Gambling in the forest canopy

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Spring in England means every day is longer than the one that precedes it by more than a few minutes. With the lengthening of the days comes the re-emergence of the forest. Earlier this week I went out with our research group to the canopy walkway at Wytham Woods.

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It is a short climb up several ladders to reach the top of the forest.

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The world changes on the journey up to the top. Leaves that look like small green dots from the ground begin to take their proper form, and branches that seemed impossibly far away come within an arm’s reach. The perspective changes from upward to sideways, and one gets a sense of how trees might see themselves and each other. As neighbors in a crowded environment, fighting amidst the sway of the wind and the bright light of the sun.

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Looking out at all these trees, it becomes clear that not every tree is responding to the longer days in the same way. Each individual is following its own particular strategy, taking its own counsel on how best to respond to the environment.

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This beech tree (Fagus sylvatica (Fagaceae)) has elongated its buds, but has no leaves deployed yet.

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in contrast, this sycamore (an unfortunate British common name for Acer psuedoplatanus (Sapindaceae) – the same name elsewhere refers to Platanus spp. (Platanaceae)) has leafed out several days earlier, and has flowers deployed too.

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The congeneric species field maple (Acer campestre) is still in bud, and has no leaves or flowers deployed at all. These buds have a beautiful waxy-red color that may assist in protected buds from ultraviolet light damage.

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This English oak (Quercus robur (Fagaceae)) tree has begun to leaf out, but there seems to be wide variation among individual trees.

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For example, this other English oak tree still has only buds.

Hyacinthoides non-scripta and Primula vulgaris

Back on the ground, the understorey is also still beginning to develop. Some species look to be near their flowering peak, as for this cream-colored primrose (Primula vulgaris (Primulaceae). Others, like this purple-colored bluebell (Hyacinthoides non-scripta (Asparagaceae)) are just beginning to flower.

Why is there such divergence in the spring strategies of these different plants? Proximately, each species is likely responding to or receiving different cues. Plants have marvelous sensory abilities. Spring leaf-out and flowering is thought to be triggered by a combination of day length (via light color detection) and temperature, with the thresholds for each varying among species. Forests also support a range of different temperature and light microenvironments. The oak tree with leaves may be experiencing very different conditions than the oak tree with buds. Ultimately, however, each species has evolved to follow a different set of rules for beginning spring growth. Grow too early and delicate leaves may freeze; grow too late and those leaves may not gain as much carbon as others deployed sooner. The physiology of each species means there are different tradeoffs each species must consider. These rules work well enough in the evolutionary and statistical average for each species to successfully grow and reproduce. What happens in any given year is a different question.

Looking in the canopy, I saw these trees making gambles. Each of these individuals has chosen to either begin or delay its investment in new leaves and flowers. Some days it is sunny; some days it snows. It is too early to know whether each developmental program will fare well or badly this year. But the air is full of hope for growth and new life.

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Melt out

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Early spring is when the elevation contrasts of Britain’s mountains are clearest. These weeks I have been wandering through England and in Wales, climbing where possible, seeing what could be found among the valleys and hilltops.

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The transition between winter and spring means that the valleys are warm, and the hilltops are still cold, so the zonation between snow-free and snow-covered areas is sharp. Mud and fields transition to occasional bunchgrass tussocks covered by snow, and then areas wholly blanketed under.

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These quiet landscapes are beautiful reminders of colder and longer winters in other parts of the world. But unlike these other regions, these hills are largely bereft of animals, who can easily walk downslope to more suitable conditions. I saw no tracks in the snow on any of my explorations.

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The snow is going. The winter has been a warm one, and the ice is melting.

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So the streams begin to fill, clearing the hills of snow and bringing life to the valleys again.

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A few species have begun their spring blooms lower down, bringing some color back to the land.

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This willow (Salix sp.) has male flowers with stamens covered in bright yellow pollen.

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And this witch-hazel (Hammamelis sp.) has beautiful dark-purple flowers.

Soon both these species will flush their leaves and begin to grow in earnest, relying in part on the snowmelt water coming off the hills. Soon the high places will lose their white cover, and the green will return. Soon the balance will tip, and the contrast between high and low will fade away.

Soon.

New paper: learning to see what is missing

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The red flowers of the invasive African tulip tree (Spathodea campanulata; Bignoniaceae) stand out in a Puerto Rican rain forest. This species may occupy a mathematical hole, having an ecological strategy unoccupied by other species in the community. Recent mathematical advances now allow detection of holes and better understandings of species invasions and extinctions.

