Fossil plant defenses and the rise of African savannas

 

Endangered Rothschild Giraffe bending over eating the leaves from a small Acacia tree in Lake Nakuru, Kenya, Africa – notice the thorns!; photo: David Gomez, from Getty Images

 

We are still a long way from understanding the animals* around us, but in many regards, it’s a lot easier to infer the emotions and actions of other mammals than it is to grasp anything about plants.

I know, for example, when my cats want attention, when they’re hungry, and—especially when one of them ambushes my legs with her furry paws—when they want to play.

I can’t say the same for my plants.  I’m not sure I ever think of them in terms of having emotions.  Am I concerned with their growth? Absolutely.  Do I make sure to water and feed them appropriately?  Yes.

But I suspect most of us think of plants in a completely different way than we think of animals.

This particular view of life on our planet was expressed in “Jurassic Park.”  After their initial introduction to the dinosaur park created by John Hammond and his team, the invited scientists gathered for lunch.  Mathematician Ian Malcolm (played by Jeff Goldblum) expressed his doubts and concerns about the park.  This led the others to offer their opinions as well.  Paleobotanist Dr. Sattler (played by Laura Dern) stated:

“Well the question is: how can you know anything about an extinct ecosystem?  And, therefore, how could you ever assume that you can control it?  You have plants in this building that are poisonous. You picked them because they look good, but these are aggressive living things that have no idea what century they’re in, and they’ll defend themselves. Violently, if necessary.”

Ellie Sattler (Laura Dern) - Jurassic Park - Universal Studios

Dr. Ellie Sattler (played by Laura Dern), Jurassic Park, 1993, Universal Studios

That very statement (albeit in a movie) challenges the conventional view of plants on this Earth.  Rather than simple sedentary life forms, it suggests that plants are more complex, engaging in the world around them, just as we know animals do.

And once you start thinking about plants defending themselves—taking an active part in the world around them rather than simply existing and having things done to them—it changes how you look at everything around you.

Scientific research into the realm of extant plant communication, defense and even participation in community is relatively new.  Dispersal of that scientific knowledge to the general public is even newer.

Remarkably—given how much we have yet to learn about existing plants—scientists from South Africa, Canada and the United States published research regarding the possible origin of African savannas, an origin that has roots** in plant defense millions of years ago.

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An example of an African savanna: Mt Kilimanjaro & Mawenzi Peak, clouds, grassland, and Acacia; photo: 1001slide, from Getty Images

 

A significant amount of land in the Miocene belonged to savannas, pushing forests to recede where they once flourished.  Some have attributed this to climate change; others to a change in the amount of carbon dioxide in the atmosphere.

The authors of “Spiny plants, mammal browsers, and the origin of African savannas”, published in PNAS this September, found a striking correlation between savannas, the evolution of plant spinescence, and the rise of ancient bovids.

“Savannas grow in climates and on soils that also support closed forests. So there is no ‘savanna climate’ uniquely predicting where they occur. Their rather abrupt appearance in the Miocene implies the emergence of new ecological processes favouring grasses at the expense of forest trees,” wrote Dr. William Bond of the University of Cape Town, one of the co-authors of the paper.

But how to even begin?  The fossil record, in general, doesn’t contain everything scientists would need to completely recreate any particular ancient ecosystem.  Where one might find animal fossils, that same rock may not preserve plant fossils, and vice versa.

The authors drew upon knowledge of today’s African megafauna, how it impacts existing ecosystems, and compared that with information about African fossils from the Miocene.  Elephants, for example, are known to knock down trees.  Antelopes, sheep, deer and other browsers  maintain open ecosystems today. Could their ancient ancestors have done the same?

“We had worked on fire as a major factor promoting [the spread of savannas,]” explained Dr. Bond. “We used a marker, underground trees, of fire-maintained higher rainfall savannas to explore their origins. Our dates of the emergence of ‘fire savannas’ in Africa were remarkably convergent with dates for ‘fire savannas’ in South America (cerrado) and also consistent with the sparse fossil record (Maurin et al 2014, New Phytologist and Pennington and Hughes, same issue with a commentary on our paper). In drier savannas, grasses do not build up enough fuel to burn regularly.  We wondered whether mammal browsing may help maintain open savanna vegetation where fire is less important. We needed a marker of savannas with high herbivore pressure and chose spiny plants.”
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A sparrow sits amongst the large white thorns of an Acacia tree, Kenya; photo: Richard du Toit, from Getty Images

 

In other words, fire was originally thought to be the reason behind the rise of savannas.  Evidence of fire has been found in fossil charcoal,  in paleosols and in fossil teeth.  The authors of this paper expanded their research to include fossil mammals.  Knowing that today’s savanna plants defend themselves with thorns from browsing mammals, the authors wanted to see if these same defenses occurred in fossil plants.

