurs are also pollinators, using their strength to open the
palm’s sturdy nectar packages, ensuring the plant can produce seeds in the first
place.

“If something happened to those lemurs, those trees, at least in the wild, would
become extinct,” Mr. Drori said.

Interactions like these remind us that plants are active members of a

complicated and fragile ecosystem — not just landscape.

“We’re only just beginning to understand how much plants and animals mean
to one another,” Dr. Valenta said, “which to me is just a signal that it’s more
important to conserve the entire thing intact.”
ON MEDICINE

For Doctors, Delving Deeper as a Way to

Avoid Burnout

Image

The anatomy laboratory was always freezing. This was our first course as
medical students, and we had split ourselves into groups — four students to
every cluster. Each of us carried a copy of “Netter’s Anatomy”; by the end of
three months in the lab, the volume would become chemically yellowed by
formaldehyde, and to leaf through the tawny, crackling pages would be to feel
your fingers becoming slowly embalmed. Our group had three men — me, S.
and B. — and a woman, G. We “shared” a 60-something female cadaver whose
name we knew by only her initials: M.C. She had died, we were told, of
metastatic breast cancer. Eventually, as we dissected her body, we would find
misshapen deposits of that cancer in her brain, liver and bones.

We met twice a week in the chilly anatomy lab and had lectures, twice a week,
in an auditorium downstairs (each of us was also given a real human skull, in a
lacquered mahogany box, to take home to study. “A Gift of Dr. Goldberger,
M.D.,” mine said, although I didn’t know whether he had merely purchased the
box or donated his cranium). There’s the old, apocryphal story about the law-
school professor who announces: “Look to your left and look to your right. One
of you is going to flunk out of this school.” But in medicine, we would soon
learn, the danger wasn’t flunking out of school. It was a phenomenon called
burnout — being propelled to leave the profession after years, or even decades,
of training and practice. “Look to your left and look to your right,” the anatomy
instructor might have said one morning. “One of you is going to flunk out of
your medical life.”

As the weeks drew on in that first year, we began to hear about residents,
fellows and even senior doctors who had packed their scalpels and stethoscopes
and left medicine. It was the late 1990s, and medical practice was just beginning
to be assaulted by a thousand surgical cuts. Hospitals were changing to
electronic medical records, and — although E.M.R. had been sold to us as a
means to ease work flow and to ensure patient safety (and yes, it did achieve
these) — a doctor’s day felt more robotic and dehumanized: The residents in the
wards seemed to spend the bulk of their time documenting notes, checking off
codes and pressing buttons to generate automated bills. One night, as I recall, I
overheard a young resident breaking down in tears, her face silhouetted against
the sharp light of the terminal as she typed manically. “I have spent two nights
in the hospital and I haven’t even touched a patient. This was not what I came
here to do.”

In the midst of all this tumult, various permutations of our small anatomy group
kept meeting, once every so often, for a quickly snatched coffee in the hospital
cafeteria. We talked about how overworked we felt, about our growing
discontent with medicine, about our detachment from our patients and about our
fraying relationships with other doctors. By then, our paths had drifted apart: B.
had skipped a year ahead and was soon entering a fellowship in hematology and
oncology; S. had gone off to a lab to finish his Ph.D. in the neurosciences; G.
was training to be a psychiatrist. But the three months that had stitched us
together with common purpose — dissecting bodies by day and our souls by
night — had somehow fastened us together and given us a sense of direction.
We had been annealed, like a metal rod that had been broken, melted and fixed.
We would never burn out, we reassured one another (albeit tacitly) during those
meetings. We’d see one another again in 50 years, on the other bank of our
professional lives.
Image
CreditIllustration by Najeebah Al-Ghadban

In 1981, the psychologist Christina Maslach, working with several colleagues,

set out to create a test to measure occupational burnout. Eventually termed the
Maslach Inventory, the scale assessed the risk of burnout by testing subjects
along three basic dimensions: emotional exhaustion, depersonalization and
personal accomplishment. The first set of questions, nine in total, measured the
feeling of being chronically overextended or emotionally fatigued in the
workplace. The second, with five items, tried to capture the feeling of becoming
detached or disconnected from the recipient of your services: toddlers in the
case of kindergarten teachers, or patients in the case of doctors (“I haven’t
even touched a patient,” as the resident put it). The final dimension that
Maslach identified, through eight questions, was a loss of personal
accomplishment, a feeling that nothing was being achieved.