Imagine an island populated by small and large animals. A reasonable assumption would be that the island might also have medium-sized species—but what if none are found? These empty spaces, or ‘holes,’ may represent missing components of ecological communities. Identifying these holes may help researchers predict the outcomes of invasions, extinctions, and long-term evolution. What we don’t see may matter as much as what we do. My new paper in The American Naturalist (link, PDF) now provides a new way to answer the previously unanswerable question—does a community have holes, or not?

The trouble is that holes are difficult to detect. Imagine a volleyball. This three-dimensional shape has an empty space inside of it, but from a two-dimensional photograph you would never be able to tell that it isn’t solid. Ecological strategies work the same way. Along any individual strategy axis (like body size, or temperature tolerance), species may be able to take on small, medium, and large values—but when considering all axes together, some combinations may never occur, just like the hidden interior of the volleyball. Yet these holes may be exactly where a new species could invade a community, or where another species may have recently gone extinct.

Computers have not been able to solve this problem before now. As the number of dimensions in the ecological strategy space increases, the number of possible ecological strategies grows exponentially. That means there are too many places to find a hole for a computer to easily find. But there is now a new set of free software tools that will enable researchers to efficiently discover such holes (CRAN link to hypervolume package). These holes may represent forbidden ecological strategies or available but unrealized opportunities that have never yet been identified. We don’t know how common holes are in real ecological communities, but we won’t know until we look. Now we can.

(This may also be the first paper I have ever published that includes a peace symbol!)
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Simple winter scenes

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Winter in the United Kingdom is quiet. Organisms retreat underground or migrate to less harsh climates. Only simple winter scenes remain, painted in broad figures with a restricted palette of colors. The complexity of summer is temporarily washed away.

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Fields are seas of black soil, prepared for spring planting.

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Coastal landscapes are brown, dominated by the decomposing fronds of the bracken fern, Pteridium aquilinum.

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Harvested fields are golden, covered by the stems and chaff of last year’s growth.

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Pastures are under frost with only few species of grass still green at the surface.

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These simple scenes do not endure. As the earth moves along its orbit, the skies brighten, and the air warms. The frost melts, and the ice retreats.

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Little by little, the memories of the previous year return. And a few species begin to flower, ushering in the spring.

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The gorse (Ulex europaeus) puts out a few tentative flowers, transforming coastal landscapes from uniform dark grays to mosaics of yellow and green.

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And the first spring Crocus blooms begin to appear. I am glad for the return of a little life to these landscapes, and for the lengthening of the days.

New paper published: a tour of the Hawaiian silverswords

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I think every biologist has a favorite kind of organism. For some people it is a charismatic animal, like an elephant, or a whale. For me it is silverswords. I first learned about these plants in my first year of graduate school. Someone was giving a lecture on adaptive radiations, and showed photographs of a strange-looking plant on a Hawaiian volcano. It had a silvery-gray rosette with long straight leaves, and was growing out of the bare lava (here, Argyroxiphium sandwicense ssp. macrocephalum).

Then he showed another photograph of a different species, this one more shrub-like and growing in a bog, but with something of the same spirit in it (Argyroxiphium kauense). I learned that these two species were part of a group of more than thirty, and were all descended from a single ancestor that colonized the Hawaiian islands a few million years ago. From an unremarkable California tarweed came the entire Hawaiian silversword alliance – the genera Argyroxiphium, Dubautia, and Wilkesia (Asteraceae). The man giving the lecture was Rob Robichaux, a silversword expert. That very day I decided I was going to see them myself, and study them.

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That was 2009. I got funding from National Geographic’s Young Explorers program in 2010 with the help of my doctoral supervisor Brian Enquist, and went to Hawaii in 2011 for fieldwork under the guidance of Rob Robichaux (below) and Bruce Baldwin (two below), with extra help from Emma Wollman.

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The silversword alliance is commonly thought of as one of the most spectacular and diverse adaptive radiations anywhere on the planet, but direct measurements of functional variation among species were somewhat limited. I was intrigued by the apparent diversity of their leaves’ venation networks, as passingly described by Sherwin Carlquist in 1959. I focused the project on understanding how functionally diverse this set of thirty-odd species really was, given that they occupy all the major habitats and islands of the Hawaiian archipelago.

