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

Sousatitan: Brazil’s oldest sauropod bone found in a sea of trace fossils

One man happened to see the bone; one scientist happened to see the picture he posted online.

These two chance occurrences brought about a remarkable discovery: the first fossil dinosaur bone to be found where none have been found before.

Not only is it the first dinosaur bone in the area, it is also the oldest sauropod bone in Brazil to-date, a new as-yet-unnamed species of titanosaur.

Luiz Carlos Gomes was looking for fossil footprints in Sousa, Brazil. Hundreds upon hundreds of trackways, footprints and other trace fossils have already been found in Paraíba–a state in the West coast of that country and where Sousa is located–in an area known as the ‘Valley of the Dinosaurs‘ (‘Vale dos Dinossauros‘). But actual bone fossils? None.

None, that is, until he recognized actual bone within rock.

“He was the main [person] responsible for the discovery,” wrote Dr. Aline Ghilardi, paleontologist at Universidade Federal de São Carlos, in an email. “Luiz Carlos is a very curious retired gentleman whose hobby is to look for dinosaur footprints. He found the bone by chance (it was still inserted into the rock, so he knew it was not only a recent bone), took a picture of it and posted on the internet. Searching information about the area, I found the photo by chance, and, knowing the importance of the discovery, immediately got in touch with him.”

 

Trackway from Bone Collectors Video - Brazil

More tracks in Brazil from Bone Collectors video

Images of fossil footprints found in the Valley of the Dinosaurs (Vale dos Dinossauros) in the state of Paraíba, Brazil; screenshots from the Colectionadores de Ossos (Bone Collectors) video; courtesy of Aline Ghilardi and Tito Aureliano.

 

Luiz Carlos and Aline from Colecionadores de Ossos video

Image of Luiz Carlos S. Gomes and Dr. Aline Ghilardi; screenshot from the Colectionadores de Ossos (Bone Collectors) video; courtesy of Aline Ghilardi and Tito Aureliano.

 

That bone was the subject of a paper published this past July in Cretaceous Research by Aline Ghilardi, Tito Aureliano, Rudah Duque, Marcelo Fernandes and Anusuya Chinsamy-Turan (“A new titanosaur in the Lower Cretaceous of Brazil“).

 

DSC_0025 - Sousa fossil in-situ

Fossil of the sauropod bone found in-situ in Sousa, Brazil, nicknamed ‘Sousatitan’; courtesy of Aline Ghilardi.

 

Through its bone histology, they believe this fibula belonged to a young titanosaur, rather than a small adult.  They noted rapid growth, and they highlighted an aspect within the bone that intrigued them.  In their paper, they point out that “…the lateral part of the bone wall has what appears to be bone tissue not formed in laminae and a predominance of longitudinally orientated vascular channels within a woven bone matrix.”

“This suggests that different parts of the bone wall [are] growing at different rates,” wrote Dr. Anusuya Chinsamy-Turan, paleobiologist and professor at the University of Cape Town, “i.e.: the rate of bone formation is not constant around the whole cross section of the bone wall.”

Research from Anusuya Chinsamy from Colecionadores de Ossos video

Image of “fibrolamellar bone tissue in the process of being deposited on the medial side of the bone wall” and Anusuya Chinsamy-Turan; screenshot from the Colectionadores de Ossos (Bone Collectors) video; courtesy of Aline Ghilardi and Tito Aureliano.

Their comparisons with other titanosaur fibula indicate it is a new species, although the authors are cautious about this.  And using a complicated mathematical formula, they can estimate the size of Sousatitan, the nickname they have given this dinosaur.

Tito Aureliano, a PhD student at the Universidade Federal de Pernambuco, helped elucidate how, equipped with a single fossil bone, they could make an educated guess about its size. His solution involved tweaking a previously published equation and quite a bit of ichnofossil measurement.  Keep in mind that the Valley of the Dinosaurs has at least 74 known sauropod footsteps.

Tito Aureliano from Colecionadores de Ossos video

Tito Aureliano; screenshot from the Colectionadores de Ossos (Bone Collectors) video; courtesy of Aline Ghilardi and Tito Aureliano.

