Theme 2. Ecology and evolution of plant defences

Two major defence strategies are used by woody plants against herbivory by mammals, termed architectural defences and direct leaf defences. Architectural defences are physical arrangements of plants that inhibit herbivore access to leaves and shoots, including spines and cagey architectures. Direct leaf defences are leaf properties that reduce the value of leaves as food for herbivores. Spines are a common feature of architecturally defended plants that are a widespread across terrestrial ecosystems, but their diversity and ecology is a field with many open questions.

We have so far focussed questions on functional diversity, biogeography and evolution of architecturally defended plants, but with an especial focus on spiny plants:

1. Do architecturally defended plants and direct leaf defender plants have distinct functional syndromes?
2. Which soil and climate characteristics select for spiny plants? and for different types of spines?
3. When did spiny plants evolve worldwide and what drove their evolution and diversification?

This research is accomplished through common garden experiments, geographical data analyses, and phylogeographic and paleological analyses.

We have more recently branched into understanding how mammalian herbivores have responded to plant defences through their skull morphology.

Key findings

Ecology

• In savannas worldwide, spiny and non-spiny Fabaceae have different functional trait syndromes (Tomlinson et al. 2016). Spiny species possess small leaves with high nutrient contents and high photosynthetic rates that can be defended by spines but this comes at the cost of total leaf mass fraction and thus at the cost of growth rate. Non-spiny species possess large leaves with low nutrient contents which ensures that they are less favoured as food by mammals (direct leaf defence), but the low leaf nutrients compromise their photosynthetic rates and thus comes at the cost of growth rate. These different strategies suggest that architecturally defended species and direct leaf defending species trade off along an LMF-ULR spectrum, which suggest that architectural defenders increase towards drier or more fertile environments whereas leaf defenders increase towards wetter and more infertile environments.
• Spine types are distributed along the leaf economic spectrum (Armani et al. 2020) with prickle species generally being associated with fast growth rates and high leaf productivity traits while leaf spines are slow-growing and associated with conservative traits and high levels of leaf chemical and structural defences. Thorns are in-between. The work in this project further showed that early growth patterns differ between spine types (Armani et al. 2019). The likely explanation is developmental constraint: leaf spines can be directly recruited onto emerging leaves, whereas thorns are modified secondary stems so they can only appear after full emergence of primary axis stems.
• Spine types differ in their efficacy against mammalian herbivores (Gelin et al, in preparation). We investigated how well different types of spines (prickles, thorns, leaf spines) defend against mammalian herbivores. All spine types reduced leaf removal by herbivores, but leaf spines were the most effective defenders and prickles were the least effective defenders. Combined with the trait data this confirms that the different spine types are aligned along a trade-off from slow growth, higher defence to fast growth, lower defence.
• Leaf phenolics change differently across soil fertility gradients for architecturally defended versus non-architecturally defended species (Wang et al. 2023). The results suggest that architectural defenders are constrained in their ability to generate phenolic defences, providing a plausible explanation as to why they need architectural defence.
• Spiny plants and plants with different spine types are differentially distributed across climate and edaphic space (Tomlinson et al., Biological Reviews). Using species distribution data combined with climate and soil data, we show that spiny plants are found in areas with greater aridity, lower temperature, or greater soil fertility. Separation of spine types along temperature gradients suggest developmental constraints on certain spine types, while separation along aridity and fertility gradients suggest trade-offs along those gradients.
• Trunk spines represent a unique type of spine that serves to defend trunks from bark-feeders and climbing animals (Lefebvre et al. 2022). Trunk spines are associated with trees and lianas and they have evolved from different organs, as observed for spines that defend savanna trees, but their spatial location means their function is different.

Evolution

• Architecturally defended plants underwent a two-step evolutionary process (Anest et al. 2024), first developing dense branching patterns and then later evolving spines as additional defences.
• The evolutionary radiations of spiny plants are linked to mammal radiations and cross-continental dispersal (Gelin et al, bioRxiv). The timing of stem spine emergence across continents matches the evolution of large mammal herbivores. This provides clear evidence that among extant angiosperm lineages, spines first evolved as defences against mammals and not against earlier radiations of herbivorous dinosaurs or insects. Spiny plant radiations are mostly due to colonisation events from other continents, indicating pre-adaption to mammal herbivory was a huge evolutionary advantage.
• Skull morphology of mammalian herbivores show systematic changes across climate aridity (Quibod et al. 2023). This analysis, which covers >80% of extent bovids and cervids, shows that grazers show especially strong skull morphological changes across aridity gradients. The most likely explanation is changes to the physical properties of their diet plants across aridity gradients, which we are exploring further.
  

Publications

Anést et al. 2024. Block then sting: the two-step evolution of defensive architecture in herbivore-driven ecosystems. Nature Plants 10: 587–597. https://www.nature.com/articles/s41477-024-01649-4

Anest et al. 2021. Evolving the structure: climatic and developmental constraints on the evolution of plant architecture. New Phytologist 231: 1278-1295. https://doi.org/10.1111/nph.17296

Armani et al. 2019. Developmental constraints and resource environment shape early emergence and investment in spines in saplings. Annals of Botany124: 1133-1142. https://doi.org/10.1093/aob/mcz152

Armani et al. 2020. Structural defence is coupled with the leaf economic spectrum across saplings of spiny species. Oikos 129: 740-752.. https://doi.org/0.1111/oik.06960

Gélin et al. The evolutionary history of spines – a Cenozoic arms race with mammals. bioRxiv preprint. https://doi.org/10.1101/2023.02.09.527903

Lefebvre et al. 2022. Trunk spines of trees: a physical defence against bark removal and climbing by mammals? Annals of Botany 129: 541-554. https://doi.org/10.1093/aob/mcac025

Quibod et al. 2023. Diet-specific responses of skull traits to moisture gradients in bovids and cervids. Linnean Society Journal for Zoological Research. https://doi.org/10.1093/zoolinnean/zlad068

Tomlinson et al. 2016. Defence against vertebrate herbivores diverges into architectural and low nutrient strategies amongst savanna tree species. Oikos 125: 126-136. https://doi.org/10.11511/oik.0232

Tomlinson KW et al. 2025. The macroecology of spines on woody plants. Biological Reviews 100: 2396–2419. https://doi.org/10.1111/brv.70051

Wang et al. 2023. Leaf chemistry of architecturally defended plants responds more strongly to soil phosphorus variation than non-architecturally defended ones. Physiologia Plantarum. https://doi.org/10.1111/ppl.13856