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.

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.”


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.

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.”

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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