They had an incredible tool to help with this task: the African Centre for DNA Barcoding.

 

Types of thorns - Supplemental info, Charles-Dominique et al

Fig. S1. Types of spines. (A) Prickles: Zanthoxylum davyi. (B) Straight stipular spines: Vachellia robusta. (C) Straight stipular spines and stipular hooks: Ziziphus mucronata. (D) Straight thorns: Gymnosporia harveyana. (E) Hook thorns: Scutia myrtina. (F) Straight stipular spines and stipular hooks: Vachellia tortilis. (G) Stipular hooks: Senegalia nigrescens. Es, epidermic spine; L, leaf; Ls, leaf scar; Ss, stipular spine; T, thorn (i.e., branch with a sharp tip); from Charles-Dominique et al. http://www.pnas.org/cgi/content/short/1607493113

 

What they discovered was that savannas existed before the large-scale evidence of fire, rather than simply because of it.  Thorns didn’t appear until well after the rise of proboscideans and hyracoids, indicating that neither of these species triggered the need for that specific physical defense.  Interestingly, the rise of ancient bovids (and possibly ancient giraffoids) corresponds to the emergence of thorns in the Miocene.  Ultimately, they found that spinescence evolved at least 55 times.

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Browsing impala — a type of modern antelope (bovid); photo by: annick vanderschelden photography, from Getty Images

“One might think that spines are a general defence against an archetypal mammal herbivore,” Dr. Bond wrote. “So we were most surprised at the late emergence of spines in African trees. We speculate that spines don’t work to limit food intake by proboscideans (a reasonable guess based on extant elephant feeding) and also hyracoids. But just why hyrax don’t select for spines is an intriguing puzzle. Observations on the remaining few hyrax species may be informative.”

“Physical plant defences are far less studied than chemical defences. They seem to resemble more plant-pollinator or plant-disperser interactions in being adapted to particular types of herbivore with particular modes of feeding. Spines don’t work for monkeys, for example, with their ability to pluck leaves with their fingers and manipulate branches. I have also worked on plant physical defences against extinct giant browsing birds (moas in New Zealand, elephant birds in Madagascar). They are utterly different from spines and exploit the limitations of beaks and the ‘catch and throw’ swallowing mechanism of the birds.”

“Molecular phylogenies dated with fossils were our main tool for exploring the past,” he continued. “Molecular phylogenies for mammals have been controversial tending to give much older dates for lineages than the fossil evidence. We used a recent phylogeny for bovids produced by Bibi (2013, BMC Evol Biol) using many more fossils than usual for calibrating the molecular phylogeny. Christine Janis, in an early e-mail exchange, kindly pointed us to the excellent book on Cenozoic mammals of Africa (Werdelin, Sanders 2010), among others, for help in reconstructing herbivore assemblages at different times.”

 

Spiny species distribution - Charles-Dominique et al PNAS

Screenshot of species distribution and environment correlates; from Charles-Dominique et al. http://www.pnas.org/cgi/content/short/1607493113

 

The sheer size and scale of the African continent is overwhelming.  This recent paper doesn’t focus on part of it; it encompassed the entire continent. When I asked Dr. Bond if this project was as enormous as it seemed, he wrote, rather amusingly, “Yes! Very daunting for me. People used to publish papers analyzing environmental correlates of single species distributions. Our team did the analyses for 1852 tree species. The mammal data was also enormous. Seems the younger generation is used to these vast data sets. I was amazed at the speed at which results became available.”

The list of websites cited in this paper (http://www.ville-ge.ch/cjb/; http://www.theplantlist.org; http://www.naturalis.nl/nl/; http://www.gbif.org; http://www.fao.org/home/en/) and the information those websites provide prompted me to ask whether it was fair to say that this paper could not have been written at an earlier point in time (without that online data). I also wondered if it was fair to say that science (in instances like this, where researchers share data online and make it accessible to others worldwide) is becoming more cooperative or team-oriented.

He responded: “You are absolutely right about ‘more cooperative and team-oriented’. The availability of massive data sets, and the tools to analyze them, has made analyses such as ours possible. Our team included people with diverse skills and knowledge. Hard to see how one or two researchers could have pulled this off.”

“The study is the outcome of several years of collaboration between systematists led by Prof Michelle van der Bank of the University of Johannesburg, ecologists working with me at the University of Cape Town, and a phylogenetic specialist, Prof Jonathan Davies from McGill University in Canada and an old friend of Michelle.