 

“We used equations in two steps in our paper,” he explained by email, “because we needed to relate and compare one single fossil specimen to the abundant ichnospecimens from Sousa. The most accurate and mathematically secure way to do that (and [to avoid] speculation) was calculating hip height joint from footprints and total leg height from the bone we found.  We didn’t work with total length because that varies quite a lot in Titanosauria, and it wouldn’t be [scientifically useful].”

“First, we observed titanosaur tracksites from the same age as Sousatitan’s leg size.  We measured the diameter of every ‘back leg’ footprint available at Rio Piranha Formation outcrops.  Then, we calculated the hip height of all titanos that roamed the area at this formation and noticed there were a variety of sizes in individuals.

Comparative image of titantosaur fibula

 

 

Fig. 4.; image from A new titanosaur from the Lower Cretaceous of Brazil, Cretaceous Research.

“Previous authors developed equations to predict general dinosaur hip heights from tracksites, but if you are working specifically with titanosaur ones, you should work with the Argentinian equation.  González-Riga found a complete articulated titano leg in the same area he has encountered large footprints that fit exactly in size with his fossil.  By using this evidence, he was able to develop this accurate equation to estimate hip height from a single titanosaurian footprint.

“Secondly, we had to estimate Sousatitan’s leg size. We had just one single bone. How did we do that?  In González-Riga’s paper I mentioned before, he also presented a formula to calculate total leg length from its skeletal elements.  The major problem is that it had so many variables and geometry elements in it.  It would be impossible [to use] if a scientist has only one or two of these elements.  So, I worked on the equation to simplify it into just three variables: femur, ulna and fibula length. H = ¼1.106*(0.96F + T), where H represents hip joint height, F is femur length, and T is tibia length.  Now colleagues with less titanosaur limb bones [can use] González-Riga’s original idea with what they have.”

 

Sousatitan fossil from Colecionadores de Ossos video

A view of Sousatitan’s fibula (or ‘DGEO-CTG-UPFE-7517’), viewed from every angle; screenshot from the Colectionadores de Ossos (Bone Collectors) video; courtesy of Aline Ghilardi and Tito Aureliano.

 

Size comparison Sousatitan

 

Great depiction of the estimated size of Sousatitan (in black) with the fossil found; image from A new titanosaur from the Lower Cretaceous of Brazil, Cretaceous Research.

 

Tito continued, “‘Ok, a cool new formula with three elements. But you have just one! How did you do it then?’

“It’s simple morphometry.  I gathered limb bones from a lot of different titanosaur genera and measured the ration between these three bones. Then, I could estimate the theoretical size of the other limb bones.”

Sousa Basin stratigraphy

Sousa Basin stratigraphy; image from A new titanosaur from the Lower Cretaceous of Brazil, Cretaceous Research.

 

Coming from an area of the United States known more for ichnofossils than bone fossils, I share their excitement.

And yet, “internationally, for now, we have only observed colleagues’ mentions regarding the work and its importance,” wrote Dr. Ghilardi.

Fortunately, this sense of excitement seems to permeate Brazil.

“The discovery is getting lots of attention in Brazil, from both our colleagues and the popular media,” she continued. “The bone’s discovery was announced in all major newspapers of the country and, [thus far], in two of the largest television channels of Brazil.  Visits to the ‘Vale dos Dinossauros’ Park (where the bone is now housed) increased significantly after the first announcement of the discovery in popular media.  The dinosaur’s nickname got very popular and soon reached even Wikipedia in Portuguese.”

Aline Ghildardi from Colecionadores de Ossos video

Dr. Aline Ghilardi; screenshot from the Colectionadores de Ossos (Bone Collectors) video; courtesy of Aline Ghilardi and Tito Aureliano.

 

When I asked what brought these six scientists–from Brazil and South Africa–together on this research, Tito Aureliano explained that he and Dr. Ghilardi are married.  In addition, he explained, “our friend, [Rudah] Duque, is a technician in paleontological preparation at PaleoLab (UFPE, Recife city). Prof. Barreto is the chief of the PaleoLab. We have been working together for the past four years visiting the least explored areas of NE Brazil in search of new Cretaceous fossils.

