Plant-Arthropod Interactions in the Fossil Record

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Insects are by far the most diverse and numerous of all animal groups and half of them are herbivores. When investigating any ecosystem, it is often wise to just look at plant leaves to get an indication for the diversity of insects there – and obviously, this principle also applies to fossil leaves and fossil insects, as can be seen in the picture below. It is slightly out of date (1998), but is still useful to show that we have these plant-arthropod interactions in the fossil record and for every relevant group. That’s what this post is about.
There are many types of traces that insects leave behind on leaves, and we’ll go through them now in no particular order (i.e. as they come in my head, not by order of prominence or importance). Important to note is the categorisation. There are ~150 recognised damage types, sorted by functional feeding groups (FFGs). It is the FFGs that will be listed here.

The most basic one is external feeding. You know, like caterpillars. I really shouldn’t have to explain this. Note that this comprises several FFGs, but I will not go through them in detail. There is hole feeding, which is the standard bite marks; surface feeding is similar, but does not go through the leaf. Margin feeding is when only the sides of the leaf are eaten, common in orthopterans and weevils. Skeletonisation is when everything but the veins of the leaf is eaten, and is common for weevils. Piercing and sucking is caused by sucking insects who pierce the leaf vein to suck out the nutrients – the pierce marks are left behind.

Some insects leave their eggs attached on or in leaves, leaving behind scars on the leaf where the eggs were attached or placed. They’re summed up in the oviposition FFG.
Some insect larvae feed on leaf tissues beneath the epidermis; this is called leaf mining and the trace they leave behind is called a leaf mine. Mining can also occur in other areas of the plant, for example the stem (where they feed on the xylem and cambium), seeds, flower heads, twig galls and the roots; for the purpose of clarity, I will only refer to them as leaf mine(r)s though. Examples of leaf miners include many individual dipteran genera that have evolved this independently, with it being an ancestral state in one dipteran family, the Agromyzidae (leaf-mining flies, 2800+ species) – it’s worth noting here that the earliest fossil evidence for the Agromyzidae, and indeed for the entire schizophoran flies (the “more evolved” flies) comes from fossil leaf mines; the picture above shows Phytomyzites schaarschmidti, an agromyzid leaf mine from the Eocene of Messel, Germany, and you can see how the larva moved through the leaf to eat. Agromyzids are obviously specialised for this feeding type and show all sorts of host plants, from angiosperms (flowering plants) to gymnosperms. Another group that exhibits leaf mining is the Lepidoptera (butterflies and moths), where leaf mining is the primitive state for the larvae, a fact made obvious by the fossil record of lepidopteran leaf mines, which are known from the Cretaceous. But leaf mining can be traced back even earlier to the Late Triassic, when beetles first started doing it – but this ancient origin doesn’t mean much, as leaf-mining beetles are rather rare now.
Another plant-arthropod interaction is galling. Some insects can make plants produce galls, abnormal tissue growths, in which the insect can then live and lay its eggs, as well as eat. These galls are excellent microhabitats and, in one case, have even led to the evolution of eusociality in a genus of gall-inducing thrips on Australian acacias, who have evolved a sterile soldier caste specialised for defending the gall. Obviously, galls are also found on fossil leaves. Finding what insects causes the fossil galls is a bit difficult as most fossils are compressed, but given that different insects have different-shaped galls, it is not at all impossible – it must be said that gall morphology is extremely specific to the galler. The types of insects that cause galls are diverse: there are gall midges (Diptera: Cecidomyiidae), gall mites (‘Acari’: Eriophyidae), gall wasps (Hymenoptera: Cynipidae) (picture above is a fossil wasp gall on oak (a, b) compared to modern gall wasp ones (c – e); the holes serve as larval chambers), etc. Galling first developed in the Cretaceous and is a relatively advanced form of damage, as the development of the insect is often dependent on the gall (they may pupate in the gall, or leave their larvae in there, as in the gall wasp).

Of course, let’s not forget that seeds are also found in the fossil record, and they can also show signs of having been eaten. The same goes for fungi, although that still needs more research (due to lack of specimens).

