Grime reviews are a series of Reviews honouring eminent ecologist J. Philip Grime. In this blog post, Tara Massad discusses her recent review ‘Plant defences as functional traits: A comparison across savannas differing in herbivore specialization‘, and the influence that Grime’s approaches to ecology had on her work:
J.P. Grime’s development of the field of plant functional ecology has inspired hundreds of ecologists and students of ecology to seek to understand why plants grow where they grow and express the traits they express1. These were two of the principal questions Grime himself sought to address, and although seemingly basic, they lead to a myriad of ecological questions that require both detailed observations and experiments to investigate.
To me, as a tropical chemical ecologist, the most fascinating ecological questions to ponder stem from Grime’s focus on the where’s and why’s of plant ecology and extend up a trophic level. I am particularly interested in how plant-herbivore interactions influence plant diversity in the tropics and how plant defences (chemistry in particular) mediate those interactions. So, when I was honored with the invitation to write a Grime Review in this series commemorating his work, I couldn’t help but want to highlight the importance of considering plant defences as defining functional traits and plant-herbivore interactions as influencing the why behind plants growing where they do.
I have lived and worked for many years in Gorongosa National Park, Mozambique, where I have the privilege to observe savannah plants ‘in action’ as they defend themselves from the charismatic grazers and browsers of African savannas and the (arguably more beautiful) caterpillars that also feed on their leaves. I have been fortunate to spend a lot of time working in Brazil and to have visited different parts of the cerrado—a savannah that, at a glance, could be confused with a mixed or broadleaf African savannah. That illusion is dispelled once you realize you can do your fieldwork in the cerrado without worrying an elephant might sneak up on you (it’s happened more than once!).
This means that we have two, seemingly similar, biomes with fairly similar plants (some are even cross-continental cousins in the same genera), but with very different guilds of dominant herbivores. The cerrado is well studied in terms of its Lepidoptera2, and leaf-cutter ants are also important herbivores3, but large mammals were erased from the scene about 15,000 years ago4. Not so long in evolutionary time, you might say, but plant defences (particularly chemistry) are quickly evolving traits—work from the Neotropics shows subspecies of a tree are actually divergent in defensive chemistry and sawfly larvae (they look like caterpillars but are actually related to wasps and bees) can definitely tell them apart5!
So, I thought it would be fun to extend Grime’s thinking to a cross-biome comparison of plants that are adapted to disturbance in the form of frequent fire and the stress of highly seasonal rains and herbivory. The distinguishing feature between these two groups (and the interesting point of the analysis) is the type of herbivore pressure they experience.
Ecologists have called fire a ‘generalist herbivore’—willing and able to consume just about anything6. Mammals have long been considered generalists as well (although advances in metagenomics are teaching us they are more specialized than originally thought7). Insects, on the other hand, are dominated by specialists8. Why would this matter? Well, plant defences differ in their efficacy against specialists and generalists, and plants also have limited resources to allocate to defending themselves against different guilds of herbivores (‘Should my limited carbon go to spines or to phenolics?’ we can imagine a plant figuratively asking itself). So, we can expect that plant traits related to defence will differ between African and South American species, while other traits—related to common selective pressures may be more similar.
That led to a dive into the plant trait literature and the extremely useful TRY database9, from where I extracted all the data I could find about defence related traits in African and neotropical savannah species. Unfortunately, and unsurprisingly, not much was to be found about plant chemistry. (Side note: If you’re looking to go into science—please consider chemical ecology!)
And, what came out of all this searching? A few potential patterns and a handful of questions for the future (one never wants to run out of those). First, unsurprisingly, spinescence and tough wood were more prominent where large mammals threaten leaves and tree trunks in Africa (fascinating work from South America shows the present day distribution of spinescent species actually overlaps with historical hotspots in large mammals richness!). And, possibly more interestingly, other traits also differ between continents. Leaves in African savannahs have more nitrogen and phosphorous, which could be influenced largely by soil rather than herbivores. But, leaves are tougher in savannahs without large mammals (which makes sense—a tough leaf is a bigger obstacle to a hungry caterpillar than to a kudu, for example).
