Importance of Natural Resources

Lemurs: Endangered Gardeners of Madagascar’s Rainforests


It’s really a pleasure to be
introducing Onja this evening as tonight’s HMSC speaker. I think it’s fair to
say that Onja works on one of the most fascinating
topics in ecology, which is plant and animal interactions. And fortunately
for us, she’s also chosen one of the most
charismatic group of organisms on the planet, the
lemurs of Madagascar. And her research
really seeks to sort of elucidate important
interactions between seed disperses in plants, which
play key roles in the assembly and maintenance of healthy
and hyper-diverse forests. I think it’s fair
to say that seldom do we see research
that equally spans two kingdoms in the tree of life
to understand and untangle the complicated ways in
which species interact. Simply put, the biology
of species interactions is really, really hard work. Now in practice,
what this means is that Onja has spent countless
hours, months in the field, leading a team of people under
very unfavorable conditions, following lemurs around forests
and investigating not only what they eat but where they poop. And poop will be a major
theme of the talk tonight. But she assures me that she
will not say the word poop once. So I will say it three times. So research has revealed
surprising findings and suggests these interactions
can be very fragile. And along these lines, in the
spirit of the Hrdy Fellowship, I’ve never really
met a biologist more committed to translating
her research into conservation practices. Using lemurs as a case study
for thinking about these issues more broadly, Onja has
published several key papers in this area. These include studies on the
use of science for decision making, elucidating the
correlates of extinction risk in non-human primates,
and highlighting the great need for increasing the participation
and prominence of women in the field of
conservation biologists. She also brings these
important elements into the classroom, where
last semester, she taught conservation biology to
undergraduates here at Harvard. And it’s fair to say that these
students found her passion for the topic infectious. In their reviews, among other
things, the students wrote, this course was simply
amazing across the board. I learned so much about
many different aspects of and challenges to the field
of conservation biology. And seeing as I’m pursuing– planning on pursuing
this as a career, this class was not only
fascinating but crucial to enlightening my career. Onja left a deep impression
on these students. Now before leaving
Madagascar, Onja completed her bachelor’s
and master’s degrees from the University
of Antananarivo. Shortly after 2009,
she left her homeland to pursue a PhD in ecology
and evolutionary biology at Rice University in Texas,
which she completed in 2015. During her time at Rice, Onja
won the best thesis award in her department and
the Autry Fellowship awarded by the Graduate
Council for most outstanding achievement and promise. She also has won numerous best
talk and best poster awards at several international
conferences, as well as money from over
a dozen organizations, including National Geographic,
the Leakey Foundation, and the Explorers Club. It’s a pleasure to
have in our community such a rising star in the field
of ecology and conservation and to inspire us all
tonight with her science and message of conservation. Please welcome Onja
Razafindratsima. [APPLAUSE] Good evening, everyone. I am happy to be here
today and to talk about my research on the
roles and impact of lemurs on forestry systems
in Madagascar. But before I go any farther
to talk about my research, I would like to give a little
bit of background about lemurs. Because lemurs are going to
be the main topic of my work. The first thing to
know about lemurs is that lemurs are primates. It’s an order that includes
humans, apes, and monkeys. So the order of
primates can be broken into two suborders–
prosimians and anthropoids. And so lemurs are prosimians,
like lorises and tarsiers. And anthropoids include
monkeys, apes, and humans. There are many features that
distinguish lemurs from monkeys and other primates. But one of the examples is
that lemurs have wet nose. So they rely heavily
on their sense of smell to distinguish what is best to– safe to eat and to distinguish
between individuals within their social groups. Also, like any
other primates, they groom themselves and the other
individuals in their group or in their family. But instead of using their
fingers, they use their teeth. And lemurs– are endemic to
the island of Madagascar. So– sorry about this. It’s a large island
about the size of Texas and off the east
coast of Africa, about 280 miles away
from the mainland Africa. Lemurs have evolved
in Madagascar and only found in natural
habitat in Madagascar. And studies of
lemur biogeography, with evidence for molecular
systematics and fossil record suggested that the
ancestors of lemurs colonized Madagascar 60
to 50 million years ago. And they came by the sea
from the mainland Africa on large raft of vegetations. And since then, they
have diversified greatly and into eight different
families, and each one of them composed of several
lemur species. Some of them are
already extinct. And others are still present. And actually, there are
about 17 lemur species that are already extinct. And there are currently
more than 100 species of lemurs alive
recognized today. But this number
keeps increasing. There are more lemur species
being found every year. And lemurs range in
different colors. As you can see here, there are
some brown, black and white, also red lemurs or
orange-looking ones. But they also come
in different sizes. So the smallest