Perhaps Maslach was inspired by Viktor Frankl’s book “Man’s Search for
Meaning.” An Austrian neurologist and psychologist, Frankl had been sent to
the Auschwitz concentration camp and then held at Kaufering, a camp affiliated
with Dachau. He became preoccupied with the experience of survivorship:
What allows some humans to acquire resilience in the face of the most brutal
and dehumanizing experiences? Frankl traced the roots of resilience not to
success or power but to a sense of purpose and the acquisition of meaning. Later
writers, including Daniel Pink, expanded Frankl’s concept of meaning along
three dimensions: purpose, mastery and autonomy. We acquire resilience when
we find purpose in our work. We seek mastery — expertise, skills, commitment
and recognition — in our domains. And we need autonomy — independence —
in what we do.

What happened to our anatomy group? B. finished his residency swiftly and
dove headlong into translational research (“translating” insights from basic
sciences into human therapeutics). He now ranks among the world’s authorities
on a group of strange, recently defined diseases in which a single cell can take
over the whole blood system, hovering on the verge of cancer but never quite
tipping into frank malignancy. S. is largely a laboratory-scientist-cum-doctor
who tries to understand how tumors become metastatic. G., whom I am least in
touch with, is a psychiatrist who specializes in a particular area of children’s
and adult’s anxiety disorders. My own path meandered and trifurcated: I run a
laboratory with a focus on leukemias and stem cells; I write books; I run trials
and see patients, but in a capacity that doesn’t involve typing endless notes into
computers. Other doctors, who didn’t have research-oriented practices,
enhanced their professional lives by concentrating on specific realms of interest.
A family doctor I know carved out a niche in his clinic to focus on middle-aged
H.I.V.-infected patients. All of us escaped burnout, but narrowly — only,
perhaps, by finding personal, often deeply specialized purpose in our work.

Others were not as fortunate. By the end of internship and residency, a slow
trickle of my classmates began to leave medicine (some joined tech firms in
Silicon Valley; some became entrepreneurs). My closest friend from those years
joined a neuroscience lab but then left to become a full-time parent. By 2018,
there was a barrage of discontent. In one study, 42 percent of doctors reported
feeling burned out. The worst affected were obstetricians, internists and
intensivists — doctors in subspecialties that require work in emergency-oriented
conditions, and those who confront frequent lawsuits, and those who require
constant documentation, surveillance and billing. The least affected were plastic
surgeons and ophthalmologists — doctors who inhabit procedure- or skill-
oriented domains. The most common reasons listed for burning out were the
overwhelming strains of bureaucracy and paperwork, the vast quantity of time
spent at work and a lack of respect from administrators and employers. Lack of
adequate compensation was fifth on the list. Among doctors, too, it seemed,
resilience and survivorship tracked along the same essential dimensions:
meaning, mastery and autonomy.
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The consequences of burning out — a phenomenon that rises linearly as a
doctor matures, until it finally dies down at about 60 — can be hard to measure.
But as the internist and writer Abraham Verghese wrote recently in this
magazine: “The total cost of recruiting a physician can be nearly $90,000, but
the lost revenue per physician who leaves is between $500,000 and $1 million,
even more in high-paying specialties. Turnover begets more turnover because
those left behind feel more stress. Physicians who are burned out make medical
errors, and burnout can be infectious, spreading to other members of the team.”

Some solutions to fixing burnout are therefore pragmatic. They involve

lessening burdens: removing paperwork that does not positively affect patient
care, lightening bureaucracies and dissolving the form-filling, diagnosis-coding,
button-pushing culture of modern medicine. But the solutions suggested by our
anatomy group — an informal, minuscule, far-from-scientific survey —
involve more work. We survived, I think, by deepening our commitments to
research. We tried to increase our mastery within peculiar medical niches. And
powerful, autonomous interests kept us going. The mysteries of metastasis, the
intractability of anxiety disorders and strange new diseases of blood cells kept
our brains and souls alive when the hospital was asking us to punch numbers
into terminals. We didn’t burn out, perhaps, by burning a little more.