“Michelle, who heads up a DNA barcoding unit, had invited me to work with her group on ecological questions that could be addressed with molecular phylogenies. It has been a wonderful collaboration.

Tristan Charles-Dominique worked with me as a post-doc bringing new skills in the French tradition of plant architecture. He made great strides in understanding plant traits of savanna trees. His work on physical defences against mammal herbivores is the most original and important contribution since the 1980s in my view.

Gareth Hempson,  also an ex post-doc with me, had spent a great deal of effort compiling a map of African mammal herbivore abundance, and species richness, as it would have been ~1000 years ago (Hempson, Archibald, Bond 2015, Science). He combined mammals into functional groups which helped enormously in simplifying ecological functions of different groups. His participation allowed us to link the key mammal browsers to concentrations of spiny plant species.”

“It’s a rare combination of people to address a big question.”

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Gerenuk, or giraffe antelope (Litocranius walleri) feeding from a bush; photo: 1001slide, from Getty Images

 

————————–

*including our own species!

**an unintended pun


It was a great honor and a great pleasure connecting with Dr. William Bond, who–despite a very busy schedule and an unfortunate stay in the hospital–responded so quickly to my inquiries!  Thank you so much, Dr. Bond!  The research by you and your colleagues has opened a fascinating door for me!!

 

References

Spiny plants, mammal browsers, and the origin of African savannas,Tristan Charles-Dominique, T. Jonathan Davies, Gareth P. Hampson, Bezeng S. Bezeng, Barnabas H. Daru, Ronny M. Kabongo, Olivier Maurin, A. Mathuma Muaysa, Michelle van der Bank, William J. Bond (2016), PNAS, vol. 113 no. 38. DOI: 10.1073/pnas.1607493113

What Plants Talk About, Nature, PBS, 2013

Savanna fire and the origins of the ‘underground forests’ of Africa, Olivier Maurin, T. Jonathan Davies, John E. Burrows, Barnabas H. Daru, Kowiyou Yessoufou, A. Mathuma Muaysa, Michelle van der Bank, William J. Bond (2014), New PhytologistDOI: 10.1111/nph.12936

Jurassic Park, (movie) Universal Studios, directed by Steven Spielberg, 1993

 

How Trees Talk to Each Other - Dr. Suzanne Simard TED

 

Further FASCINATING information on contemporary plants

How Trees Talk to Each Other, Suzanne Simard, TED talk, June 2016

Published papers by Suzanne Simard, University of British Columbia

The Hidden Life of Trees, Peter Wohlleben, 2016, Greystone Books

How Trees Fight Back, Dave Anderson, Chris Martin, and Andrew Parrella, “Something Wild,” NH Public Radio, September 23, 2016

The Herbivore Elicitor-Regulated1 (HER1) gene enhances abscisic acid levels and defenses against herbivores in Nicotiana attenuate plants, Son Truong Dinh, Ian T. Baldwin, Ivan Galis, Plant Physiology,162, 2106-2124, 2013. doi:10.1104/pp.113.221150.

Plant Kin Recognition Enhances Abundance of Symbiotic Microbial Partner, Amanda L. File, John Klironomos, Hafiz Maherali, Susan A. Dudley, PLOS One, September 28, 2012.

Fitness consequences of plants growing with siblings: reconciling kin selection, niche partitioning and competitive ability, Amanda L. File, Guillermo P. Murphy, Susan A. Dudley, Proceedings of the Royal Society B, vol: 279, issue 1727, 2012. doi: 10.1098/rspb.2011.1995

 

Hidden Life of Trees - Peter Wohlleben

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Exciting New Info About Mastodons and Humans – Yukon Paleontology, Part 1

“Good morning!”

It’s not just a greeting; it sounds like a proclamation.

The voice on the other end of the phone is deep, melodic, and—as our conversation progresses—punctuated with moments of laughter.  We have been discussing paleontology in the Yukon, and with each new detail, I begin to wonder why this territory is not making regular international headlines.

Dr. Grant Zazula’s work is fascinating, and it is neither a short phone call nor the only communication we’ve exchanged. And yet, it is all that I can do not to encourage him to keep going, long after social decorum dictates that he has been more than generous with his time.

Dr. Zazula and mastodon leg

[image of Dr. Grant Zazula with a mastodon ulna, part of the Earl Bennett mastodon, courtesy of the Government of Yukon]

Dr. Zazula is the Yukon paleontologist, a job that has only existed since 1996. His own tenure began in 2006.  With an office in Whitehorse, the capital of the territory, his work oversees an expanse of Canada that abuts Alaska.  It is a land of dramatic beauty, where colors dance in the sky and mountains tower in silent grandeur.