living lemur species, which is also one of
the smallest living primates in the world,
is the mouse lemur. It’s about 30 grams and less
than 10 centimeters long. And the largest living
lemur is the Indri, which is about 20 pounds. So just to give you a
perspective of that size, this is a picture of a mouse
lemur with Shaquille O’Neal. And here is a picture of
an Indri with a scientist in their natural habitat– the lemur’s natural
habitat, not a scientist. And it could be both, actually. But there were some really big,
giant lemurs in Madagascar, like this Archaeoindris that
weighed about 350 pounds. And it’s the largest
known lemur that have evolved in Madagascar. And it’s taller than me. But they’re already extinct. And some of the other
extinct lemur species were also really, really
big, giant lemurs. There are also a
diversity of diet among lemurs, from eating
leaves, fruits, flowers, and insects. Some species even
specialize in eating bamboo. And they are called
bamboo lemurs. Unfortunately, these unique
and diverse creatures are in trouble. Currently, more than
90% of lemur species are highly frightened
at the risk of extinction because of
anthropogenic and natural pressures. So there have been
a lot of efforts into lemur conservation. And they even got
their own festival. There is a week-long of lemur
festival for the past three years, where people
educate others about lemurs and raise awareness
for lemur conservation. And even the students at Harvard
participated in this event last year. They organized this film
screening event and fundraising event for lemur
conservation in Madagascar. But why do lemurs matter? Why do we care so much? Besides them being fluffy and
cute and unique and diverse, why should we care? So one way to consider
this is their potential to have ecological holes,
important ecological holes, and supporting
ecosystem services. So for example, fruit-eating
lemurs, or frugivores, disperse seeds. So they eat the fruits,
swallow the seeds, and then disperse intact seeds
through their defecation. And since trees don’t move
but lemurs do like to move, this is really important for
the survival of the plant. Because it can help them to
colonize new habitat and also reduce the mortality
pressure of their offspring. And by doing so, the lemurs can
provide benefits to the plants and to the forests in general. For example, they can improve
the chance of the seeds to germinate and grow
into adult stage. They can help restore
degraded habitat. They can increase
plant survival. And they can
structure the forest, like engineers of the forest. That’s why I call them the
gardeners of the rainforest. So– sorry– so I’m going to
talk about each one of these. Because I set to investigate
this role of lemurs and their impact on the plants
and the forest ecosystem. So to check this
first point, how do they improve the chance
of seeds to germinate? I did research on
red ruffed lemurs. It’s a large arboreal lemur
with a highly frugivorous diet. And they are
currently considered as a critically
endangered species. It’s one of the
largest frugivores in that area where they live. So a lot of plant species would
rely on them to be dispersed. Red ruffed lemurs defecate
seeds while they’re traveling, resting, or
even feeding in the canopy. And they disperse the seeds of
up to 75% of the plant species that they consume. And they disperse both
small sized and large sized seeds of up to 5.5 centimeters,
these seeds right here. I don’t have a scale. But it’s about five centimeters. So the distribution
of red ruffed lemur is constricted to the
Masoala Peninsula, which is in the northeastern
part of Madagascar. So that’s where I
did my research. So to investigate
that first point, I did germination
experiment where I planted seeds that
were I extracted from the feces of the lemurs and
compared with seeds that were taken manually from fruits. I called them control seeds. And I did this for
about 40 plant species. So to collect the
defecated seeds, we followed three groups
of red ruffed lemurs. Each one of them had
two to six individuals. And we put on at least one
individual per group a radio collar. So that will allow
us to follow them– to find them in the morning and
then follow them the whole day. So we would start at
5:00 in the morning until they go to bed at
6:00 in the evening or 7:00. And so for about seven months,
we would collect their feces. They can defecate up
to 18 times in a day. So you can imagine
how many feces I will collect in one day. And then we extracted the
seeds within these feces. And then also, we collect
the fruits of the same plant species to take out the
seeds to do the experiment. So the number of seeds
in one fecal sample can range from one seed to
up to 120 seeds or even more. But on average, there are
like seven individual seeds in the feces. And I planted these seeds
in an outdoor nursery that looked like this. And I ran the experiment
for about eight months. So as a result, we found that
seeds defecated by lemurs had higher germination rate
than those that were manually extracted from the fruits. As you can see here,
we have the proportion of seeds that have germinated
at the end of the study. And what’s also interesting
is that the emerged seedlings from the defecated seeds had
better growth performance over time and lower
mortality rates from seedling from
the control seeds. So what this result
means is that the passage of seeds in the lemur’s
gut may scarify the seed. And that can enhance
their germination. Because it reduces
the cost, the energy cost associated
with germination. And it also contributes to
accelerated germination. And For some plant species like the
ones that have hard seed coat, it is really important. Because without the help of the
