In a new article available online at the Royal Society Open Science, I tested several predictions of adaptive radiation theory for lemurs of Madagascar. This charismatic group has long been suggested to be the result of adaptive radiation, but my results suggest the long evolutionary history of lemurs may not fit all the predictions.
Adaptive radiation is a key concept in evolutionary biology, with a fantastic diversity of species arising to fill every conceivable niche. Famous examples include Darwin’s finches of the Galapagos, lizards of the Caribbean, and cichlid fishes in Africa. Madagascar, an island nation off the coast of Africa, is a biodiversity hotspot, with thousands of species found nowhere else on earth. The primates – lemurs – have long been suggested to be an example of adaptive radiation, with around 100 species alive today that have unique and diverse niches. The theory of adaptive radiation makes several explicit predictions, which have not yet been tested for lemurs. For example, evolution of morphological adaptations to fill unique niches is an important part of adaptive radiation theory. Do lemurs fit these predictions?
In a new article accepted in the Royal Society Open Science, I tested multiple predictions about the rate that species diversified, and how their body size adapted to different niches of diet and activity pattern. I also tested the possibility that a mass extinction event in the past, 34 million years ago, may have changed the rate of speciation and extinction. While theory predicts that speciation rates should be highest early in the evolution of an adaptive radiation and slow down towards the present, lemur speciation rates were either constant through time, or may have even increased slightly over time. The rate of body size evolution fit predictions better than speciation rates; the major groups of lemurs seem to have differentiated into unique niches with different optimal body sizes. Lemurs that eat leaves and are active during the day have larger body size than day-active fruit eating lemurs. There are three unique groups of small-bodied lemurs that have independently evolved adaptations for eating leaves. Additionally, there are small nocturnal species adapted for eating fruits, nectar, and insects. This diversity of niches and associated body size evolution suggests that lemurs may have evolved via adaptive radiation, despite the contrary results from speciation rates.
While there was no evidence that a mass extinction event disrupted speciation dynamics in the deep past, 17 species of giant lemurs have gone extinct within the last 2,000 years, not long after the arrival of humans around 4,000 years ago. The giant lemurs were unlike most alive today, with one species as large as a silverback gorilla. The loss of these unique species represents a significant change in Madagascar ecology and evolutionary history. This study provided explicit tests of the adaptive radiation theory for lemurs, with mixed results suggesting that body size and niche evolution fit expectations, but speciation rates may tell a different tale.
Lemur phenotypes - or their morphology, ecology, and behavior - are so diverse, they fit the prediction of adaptive radiation. While some species are small, nocturnal omnivores, including the smallest primates, the mouse lemurs, other lemurs are larger, diurnal and eat leaves. Some species are even specialized to eat bamboo with enough cyanide to kill people! The largest living lemur, the 6-10kg (12-20lbs) Indri, is tiny compared to the giant lemurs that went extinct just 2,000 years ago, which were as big as gorillas - up to 150kg, or 300lbs!
Phylogeny of lemurs and other primates, illustrating living and extinct species. Figure from Herrera and Davalos 2016, Syst. Biol. Illustrations courtesy of S. Nash, used with permission.
Strepsirrhine phylogeny illustrating the distribution of body mass (black bars next to tips, scale at the bottom, natural log transformed) and adaptive niches of diet and activity pattern (colored circles next to tips). The evolution of niches was estimated at internal nodes (colored pie charts on nodes representing the proportional probability of each state) and the best estimate at each node was assigned to the descendant lineages (colored branches). This tree was used to test how body mass evolved at different rates in different niches.
My latest paper on lemur conservation priorities just came out in the journal of Biological Conservation. In it, I discuss a new priority scheme for 100 protected areas that have high lemur diversity in terms of threatened species, functional traits of species, their evolutionary history, as well as the quality and threat to their habitat. This multidimensional approach allowed me to rank protected areas based on a diversity of measures.
Biodiversity worldwide is threatened with extinction due to human activities. Primates, the group including monkeys, apes, and people, are vulnerable to habitat loss, hunting, and future climate change. 44% of primate species are considered threatened by the International Union for the Conservation of Nature and Natural Resources (IUCN). The lemurs of Madagascar, found nowhere else, are the most endangered primate group, with 93% threatened due rapid habitat loss, as well as hunting in some areas. There has been a tremendous effort to conserve lemurs and the habitats they thrive in, including the creation of over 100 parks and reserves (protected areas, PAs) to protect montane rainforests, tropical dry forest, and arid spiny forest. Madagascar is an impoverished nation, however, with limited funds to maintain PAs. In 2013, conservation priorities for PAs were set based on the number of species in each PA and how endangered they are in the Lemur Action Plan. In a new study, I propose a new priority ranking for 100 PAs based on their lemur diversity and habitat quality. Assessing diversity is difficult, though – how should we calculate the value of a PA for lemurs? I quantified diversity in terms of 1) the number of species, 2) how endangered those species are, 3) how diverse the functional traits of species are, 4) how much evolutionary history species represent, and 5) how diverse and productive the habitats are. To measure the level of anthropogenic threat to these PAs, I calculated the rates of deforestation using data from Hansen et al. 2013 (data found here).