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His most recent paper, co-written with 14 other people, made news throughout the world and continues to attract media attention. In it, the scientists present data that completely overturns previously believed information about extinct animals and the impact that humans may or may not have had upon their survival.

“[T]here were two radiocarbon dates in the literature from Yukon mastodons,” he explained in an email. “One that was ~18,000 and the other 24,000 years old.”

“Based on analysis of the paleoecology, that was a time when steppe-tundra grasslands covered Alaska, Yukon and Beringia. There were probably no trees, few shrubs and almost no standing water. It was very cold and, especially, dry. This seemingly is not good mastodon habitat. So either the dates were incorrect, or our understanding of mastodon ecology, behavior and adaptations need[s] to be revised.”

Various species of mastodon once existed throughout the world.  Although their fossils look elephantine, they are not believed to be direct ancestors of today’s elephants. They are, however, part of the same umbrella mammalian group: the Proboscidea (so-named for the trunks possessed by many—but not all–of their members).  In North America, that group contained the American mastodon (Mammut americanum), the woolly mammoth (Mammuthus primigenius), and the Columbian mammoth (Mammuthus columbi).

Cohoes mastodon

 [image of the Cohoes mastodon, NY State Museum, Albany; taken by the author]

Mastodons tended to have straighter tusks and were shorter than their mammoth cousins. They also ate hardier vegetation, food that required a much different tooth structure than mammoths.

ISM - Mastodon tooth

[image of mastodon tooth, courtesy of the Indiana State Museum]

ISM - Mammoth tooth

[image of mammoth tooth, courtesy of the Indiana State Museum; for more info about the differences between mammoths and mastodons, see this post.]

Parts of Siberia, Alaska and the Yukon were once connected in an area known as “Beringia.”  The Bering Strait did not yet exist, enabling animals and eventually the first humans to cross into our continent.  It is believed that humans arrived in what is now North America about 14,000 years ago.

And this is where the research of Dr. Zazula and his colleagues becomes particularly important.

Prior to their paper, one theory to mastodon extinction laid the blame upon first humans: it was proposed that they overhunted these animals.

Sampling 36 fossils and presenting 53 new radiocarbon dates, Dr. Zazula and his colleagues found that mastodons within Alaska and the Yukon were much, much older than the originally published dates.  In other words, their research suggests that mastodons from what was once Eastern Beringia were no longer present when the first humans appeared.

The path to this remarkable research did not happen overnight.

The foundation appears to have been laid by two different events: by the chance meeting of Dr. Zazula and a gold miner, and later, by the PhD work of a graduate student.

If one reads the acknowledgements on the aforementioned paper, Dr. Zazula references Earl Bennett as both the donor of a partial mastodon skeleton and his inspiration to learn more about mastodons within the Yukon.

“Earl is a great Yukoner,” Dr. Zazula wrote when asked about this. “He mined for gold underground in the winters with a pick and shovel, decades ago. He worked on big gold dredge machines. And, he loves paleontology.

“While mining, he made collections of Ice Age bones that were just left around the mining camp or were encountered while mining. He eventually amassed an amazing collection.

“In the early 1970’s a gold dredge on Bonanza Creek hit a skeleton of a mastodon. An incredibly rare find! Someone collected it and was looking to sell it. So, Earl bought the skeleton just to make sure that it never left the Yukon. He had it in his garage for decades.

“One day a mutual friend introduced me to him in a coffee shop, about a year after starting my job [as the Yukon paleontologist]. He said that he had a mastodon skeleton and wanted me to see it. I ‘corrected’ him, saying that it was more likely a mammoth, because we almost never find mastodons in the Yukon. He assured me he know the difference and said he would see me tomorrow at my office.

“The next day he backed his truck up and in it was a partial mastodon skeleton. I couldn’t believe it. There were several postcranial bones, some vertebra, scapula, parts of the skull and parts of the mandible with teeth. It was amazing. I wanted to find out how old it was, and that was one of the inspirations for this project. Earl is a good friend now and big supporter of our research.”

Bennett mastodon skeleton

[Paleontologist Grant Zazula with a partial American mastodon (Mammut Americanum) skeleton found on Bonanza Creek and donated to the Yukon fossil collection by Earl Bennett, from Ice Age Klondike, courtesy of the Government of Yukon]

That partial skeleton was indeed one of the many fossils sampled for the paper.

Dr. Jessica Metcalfe, one of the co-authors, also prompted this research when conducting work for her PhD.

“[S]he was doing a project looking at stable isotope ecology of mammoths and mastodons in various places in North America,” said Dr. Zazula.