Moving on to the best (and least studied) part—the chemistry… The data we have so far indicate that plants in the cerrado are more chemically rich than those in Africa. This requires targeted studies before any firm conclusions can be made, but we are at the right point in ecology to be able to conduct this type of research. The biggest deal in chemical ecology today is secondary chemistry metabolomics, and we are learning that chemical richness is itself an important defence (meaning the more different chemicals a leaf produces, the better defended it is). This should be especially important for plants faced with pressure from specialized insects, as those specialists are relatively constant selective pressures for novel defenses, and a plant’s chemical arsenal thus diversifies. Studying this will help us further understand plant defences as evolutionarily and ecologically critical plant traits and will allow us to use the invisible clues chemistry provides to understand Grime’s question of why plants grow where they do.
Tara Joy Massad, Gorongosa National Park, Mozambique.
Read Tara’s full Grime review online: Plant defences as functional traits: A comparison across savannahs differing in herbivore specialization
References
1 https://royalsocietypublishing.org/doi/10.1098/rsbm.2021.0021
2 Scherrer, S., Lepesqueur, C., Vieira, M. C., Almeida‐Neto, M., Dyer, L., Forister, M., & Diniz, I. R. (2016). Seasonal variation in diet breadth of folivorous Lepidoptera in the Brazilian cerrado. Biotropica, 48(4), 491–498. https://doi.org/10.1111/btp.12325
3 Costa, A. N., Vasconcelos, H. L., Vieira-Neto, E. H. M., & Bruna, E. M. (2008). Do herbivores exert top-down effects in Neotropical savannahs? Estimates of biomass consumption by leaf-cutter ants. Journal of Vegetation Science, 19(6), 849-U14. https://doi.org/10.3170/2008-8-18461
4 Sandom, C., Faurby, S., Sandel, B., & Svenning, J.-C. (2014). Global late Quaternary megafauna extinctions linked to humans, not climate change. Proceedings of the Royal Society B-Biological Sciences, 281(1787), 20133254. https://doi.org/10.1098/rspb.2013.3254
5 Endara, M.-J., Weinhold, A., Cox, J. E., Wiggins, N. L., Coley, P. D., & Kursar, T. A. (2015). Divergent evolution in antiherbivore defences within species complexes at a single Amazonian site. Journal of Ecology, 103(5), 1107–1118. https://doi.org/10.1111/1365-2745.12431
6 Bond, W. J., & Keeley, J. E. (2005). Fire as a global “herbivore”: The ecology and evolution of flammable ecosystems. Trends in Ecology & Evolution, 20(7), 387–394. https://doi.org/10.1016/j.tree.2005.04.025
7 Kartzinel, T. R., Chen, P. A., Coverdale, T. C., Erickson, D. L., Kress, W. J., Kuzmina, M. L., Rubenstein, D. I., Wang, W., & Pringle, R. M. (2015). DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proceedings of the National Academy of Sciences of the United States of America, 112(26), 8019–8024. https://doi.org/10.1073/pnas.1503283112
8 Forister, M. L., Novotny, V., Panorska, A. K., Baje, L., Basset, Y., Butterill, P. T., Cizek, L., Coley, P. D., Dem, F., Diniz, I. R., Drozd, P., Fox, M., Glassmire, A. E., Hazen, R., Hrcek, J., Jahner, J. P., Kaman, O., Kozubowski, T. J., Kursar, T. A., … Dyer, L. A. (2015). The global distribution of diet breadth in insect herbivores. Proceedings of the National Academy of Sciences, 112(2), 442–447. https://doi.org/10.1073/pnas.1423042112
9 Kattge, J., Diaz, S., Lavorel, S., Prentice, C., Leadley, P., Boenisch, G., Garnier, E., Westoby, M., Reich, P. B., Wright, I. J., Cornelissen, J. H. C., Violle, C., Harrison, S. P., van Bodegom, P. M., Reichstein, M., Enquist, B. J., Soudzilovskaia, N. A., Ackerly, D. D., Anand, M., … Wirth, C. (2011). TRY – a global database of plant traits. Global Change Biology, 17(9), 2905–2935. https://doi.org/10.1111/j.1365-2486.2011.02451.x