I found that the priority ranking of PAs differed depending on the measure used, leading me to create a summary metric that captures the importance of each PA on multiple levels of diversity and threat.
Surprisingly, I found that deforestation inside of PAs was high; up to 31% forest loss between the years 2000 and 2014, totaling ~3,000 km2, which is 50 times the size of Manhattan. The highest deforestation occurred in PAs with high species richness and functional trait diversity.
I ranked PAs to suggest the priorities for more intensive future conservation efforts. The top PA is a corridor in the southeast that links the Fandriana National Park to the Marolambo forest south of it, and has only recently been declared. Corridor forests are especially important as a means for individuals to disperse among populations and aid gene flow, as well as a means of repopulation if some populations suffer declines. Based on phylogenetic diversity - the evolutionary distance separating the species in the park - some internationally recognized PAs were found to be priorities, such as one UNESCO world heritage site (Tsingy de Bemaraha). There are also several highly threatened environments with high functional diversity, especially in the arid southwest like Beza Mahafaly. With these new priority rankings, scientists can collaborate to focus their efforts on the most threatened and diverse PAs. Efforts should also be maintained in successful PAs, which have had limited deforestation. These sites have created partnerships with local stakeholders to collectively protected natural habitats, such as Ranomafana and Analamazaotra. The full list of PAs, and their ranks based on each metric can be downloaded here. While there are many impediments to conservation in Madagascar, especially high deforestation for agriculture, there are many success stories which provide a framework for conserving species in the future.
Much remains to be learned about conservation priorities in Madagascar. It is especially important to quantify the importance of these PAs for the people of Madagascar. PAs are important at the national level because of the revenue generated by tourism. They significantly impact the lives of local populations surrounding them, who depend on the land for subsistence, like farming and building materials, as well as for ecosystem services such as clean water. Parks generate revenue for local populations through tourism and research, but often the economic loss of restricted access to land is not offset. Lastly, some forests have spiritual value, because some ethnic groups bury their dead in tombs within forests. Therefore, nature conservation must also determine the value of PAs for people.
Another way this study can be improved is to enumerate these diversity data for multiple taxonomic groups. These data are accumulating with many field projects collecting data on diverse groups such as birds, small mammals, bats, amphibians, reptiles, and plants. Combining these new occurrence records for diverse groups will allow a more multifaceted approach to conservation in Madagascar.
To summarize, this new paper reports conservation priorities based on the sum of lemur diversity, habitat quality, and deforestation. Rapid loss of habitat is threatening important biological systems that also provide crucial services for people. I hope that the results of this study will be well received by the community and can help guide future conservation efforts.
Below are figures illustrating the extant of forest in the year 2000 (green gradient) and the forest loss is in red. I also zoom in on a few key areas where there is especially high deforestation, like in the northeast. The semi-transparent colored blobs are protected areas. Some areas have surprisingly high deforestation.
This is what is really at stake! The cutest creatures on the planet. We cannot let these unique animals and the habitats in which they live disappear.
Cheirogaleus sibreei at Ranomafana National Park is one of the many diverse and critically endangered species found in this top priority protected area. C. sibreei is also found in the corridor forest north of Ranomafana which connects it to Fandriana, another top priority site.
Habitat for Cheirogaleus sibreei in the Fandriana-Ranomafana corridor, north and outside the boundary of Ranomafana National Park. This corridor is technically protected.
Slash-and-burn agriculture in habitat for Cheirogaleus sibreei in the corridor forest north of Ranomafana National Park.
We humans —along with apes, monkeys, and lemurs— are primates, and exploring primate evolution helps us understand where we came from. Indigenous to Madagascar, lemurs form a unique branch of the primate family tree. But there is one important obstacle to understanding where lemurs came from and how they evolved– there are no ancient fossil lemurs. This void makes it difficult to track the stages of evolution often observed in transitional fossil forms. Making matters more confusing, but fascinating, there are remains of lemurs extinct around 2,000 years old. Those lemurs were radically different from the ones alive today. Many of the extinct lemurs were giants, with some weighing as much as gorillas! Placing them in the tree with living species has been difficult because of their unique features. To understand the factors that may place species at risk of extinction, it is important to compare the traits the extinct species had to those of living species. For my Ph.D. research, the first step was to do just that. With my committee member and collaborator, Stony Brook University Professor Dr. Liliana M. Dávalos, I studied the evolutionary history of lemurs in detail with support from the National Science Foundation. The findings are out this week in the journal Systematic Biology. For the first time since the early 1990s, I combined data from living and extinct species with cutting-edge techniques to place all lemurs in a single tree, providing the most complete tree of lemur evolution yet.