Prof. Anusuya had previously assisted us in pterosaur research [that included] some histological observations. She possesses not only great knowledge on the subject, but she is also very polite and friendly. Aline and I think it was wonderful to work with her and to learn from her.

“Our friend Marcelo is the chief of the Paleontological Museum of the Universidade Federal de São Carlos. He is a renowned specialist in dinosaur ichnofossils (he is that guy that published the first urolite, ‘dinosaur pee‘).”

Marcelo Fernandes from Colecionadores de Ossos video

Dr. Marcelo Fernandes; screenshot from the Colectionadores de Ossos (Bone Collectors) video;  courtesy of Aline Ghilardi and Tito Aureliano.

 

Urolites from Fernandes et al paper from Colecionadores de Ossos video

Trace fossils from paper by Fernandes et al corresponding to liquid wastes (urolites!); screenshot from the Colectionadores de Ossos (Bone Collectors) video;  courtesy of Aline Ghilardi and Tito Aureliano.

 

Without doubt, the authors will continue to search for additional bone fossils in the area.

“The intention is to seek funding to continue doing searches in the region.  We hope to find more material in [the] Lagoa do Forno site (including other parts of the same individual) and also other promising localities,” Dr. Ghilardi wrote.

 

Sousatitan map of discovery

 

Location of the find and map of Brazil; image from A new titanosaur from the Lower Cretaceous of Brazil, Cretaceous Research.

 

“I believe it is worth mentioning the importance of the contact between researchers and the population,” she added.  “It is always a good partnership and yields good results.  The locals are interacting every day with the fossiliferous rocks, therefore, they are the most likely people to find materials such as this bone.

“[Making] people feel part of the scientific knowledge process is a very effective way to preserve paleontological heritage for future generations. And not only create a sense of protection about it….but also a sense of pride in their heritage and their land.  Finally, this can be a fundamental social change factor for the local population, which is so needed in so many respects.”

Referencing Sousatitan’s discoverer, Luiz Carlos Gomes, she wrote, “Today, he is very proud of [what has transpired since the initial find].”

 

Sousatitan by Marcos Paulo

Depiction of Sousatitan amongst larger sauropods of the same species; artwork by Marcos Paulo; courtesy of Aline Ghilardi and Tito Aureliano.

You can help the Bone Collectors continue to educate the public by donating here

 

It was a remarkable honor and pleasure connecting with Dr. Aline Ghilardi, Tito Aureliano and Dr. Anusuya Chinsamy-Turan. That cannot be stated enough! It was exciting to learn more about their incredible discovery, and they were very generous with their time and help. From New England to Brazil and South Africa: THANK YOU!!

 

References:

  1. A new titanosaur from the Lower Cretaceous of Brazil, Aline M. Ghilardi, Tito Aureliano, Rudah R. C. Duque, Marcelo A. Fernandes, Alcina M. F. Barreto, Anusuya Chinsamy; Cretaceous Research, Vol 67, December 2016; http://dx.doi.org/10.1016/j.cretres.2016.07.001

Videos by the Bone Collectors (Colecionadores de Ossos), several authors of this research:

Further Information:

  1. Bone Collectors – Colecionadores de Ossos: http://bonecollectors.org (website of several of the authors in this paper)
  2. The Bone Collectors’ Blog: http://scienceblogs.com.br/colecionadores
  3. Bone Collectors – Colecionadores de Ossos on YouTube: https://www.youtube.com/user/ColecionadoresOssos
  4. Um novo dinossauro Brasileiro: blog post about the Sousatitan discovery by Aline Ghilardi on the Bone Collector blog
  5. Occurrence of urolites related to dinosaurs in the Lower Cretaceous of the Botucatu Formation, Paraná Basin, São Paulo State, Brazil, Marcelo A. Fernandes, Luciana B. R. Fernandes, Paulo R. F. Souto, Revisita Brasileira de Paleontologia, July/August 2004
  6. Dinosaurs Without Bones, Anthony J. Martin, 2014, Pegasus Books — (Dr. Martin includes an illustration of one of the urolites discovered by Fernandes et al in this book; he also discusses their research on pages 245-246!)

 

Pegasus - Dinosaurs Without Bones, Anthony Martin