lemur gut to scarify the seed, they might be
unable to germinate. And also, because the seedling
from the defecated seeds were emerging earlier from
the control seedlings, that may explain why there
is higher growth and lower survival. Because the seeds that came
out earlier had more time to develop. So the second point I
was interested to look at is how does lemur help
restoring degraded habitat. So for this second point, I
still walk on the same lemur species and still in
Masoala National Park where red ruffed lemurs are found. So in this park, there are
these two large blocks of forest that are connected by a narrow
strip of forest of about one kilometer long by
2.5 kilometer wide called Ambatoledama Corridor. And before the park
was created in ’97, people were cutting
down trees some parts of the forest in Ambatoledama
to do some subsistence farming where they
planted small scale crops for their subsistence. But after the
creation of the park, it was decided that
these fields should be restored to connect
the large forest, the two large blocks of forest. So in an effort to connect
these large blocks of forests, the park manager planted a
few lemur fruit tree species in this farming field. So in that way, when
the plant grows, they will be able to
attract the lemurs. So the lemurs could disperse
seeds from the forest into this degraded habitat. So by the time I
worked there in 2006, the fields have become some sort
of regenerating forest patches with a discontinuous canopy
of pioneer tree species and an understory of shrubs
of native and non-native plant species. So I examined whether
the red ruffed lemurs will disperse seeds into
these regenerating patches. So to do that, we
observed where lemurs would defecate the seeds. And so this happened during
the lemur observation effort. We would take the
GPS points of where the seed landed in addition to
identifying the seed species. So as a result, we found that
these lemur species actually dispersed the seeds
from the forest into regenerating
forest patches. So about 8% of the collected
feces in the regenerating patches contained seeds. And what’s really interesting is
that the lemurs were attracted by the fruits of
these exotic shrub species that exist in the
regenerating patch of forest. So they will go there
to consume the ripe fruits of these species
while traveling on the ground under an open canopy, which is
quite unusual for this species. Because they’re supposed
to live in the canopy. And by going there,
they dispersed the seeds of the native
trees from the forest into the habitat. And as I said earlier,
they defecate even when they are foraging. So they go there to eat. So they defecate as well. So by bringing the seeds
of the native trees into the regenerating
patches of forest, they provide opportunities
for these native plant species to colonize the areas,
which may affect the structure and the species
composition of these forest patches. So I’m taking you really
far away from Masoala to look at the next point
that I want to talk about– the increase in plant survival. So for this point, I worked
on these three lemur species– red-bellied lemur,
red-fronted brown lemur, and black-and-white
ruffed lemur. Similar to the red
ruffed lemur, they are also large and arboreal and
have highly frugivorous diet. And they share many
plant species for food. But they’re also in danger
and at risk of extinction. So one thing to know about
their foraging behavior is that they tend to
repetitively use the same route within their territories. And they frequently use and
reuse the same certain feeding trees and resting trees. So this is a few examples of
the daily path, so the path that we do during the day. So they will start here
and then go around but then come on the same tree and then
go back on the same tree often. And they are the
primary seed dispersers of several large
seeded plant species in the area where they live. And previous studies
have shown also that the seeds that pass through
the guts of these three lemur species have also germination
success from the seeds that were extracted from plants– from fruits. And like the red ruffed
lemurs, they also disperse seeds while they
they’re traveling, resting, or even feeding. So the distribution
is not as restricted as that of the red ruffed lemur. But I did my research
in the rainforest of Ranomafana National Park,
where all three of them occur and where they are the
largest frugivores. Ranomafana National Park
is in the southeastern part of Madagascar. It’s a beautiful montane
evergreen rainforest, home for more than
350 species of trees. And the tree community
in Ranomafana is mostly dominated
by species with traits that are adapted for seed
dispersal by vertebrates. And most of them are
primarily consumed and dispersed by lemurs. So to investigate how do lemurs
increase plants survival, I ran probability
recruitment models to compare the survival
and recruitment of saplings on the scenarios with and
without lemurs in the forest. So for these models, I
parameterized them using data from observation of
seed dispersal and data from experiment on seed
fate and recruitment. So for the observation
data, we would follow eight groups of each
lemur species for one year. And every time they defecate– this one, they can defecate
up to 25 times in a day. And the majority
of the feces had seeds with sometimes some leaves
or some remains of fruits. We would identify the seed
species for every single feces. And then we identified
the adult neighbor whether it is the same species
or a different species. And we measured the canopy
cover of where the seed landed. So these canopy
covers were later classified as whether it was
a gap if it’s less than 55% covered, medium-shaded