The picture below (again, from 1998, so may be outdated) shows that these FFGs have all been found in the fossil record and are well-represented.
As always, there are general trends that can be highlighted. Herbivory follows a climate gradient: in tropical regions, more herbivory occurs than in temperate regions. In arid areas, galling is much more frequent (galls are excellent microhabitats – full of nutrients, cool temperatures and safe). Another generalisation to be made is about the specialisation of insect herbivory: generalists are the exception rather than the rule, and specialisation to few or even single host plants is rampant – this hints at evolutionarily old associations (the origins of which can be uncovered by looking at the fossil record). From observations and studies in modern ecosystems, we also notice how specific insects can be on single trees: tall trees are attacked more often than shrubs (shrubs can invest more energy in defense rather than growth); sub-canopy leaves are attacked more often than canopy leaves (in a jungle; important because canopy leaves are more often preserved as fossils than low-lying leaves); young leaves are preferred to older leaves.

Let’s take a look at the first of the generalisations there: in warmer climates, there is more herbivory. The reason for this is rather simple. Insects eat plants to get nutrients. Warmer climates are always associated with a higher concentration of CO2. CO2 may cause plants to grow more, but the quality of the plant decreases (the more carbon there is, the less nitrogen there is), hence forcing the insects to feed more. The reason I wanted to bring this one up is because this is a good counterpoint to a common global warming denialist argument.

The importance of this topic not only involves documenting past insect biodiversity and the evolution of plant-insect associations. It’s also a very reliable indicator of climate and other, more sudden changes.
Of the latter, surely the most known is the K-T event, which involved an asteroid impact and extensive volcanism and the extinction of some vertebrates (who, to be honest, were already on their way out anyway). More noticeably (hooray for disciplinary bias!), there was a huge turnover in ecosystems – where before, you had a rich record of insect herbivory, afterwards you have nothing (except in two exceptional cases, one of which is a tropical rainforest where you expect rich feeding anyway). At least this is what we see in horizons on the North American continent (e.g. Labandeira et al., 2002). Once you move out of there and look at Paleocene floras of Argentina or of Europe (fossils pictured above), you don’t really notice much difference in terms of ecosystem functioning – this tells us basically that while the K-T event had a global impact in terms of taxonomic diversity, its major cause, the Chicxulub asteroid, had a much more localised effect that did not extend much beyond where it hit, as far as ecosystem functioning is concerned.
To look at a less explosive, but very societally [Ed. Note: Is that even a real word?] relevant scenario, we’ll turn to the late Palaeocene, ~53 Ma, when the Palaeocene-Eocene Thermal Maximum (PETM) occurred. This was a 100 thousand year spike in temperature (and, of course, CO2 levels, which tripled) and is by far the best analogue to modern global warming we have. The rate of warming was pretty extreme, as it is now, with the global temperature rising by 5°C within 10000 years. The biosphere reacted accordingly, with mass northward migrations of subtropical taxa as the climate became more suitable for them. Leaf damage from the PETM (pictured above) records how insect herbivores reacted. One fossil locality, the Bighorn Basin, spans the time from before, during and after the PETM, and has fossil leaves and associated insect damage. The trend is pretty clear: 57% of the leaves during the PETM were damaged, compared to 15-38% before and 33% after, perfectly correlated with the temperature (the actual analysis was deeper; I’m just summarising here). The diversity of the insects also increased, as evidenced by the different types of damage. I’m only writing this so that I have an excuse to relentlessly mock failing global warming-denialing farmers in the future: all the warning signs were there, you ignorant dolt.

The basic point is that plant-insect interactions are very practical indicators of how active ecosystems were during different periods of Earth’s history – we can trace them back to the very first complete terrestrial ecosystems in the Devonian (~400 Ma) – and even earlier to the Early Silurian, in the form of plant matter in coprolites (fossilised shit). The first complete terrestrial ecosystems were necessarily simple, with an emphasis on detritivores rather than herbivores and carnivores, even though stem mining and feeding from primitive mites and collembolans is known from the Early Devonian (no leaves yet ;) ). Arthropod herbivory was at an all-time low in the Middle Devonian, most probably due to low levels of oxygen – herbivory is a metabolically costly way of feeding and necessitates efficient respiratory systems to excrete the CO2 produced; it wasn’t until the mid-Mississipian (Early Carboniferous) until we get proper traces of herbivory in the fossil record with the first records of folivory (feeding on foliage, i.e. leaves) on seed-ferns, a paraphyletic group of ecologically dominant plants of the period (they formed shrubs, vines, trees, so lots of opportunity for specialisation – which subsequently took place concretely in the Pennsylvanian (Middle Carboniferous)).