Surprisingly, the new phylogeny finds some of the subfossil species were unique branches with no living close relatives. The giant, extinct koala lemur (Megaladapis) had short limbs and long finger and toe bones, which may have allowed it to cling to branches, much as living koalas do. Megaladapis also had an extremely long snout with no upper front teeth, and may have even had long dexterous lips for manipulating food. The koala lemur was thought to be closely related to either of two living groups: the sportive lemurs (Lepilemur), or ‘true’ lemurs, like the ring-tailed lemur (Lemuridae). Because of the unique features with few similarities to living species, placing them in the lemur tree based on skeletal traits has been difficult. Fragments of ancient DNA had suggested a close link between koala and true lemurs. By combining genetic and anatomical data, the new tree finds the koala lemur was a completely extinct, unique branch of the lemur tree.
Other fossil groups are more closely related to living species, but the fossil groups were giant compared to living species. While the largest living lemur is about 22 pounds, the largest and closely related extinct lemurs may have weighed over 300 pounds! Large body size is one important component of extinction risk, and so by understanding the evolution of body size, we can better understand the factors threatening lemurs today. The implications for the future of lemurs are substantial; 95% of living lemurs are threatened with extinction. With all living and extinct lemurs together in the same tree, we can begin to understand how evolution and extinction have worked in the past, and project risks into the future.
Another way the study helps us understand primate evolution is by illuminating how geography has contributed to splitting off species. Madagascar has been an island separate from all other landmasses for at least 90 million years, long before primates first appeared. As in previous analyses of molecular clocks, the new study suggest lemurs first evolved ~50-60 million years ago. This means the ancestor of lemurs likely arrived on Madagascar by dispersal – perhaps washed from Africa to Madagascar floating on vegetation, or with some small stepping-stone islands to help along the way. A surprising new twist arises from the new lemur family tree: could lemurs have dispersed from Madagascar back to Africa? In some analyses, there was evidence a fossil primate found on Africa 34 million years ago (Plesiopithecus) was most closely related to the aye-aye, the first lemur to diverge from other species. If confirmed, this evolutionary pattern means the aye-aye and the ancestor of all other lemurs dispersed from Africa to Madagascar separately, or the ancestor of all lemurs arrived on Madagascar and this unique branch dispersed back to Africa. This finding warrants an intense focus on the similarities between the aye-aye and the African fossil Plesiopithecus to determine whether they are the result of common ancestry, or if this link is an artifact of similar ecological pressures leading to similar traits.
With this new evolutionary tree, we have a much better understanding of the evolutionary dynamics of primates and how evolution shaped the primates of Madagascar over the last 50 – 60 million years. We can now compare the factors associated with the extinction of all subfossil lemurs, and predict how living lemurs may fare in the future. This information is crucial if we hope to prevent further extinctions of these distant human relatives.
Check out the Huffington Post's piece on this article
And Forbes too!
Illustrations copyright S. Nash, used with permission
The first chapter of my dissertation to be published is now out in the Journal of Animal Ecology, detailing a close connection between the diversity of primates and the abundance of their food tree resources. Lemurs are primates endemic to Madagascar – they are indigenous and found nowhere else on earth. They are also highly threatened with extinction; 95% of lemurs are considered at risk of extinction. The primary threats to lemur persistence are habitat loss due to deforestation for agriculture, cattle grazing, logging, and mining, as well as hunting for bush meat. The new study illustrates the tight links between lemur diversity and ecosystem health.
In case this is your first time on my page, my name is James Herrera, and I am a researcher at the American Museum of Natural History. I conducted the study as a Ph.D. student at Stony Brook University. I spent two years trekking across rainforests in southeast Madagascar to count lemur species and determine their abundance in relation to habitat characteristics such as human disturbance, altitude, and tree community composition. I surveyed five different habitats with teams of Malagasy field assistants and graduate students. The study was conducted in Ranomafana National Park and an adjacent forest corridor that connects Ranomafana to the Fandriana Park to the north. Some habitats were low altitude pristine rainforests like green cathedrals of massive, broad canopy trees. Other habitats were high mountain peaks of granite, festooned with forest clinging to rocks. I also surveyed heavily disturbed sites, some of which had been logged or cultivated in the past and subsequently grew back, while others were actively being logged and mined for gold around his camp site. This variety of habitat types allowed me to compare the primate communities in relation to variation in habitat features.