Five years later, the work is all done and the paper is finally out. You can read it, “Variation and macroevolution in leaf functional traits in the Hawaiian silversword alliance (Asteraceae)”, in the Journal of Ecology (link, PDF).

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The short message from the paper is that the clade really is a world-class example of adaptive radiation. The variation in traits among the clade is closely matched to global ranges of trait variation across all species – and this variation seems to evolve very quickly with few evolutionary constraints. These findings provide a quantitative perspective on a charismatic group of plants, and hopefully support arguments for conservation of this endemic and often threatened flora.

It has been a dream to work on this group of plants alongside some of the botanists who love them best. A few species in the clade are now extinct, and several others are either threatened or endangered – for example, this Argyroxiphium sandwicense ssp. sandwicense individual high on a cliff face, protected from non-native sheep browsing – one of fewer than 40 individuals known to exist when Rob became involved with the ongoing state conservation efforts.

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Or this Dubautia latifolia individual that I was only able to sample from a herbarium collection – no more than a few dozen individuals are known to be alive in the wild.

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Or this Wilkesia hobdyi, in cultivation at the National Tropical Botanical Garden on Kaua`i.

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It was humbling getting to work with such rare species, touching individuals of something shaped by millions of years of evolution and now so close to being gone. I had never held an USFWS endangered species recovery permit before this project, and felt very much the obligation to take good care of the plants I was studying, but also the challenges faced in conserving and restoring populations of these native species on an archipelago now run over by non-native species.

Yet among these challenges, the beauty of the habitats and forms of these species remains incredible. Here are a few examples of other species in the clade:

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Dubautia platyphylla, growing on the dry slopes of Haleakalā volcano.

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Dubautia menziesii, on cinder cones at the summit of Haleakalā.

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Dubautia reticulata, a tall tree-like species growing at The Nature Conservancy’s Waikamoi Preserve.

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Wilkesia gymnoxiphium, a spindly rosette growing near Waimea Canyon.

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Dubautia linearis, a tall shrub in the high plateau between Mauna Loa, Mauna Kea and Hualālai.

I’m not sure what resonates with me so deeply about these plants. Maybe it is the tenacity and hope their continued existence represents. Maybe it is how their underlying form becomes multiplied and reflected on different island habitats. Maybe it is the feeling of touching a soft and silvery leaf. But it is a deep sort of affinity that persists across thousands of miles of ocean, and I am sure our paths will cross again soon.

The pleasures of slow botanizing

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Hiking and botanizing are distinct pleasures. Hiking is the joy of pushing one’s body, of covering long distances, of discovering new landscapes. Botanizing is the opposite. It is the joy of moving slowly, of looking closely, of reading the story of a place, and of relishing the discovery of something beautiful or unexpected. On a recent trip down to Sonora, in northern Mexico, I took the time to slowly and carefully explore a coastal landscape, and was amply rewarded by the stories I found hidden in the landscape.

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Chollas are one of the principal hazards of desert walking, especially at high speed. On a slower meander, they are easy enough to avoid, but beautiful in their improbable forms and sharp armor. Every once in a while a bird finds a way to construct a nest in their branches, making for a well-hidden and well-defended home. Here you can see one of these nests in a hanging chain cholla, Cylindropuntia fulgida (Cactaceae).

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Other plants also have spines, though not as prominent or painful as those of a cholla. On this species the long spines and leaves branch in opposite pairs, giving some clue to its identity. I was flummoxed in the field, despite having a flora, and decided to break open one of the fruits to find out what it might be.

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I was dismayed to find a black sludge inside every fruit, hiding a profusion of small flat seeds. On a whim I tasted the sludge and found it to be one of the least pleasant flavors I’ve yet to encounter. Some help from my friend and better botanist Brad Boyle revealed this to be Randia thurberi (Rubiaceae), the papache. According to some reports the fruit is consumed locally and has a sweet flavor – maybe the ones I found were rotting or molded. A mystery I am not keen to soon resolve.

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And my best discovery, hanging low on the branch of a Jatropha (Euphorbiaceae) shrub – an enormous cocoon of the saturniid moth, Rothschildia cincta. I had seen these used before as ankle rattles in ceremonial dances by the Yaqui people, but never knew where they were from. They are marvelously light, smooth, and strong. I only found two in three days of looking.

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For me, hiking and botanizing rarely go together. The rhythms are too different, and I like covering ground, so I tend to hike more than to botanize. But the true pleasures of discovering a landscape only come when it is explored with open mind and eyes.