Of course, later on in the Permian, ecosystems globally collapsed during the Permian mass extinction. The aftermath of that event was the radiation of other, partially new, groups of plants and insects. This was the time when completely modern ecosystems evolved: in terms of feeding types, nothing new has evolved since then, so this was a critical turning point in the history of life on Earth – and we can uncover it simply by looking at these traces of insect damage on leaves.

Another thing that can obviously be investigated is the evolutionary pattern of plant-insect coradiations. There are three patterns (that are not mutually exclusive) that may be observed: there are cases where the host plants radiate, followed by the radiation of their associated insects (a cospeciation that can be very easily detected by phylogenetics); there is the ‘fast colonisation hypothesis’, which states that the plants will radiate not due to coevolution, but because of some other factor, in which case the insect radiation will take place later; the third, ‘delayed colonisation hypothesis’, states that the insect coevolution happens after some evolutionary novelty by the plant or the insect (in the latter case, most probably a host shift) and so there will be a noticeable lag between the plant radiation and the insect radiation.

For example, if we look at the fossil record of the phytophagous beetles, we notice two radiative bursts that led to their great diversity today: one at 90 Ma, in association with the radiation of the angiosperms and later, the relative lack of competition after the K-T event, and another burst during the Cenozoic, ~10 Ma, related to changes in host plants due to climate change. The first case is a cospeciation, but also has aspects of the fast colonisation hypothesis, while the latter case fits with the delayed colonisation hypothesis as the beetles had to change their host plants, or even the tissue which they feed on (a change from leaf- to stem-mining, for example).

Picture Sources

• Currano, E. D., Wilf, P., Wing, S. L., Labandeira, C. C., Lovelock, E. C. & Royer D. L. 2008. Sharply increased insect herbivory during the Paleocene-Eocene Thermal Maximum. PNAS 105, 1960-1964.
• Labandeira, C. C. 1998. Early history of arthropod and vascular plant associations. Annual Review of Earth and Planetary Sciences 26, 329-377.
• Labandeira, C. C., Johnson, K. R. & Wilf, P. 2002. Impact of the terminal Cretaceous event on plant-insect associations. PNAS 99, 2061-2066.
• Stone, G. N., van der Ham, R. W. J. M. & Brewer, J. G. 2008. Fossil oak galls preserve ancient multitrophic interactions. Proceedings of the Royal Society B 275, 2213-2219.
• Wappler, T., Currano, E. D., Wilf, P., Rust, J. & Labandeira, C. C. 2009. No post-Cretaceous ecosystem depression in European forests? Rich insect-feeding damage on diverse middle Palaeocene plants, Menat, France. Proceedings of the Royal Society B 276, 4271-4277.
• Winkler, I. S., Labandeira, C. C., Wappler, T. & Wilf, P. 2010. Distinguishing Agromyzidae (Diptera) leaf mines in the fossil record: new taxa from the Paleogene of North America and Germany and their evolutionary implication. Journal of Paleontology 84, 935-954.

Research Blogging necessities :)
Wappler, T., Currano, E., Wilf, P., Rust, J., & Labandeira, C. (2009). No post-Cretaceous ecosystem depression in European forests? Rich insect-feeding damage on diverse middle Palaeocene plants, Menat, France Proceedings of the Royal Society B: Biological Sciences, 276 (1677), 4271-4277 DOI: 10.1098/rspb.2009.1255
Currano, E., Wilf, P., Wing, S., Labandeira, C., Lovelock, E., & Royer, D. (2008). From the Cover: Sharply increased insect herbivory during the Paleocene-Eocene Thermal Maximum Proceedings of the National Academy of Sciences, 105 (6), 1960-1964 DOI: 10.1073/pnas.0708646105

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