if it’s and 55% to 75%, or shaded for more than 75%. And for the experiment part,
we were conducting experiments on seed fate and
recruitment across these different microhabitats
by planting seeds in each one of
these microhabitats and also under the crowns
of conspecific trees. And so this experiment
was run for three years. And using these results
from observation data and the experiment
data, I ran these models with these really
simple equations. So for each microhabitat,
I had the number of seeds deposited per adult
tree per fruit in season and the number of the
probability of seedlings to survive after three
months and the probability of seedlings to transition
into one-year-old and the probability of transition from
one-year-old to three-year-old. And I ran these models under
two different scenarios, as I said earlier, so dispersal
by each and all three lemur species and then as another
with no seed dispersal. So all the seeds would
fall under parent trees. And I did this research by
focusing on one plant species, Cryptocarya crassifolia. So this a pretty common
plant species in Ranomafana and dispersed by these
three lemur species. And it’s a long-lived canopy
tree species with seeds about the size of an apricot. And it’s– apricot seeds. And it’s fruiting between
March and October. So as a result of
this model, I’m showing here the
probability recruitment per seed for each of
the three lemur species and compared with the
probability recruitment for seeds that are dropped
under the parent trees. So if you look at this,
the probability recruitment of the seeds that are
dispersed by the lemurs, they look pretty similar. But when compared
with the seeds that weren’t dispersed by the lemurs
but were dropped under parent tree, there is about
four times decrease in the probability
of recruitment. And so this advantage of
seed dispersal by lemurs could be due to the fact
that they disperse seeds into suitable microhabitats. So what I mean by a
suitable microhabitat is one where there is a
higher chance for the seeds to survive and to recruit. So in this case of this
particular plant species, seed survival and
seedling recruitment was higher for seeds planted
in more open microhabitat and under heterospecific trees. So as you can see here, this– I’m going to try to use
this– so this graph here shows the survival and
recruitment probability of all the plant species
that are planted on the different microhabitats. And the green dots
with the green line shows the recruitment
and survival of the plants that
were in the gaps. So it’s high
compared to the rest. And then even when I controlled
for whether the seeds were planted under heterospecific
or conspecific tree species, I found that there is
still higher recruitment under heterospecific trees
and lower recruitment under conspecific trees. And this is interesting,
because two of the lemur species were less likely to disperse
seeds near conspecific trees, than you would expect by chance. So this graph here shows
the mean proportion of seed dispersal
events that occurred under conspecific trees
as compared to what would you expect by chance if
seeds were randomly dispersed and if that was dependent
on the density of trees of the same species
in the habitat. And as you can see here, only
the red-fronted brown lemur , Eulemur rufifrons, had a
tendency to disperse seeds under conspecific but not
the other two species. And also, these lemurs were also
more likely to disperse seeds under gaps, like here. So this figure here shows
how likely each lemur species will disperse seeds under
each one of the three different microhabitats. So the positive value
would mean that they prefer to disperse seeds in
that particular microhabitat. And negative values
would mean that they avoid to disburse seeds there. And value zero means there is
no preference or avoidance. So you can clearly see here
with the two Eulemur species that they tend to
disperse seeds under the– in gap but not Varecia
veiegate editorum. And they all disburse seeds
under medium-shaded area. And they all avoid
the shaded areas. So it’s a combination of this
behavior of where they disperse the seeds in addition to
the requirement of the plant species that make them– that contribute to the advantage
that they provide to the plant. And so in addition to
that, this advantage may also be due to the
fact that these lemur species take the seeds away
from the parent plants. So they are releasing
them from high mortality that is usually associated
with being under a parent tree. So this is a well-known
hypothesis in tropical plants, actually. So basically, because
there is a high density of seeds near the
parent tree, there will be a lower probability
of survival for being under the parent tree. Am I losing you? Or you are still there? OK, I want to talk
about the last point. So the last point is that how
do lemurs structure the forest? So we know that plants don’t– most adult trees don’t move. So for them to be able to
build a new plant community, they need to be dispersed. And there’s this spacial
pattern of seed dispersion will form a template from which
plant communities develop. So for example, if seeds
fall under these boxes and survive there, that’s
where the adult trees are going to be. And one of the many ways
that animal frugivores set that template is by
directing seed dispersal toward certain trees
in the landscape, such as certain fruiting trees. Because they are frugivores. And they hang out among
fruiting trees most of the time. That’s where they will
disperse most of the seeds. And this biased
dispersal pattern could be important for
structuring in plant and for plant distribution. Because the spatial
proximities of plants would influence their