Why is it so hard to detect species interactions?

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The western coast of Sonora, México is populated by a fascinating mixture of desert and dry forest species. Here the organ-pipe cactus (Stenocereus thurberi) rises over a landscape dominated by Bursera, Ruellia, Jatropha, and a range of other common shrubs. Do any of these species care about each other? Do they co-occur entirely by chance, or do they actively interact? Presumably they compete for nutrients and water; they may also share pollinators, or require the same seed dispersers, or mutually suffer when one inadvertently attracts herbivores. But does any of this matter when we simply want to predict the distribution of these species?

To answer that question, consider these two contrasting examples from the coast of Sonora.

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The first example is from a canyon bottom. A palm (Washingtonia robusta (Arecaceae)) is growing adjacent to a fig tree (Ficus insipida (Moraceae)). But their co-occurrence is probably not due to any direct interaction. They are both here because they share similarly high water requirements. They would both be outcompeted in drier environments or be physiologically unable to survive and reproduce in the open desert. We can safely call this the absence of a direct interaction.

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The second example is from a seaside promontory. This is actually not one plant, but two – a Bursera microphylla (Burseraceae) tree, with a hemiparasitic Psittacanthus sonorae (Loranthaceae) rooted onto its branches, happily flowering using stolen water and carbon. In this case the Bursera suffers from the Psittacanthus, and the Psittacanthus cannot live without the Bursera. This is a clear case of a direct interaction.

One of the major goals of ecology is to accurately predict how species will adapt, move or die, as the Earth’s climate begins to change. If species do not interact, the problem is relatively easy; each species can be modeled as independent from all others. But if species do interact, then the problem becomes difficult much more quickly. In these two examples, we know enough about the natural history and physiology of the organisms to determine whether interactions are occurring. But this doesn’t work when the goal is to predict the distribution of all the species on Earth. The problem is that the number of possible pairwise associations between n species is equal to n(n-1)/2. For two species, there is only 1 association to understand. For a thousand species, there are 499,500 possible pairwise associations that need to be understood. These associations provide a lower bound on the number of possible interactions. Too many to ever understand through natural history and expert knowledge.

Back in 2012, my friend Naia Morueta-Holme and I began developing some new statistical approaches to resolve this well-known but unsolved problem. Our idea was that interactions could be determined by subtracting away other confounding factors like shared habitat requirements. We proposed to first build models of species’ broad-scale geographic distributions based on climatic tolerances and predict how likely it was for species to co-occur. We then proposed to compare these co-occurrence scores to how often species did co-occur in small-scale communities. If species were found more often or less often than under the regional climatic expectation, then they were positively or negatively associated with each other. We then further subtracted away any indirect associations between other species. This final association could then hopefully be interpreted as an interaction. We also argued that species associations may exist between pairs of species, but are much more useful in a network context, just as individual friendships are less interesting that an entire social network. This let us identify species that (for example) were hubs in communities, actively attracting or repelling other species.

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Three years later, the framework for doing all this is now published as a shared first-author piece in the journal Ecography as Morueta-Holme, N., Blonder, B., et al., A network approach for inferring species associations from co-occurrence data. I also wrote a free R package, netassoc, that implements the framework.

We used a large dataset of New World plant distributions from the BIEN initiative to explore the framework’s inferences for the trees of the eastern United States. We found that interactions between species are surprisingly rare, and are positive when found. A few species seem to act as key aggregators, like the balsam-fir, Abies balsamea (Pinaceae).
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And you can see this species does happily co-occur with white cedar (Thuja occidentalis (Cupressaceae)) in this Maine forest!

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The framework makes these predictions without needing to know the natural history of every possible pairwise interaction between species. We hope that the approach will provide a useful tool for predicting the future distributions of species under climate change.

It doesn’t work perfectly – the error rates in simulations are higher than we’d like, and small changes in inputs can lead to relatively high uncertainty in predictions. It took three years of simulations and arguments and failures to get this far. At times we thought about giving up and abandoning the whole project. But I’m glad we stuck with it. I think that the ‘easy’ co-occurrence data that the framework uses is inherently very limited. We throw a lot of mathematics at the data, and push the limits as far as they can go. It’s a start.

(The desert photos were taken on a New Year’s trip with two other botanists. As the ecologist Rob Colwell has apocryphally but accurately said, “One botanist, half a walk. Two botanists…quarter of a walk. Three botanists….no walk at all”.)

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