The study revealed the overwhelming effect of food tree abundance on lemur diversity. While some small nocturnal lemurs eat insects, many lemurs are vegetarians, and most specialize on the fruits or leaves of just a few key tree species to obtain most of their diet. Collaborating with Malagasy botanists, I enumerated the food trees in each habitat compared to non-food trees, and found the relative abundance of preferred food trees was most closely tied to lemur diversity. Where food trees were most abundant, the lemur communities were dominated by a few large-bodied species that form large groups, while small species with small group size were rare or absent. When food trees became scarce, those previously dominant large-bodied species became rare or absent and other species increased in abundance. This result illustrates how resource limitation affects the abundance and diversity of lemurs. This finding is especially pertinent for healthy ecosystem functioning. The fruit-eating lemurs are important seed dispersers; when lemurs eat the fruits, they pass the seeds whole which germinate much better than seeds not passed by lemurs. Different lemurs specialize on different trees and disperse the seeds far from the parent trees, like gardeners sowing the future forests. Without these lemurs, the trees may not be able to reproduce as efficiently, and so lemur extinctions could have cascading effects on ecosystems.
Surprisingly, human disturbance did not have a strong effect on lemur diversity, possibly because of the indirect effects on food tree abundance. For example, while some heavily degraded sites had low food tree abundance, so did high altitude pristine forests. The study illustrates that some lemur species may be resilient to habitat disturbance, especially those small-bodied species that have small group sizes and can be sustained with lower resource abundance. The result is important for understanding how entire lemur communities will respond to future habitat loss, which is especially important because of the ongoing degradation of natural habitats. While I surveyed corridor forests that connect two national parks, migrants from far-away cities were cutting forest, damming rivers and panning for gold. The recent surge is especially troubling because it attracts bandits who rob gold miners and threaten the safety of rural villages. Further, many of the miners are immigrants from cities, not the local land owners with rights to the forest resources. Protective action is needed to suppress the burgeoning deforestation, and this corridor is especially important to maintain safe passageways for lemurs to move among parks and maintain healthy stable populations.
This study was funded by the National Science Foundation, Margot Marsh Biodiversity Foundation, Conservation International, Explorer’s Club, Leakey Foundation, Primate Conservation, Inc., Rufford Small Grants Foundation, International Primatological Society, American Society of Primatologists, La Conservatoire pour la Protecion des Primates, and the Turner Fellowship while at Stony Brook University, as well as a Gerstner Scholarship and Postdoctoral Research Fellowship from the Richard Gilder Graduate School, American Museum of Natural History. I also acknowledge the help of over 30 Malagasy research assistants, especially Tongasoa Lydia, a Malagasy Ph.D. student who worked with me during this study.
To kick start some blogging on the latest research that I find interesting and exciting, two recent papers examine speciation and extinction rates in carnivores using extensive data sets on fossil occurrences.
One of the best ways to estimate the past diversification dynamics (speciation and extinction rates) is using the rock record - fossils preserve the timing and location of speciation and extinction events. Other ways that are informative include using the evolutionary tree of living species, because the structure of the tree reflects past speciation patterns. But more on that another day...
Using a sophisticated biological model of speciation and extinction dynamics that includes preservation bias (the rock record is not perfect!), Pires, Silvestro and Quental inferred rates for each carnivore family, including entirely extinct groups, and found strong evidence for rapid and exceptional speciation when carnivores moved from North America to Eurasia, an example of adaptive radiation.
Reconstructing the waxing and waning diversification of carnivores can test hypotheses about the biogeography and environmental causes of speciation and extinction in deep time.
Next, Silvestro and colleagues step it up even further to test the effects of past competition and climate change on the speciation and extinction rates of North American fossil canids: http://www.pnas.org/content/112/28/8684.short
I've got to go over this second paper in more detail (don't you love it when the article is 6 pages but the online supplemental information is 60?). But it seems like a really innovative look at the Red Queen hypothesis - that species evolve as fast as they can to just to stay in one place...to keep pace with a changing environment. Previous research has shown that the failure to keep pace with the changing environment has driven species to extinction: http://www.sciencemag.org/content/341/6143/290.short
One of the projects I'll be working on for my postdoc at the AMNH is this kind of analysis for all primates. I'm still working on the first step - assembling the fossil occurrence data. It takes time and screening the data for the 'perfect' ages is no easy chore. But hopefully this project will move forward quickly.
The Center for Humans and Nature posed the question: what are the connections between culture and conscience? The respondents, especially the featured respondents, gave their thoughts: http://www.humansandnature.org/what-are-the-connections-between-culture-and-conscience#all-responses
Particularly controversial was the response by Jonathan Haidt (NYU), who suggests capitalism is the route to democracy, autonomy, and good environmental conscience: http://www.humansandnature.org/culture-how-capitalism-changes-conscience
What do you think?