interaction and the interaction between the seeds
and the adult trees, such as the identity
of the adult neighbor and its relatedness
to the seed, which may also influence the
seed establishment. So what I mean by
relatedness here is phylogenetic relatedness,
how more closely related the dispersed seed is with
the adult neighborhood. So for example, in a
hypothetical phylogenetic tree, species A here and species
B are more closely related to each other than
species B to species C. Because A and B share
common ancestor. So in a certain way, it’s
like you and your siblings are closely related but
not you and your cousin. You and your sibling
are more closely related from you and your cousin. But here, I’m talking
about seed and trees. So I’m interested to know
whether the dispersed seed is more closely related to the
adult tree where it falls. And this is important. Because if the seeds
land near trees that are more closely related
to them, they may not thrive. Because closely-related species
tend to have similar traits, like their vulnerabilities
to natural enemies like to seed predators
and pathogens. So how do lemurs
structure this association between the dispersed
seed and the adult tree? So to answer that, we
recorded the fruiting status of the adult neighbor
to where the seeds were deposited during the lemur
observation effort that we did. And then we also monitored
the fruiting phenology of more than 3,000 trees in
the forest for two years. And in addition, we also
conducted indirect observation of seed dispersal
using seed traps. That is a wide basket that
looks like this one here. So it is hanging. We hung it in the forest to
collect feces and the seeds that come with the feces. So these traps were hung in
the forest for 16 months. And we monitored
them every two weeks to identify the seed species
in the feces and the fruiting status of the trees that
have their crowns overhanging the traps. So as a result, what we found
was that these lemur species were more likely to disperse
seeds under fruiting where they recently fed. Because as I said
earlier, they also spend a large
proportion of their time around fruiting trees. So they tend to defecate
while foraging also. This graph here shows the mean
percentage of seed dispersal events that fall
near fruiting trees, compared to what you
would expect by chance under a random
distribution of seeds where they will fall
randomly depending on the density of the
trees fruiting in the area. And so as you can
see, there is– so the orange bars are what
we observed and the green are what we would expect by chance. So you can see here
that there is always higher probability that a higher
percentage of dispersal events that occur under fruiting trees. And because of
these behavior, they influence the pattern of
phylogenetic relatedness between the dispersed
seed and the adult tree. So the data I’m showing here is
actually from the seed traps. So in nine out of 16
months of studies, shown by the yellow points,
all the yellow points here, we found that
lemurs direct seeds under distantly-related
species during certain months of the year. And in other months,
they will direct seeds under closely-related
tree species. So what it means is that lemurs
structure the early stage template for plant communities
at the seed dispersion level. And as I said earlier, these
seed-adult associations are really crucial for seed
establishment and survival. And by using these fruiting
trees as seed dispersal foci, where they would direct
the seed dispersal, lemurs bias dispersal under
adult trees that share the same seed dispersers and
fruiting at the same time as the dispersed species. So by doing that, they may
be limiting the frequency and diversity of interaction
that the dispersed seed can have with adult trees. And if this is
common in the forest. And with all these
lemurs species, they will also promote
plant diversity. So to answer my
original question, why should I care
about lemurs, here is a summary of what I found. They improve the chance of
seeds to germinate and grow into adult stage. And they can help
restore degraded habitats by dispersing seeds into the
regenerating patches of forest. And they help increase
plant survival by four-fold. And also, they structure the
template from which plant community patterns develop. And they’re all
doing this for free. [LAUGHTER] So as lemur populations
become functionally extinct across the island, there could
be some drastic consequences in tree communities. For example, there could be
changes in plant diversity. Because there will be decline
in the plant population that are dispersed by lemurs. But there could also be
changes in the composition of the forests. For example, the tree
species with other means of dispersal like bird
disperse or wind disperse might do better and
might become more common. And these changes may
affect the other organisms that also rely on these plants
species for their survival. And so the conclusion is
we should save the lemurs. And I know there
is hope for lemurs. And each one of you can
contribute in many ways. And before I close
this talk, I want to take a minute to thank
the amazing research team that I have had for
the past more than a decade. This research was actually
a work of team effort that involved a lot
of local villagers, a lot of undergraduate students,
of volunteers and collaborators who were highly involved
in data collections. And some of them are shown
in these pictures here. And also, this research
couldn’t happen without the generous logistical
and financial support from many organizations
and institutions. And with that, thank
you for coming today. [APPLAUSE]


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