Jessica Metcalfe with mammoth bone

[image of Dr. Jessica Metcalfe with mammoth bone, courtesy of the Government of Yukon]

Her work included Yukon fossils that were sent to the lab at the University of Arizona to be radiocarbon dated.   Those dates turned out to be older then 50,000 years old.

“So that’s what got me thinking,” he continued, “‘well, maybe those original published dates are wrong.’”

“The first step was to re-date [the specimens that had produced the original published dates]. The new dates turned out to be >50,000 years. So we knew there was a problem with the previous dates. We figured then we should date as many as we could get our hands on.”

This lead Dr. Zazula to connect with Dr. Ross McPhee, another co-author.

“I got in touch with him early because he oversees collections at the American Museum of Natural History, [and] he has a big interest and lots of experience working on Ice Age extinctions. [H]e’s an excellent writer and really kind of kept us going with some of the writings. He was really integral to keeping things together.”

The paper eventually involved a total of 15 people.

“I feel pretty strongly that if you worked on it and contributed to it, then you should be considered an author,” Dr. Zazula stated.  “So it ended up being a long list.”

One of the first aspects their paper addresses is the reason behind why the original published dates are incorrect: the dating analyses were contaminated by fossil conservation methods.

“Humic acids in soils can be absorbed by the bones and teeth and chemically bind themselves to the collagen,” he wrote, explaining further. “So, modern ‘young’ carbon in those acids basically contaminates the ‘old’ collagen in the ancient fossil. And, it can be tricky to remove.

“The same with consolidants in museums. Varnish, glue, and other substances to preserve fossils can be absorbed into the bone and chemically bind with the collagen in the bone. These substances probably contain young, modern carbon which messes up the radiocarbon dating measurements.”

When asked whether museums continue to use the same preservation products that contaminated the dates, he wrote, “Yes, for sure. The thing is now museums keep better records of what they use. Many of the fossils we dated were collected in the 1940’s or at least several decades ago. Museums were not that vigilant about keeping detailed records on those things then. Also, they seemed to put preservatives on everything. Now, at least if we know what was put on it, the chemistry can by developed to remove it. Most of the common preservatives now are soluble in alcohol or acetone and can be dealt with. The problem is when they are unknown.”

We discussed this further by phone.

“One thing about Alaska and the Yukon,” he said, “is that the Ice Age bones that come out of the ground are so well preserved because of the permafrost. In other localities, say, the deserts of the American Southwest or the Great Basin or the Plains, where bones have been out in the sun and [are] dry and hot, they [sometimes] fall apart really easily when they come out of the ground. They need to be glued and consolidated with these various types of museum products.

“So you kind of have to weigh the different values.

“Say if it’s a specimen that’s already been radiocarbon dated, and it starts to slowly disintegrate, well, then you kind of have to intervene or else you’re just going to end up with a box of dust and broken bone. You have to decide whether the importance is more with display or preservation of the morphology versus needing to radiocarbon date or other types of analysis.

“[Y]ou have to look at the pro’s and con’s of whether the sampling [for radiocarbon dating] will ruin the specimen or not, and what is the potential information that can be gained by doing it. To me, I feel that having a research collection [in the Yukon], it’s all about research and learning new things from these specimens.”

Ultimately, I wondered whether Dr. Zazula expected the results he and his colleagues uncovered.

“I wasn’t quite sure,” he answered. “I had the gut feeling that these previously published radiocarbon dates were probably wrong. It didn’t make a lot of sense ecologically to have mastodons living in the far North when it was seemingly habitat they couldn’t live in: habitat with grassland and cold, dry steppe tundra conditions, no trees and very few shrubs.

“But there [was] also a part in the back of my mind that thought, ‘well, if those [previously published dates] were right, that’s maybe even more interesting because they are telling us something about mastodons and their behavior and their adaptations that we didn’t know before.’”

————

It was a great honor and pleasure to connect with Dr. Grant Zazula! Not only patient with my myriad questions, he is an adept and fascinating ambassador for the Yukon. A Mammuthus columbi-sized thank you to him!

A Mammuthus columbi-sized thank you to Dick Mol, as well, who is the reason behind this post!

Dick Mol with horse skull

[image of Dick Mol with fossil horse skull, found near Dawson City, Yukon; courtesy of the Government of Yukon]

Yukon Paleontology Program: http://www.tc.gov.yk.ca/palaeontology.html

Articles and publication referenced:

 

Listen to Dr. Zazula discuss his paper on the CBC’s Quirks & Quarks: http://www.cbc.ca/radio/quirks/quirks-quarks-for-dec-6-2014-1.2864605/mastodons-made-an-early-exit-from-the-north-1.2864634