Outside I look lived-in
Like the bones in a shrine.
~ Jeff Tweedy in the Wilco song One Sunday Morning (Song for Jane Smiley’s Boyfriend)
[This is the second of a two-part post on leaves. The first dealt with deciduousness and where I might place the blame for having to spend many Fall hours raking leaves.]
Fossils are time travelers, dancing past those temporal constraints that bind the living. Connecting past, present, and future, they often carry insights (sometimes profound) into events of deep time which can, perhaps, elucidate what is transpiring today and what may happen in the future. All of this is contingent on us being smart enough to read and understand their messages.
My current obsession with leaves has exposed me to what I find to be a striking example of how intimate the interplay in fossils among past, present, and future can be. Case in point is paleontological work on the insect damage appearing on fossil leaf compressions. The beauty of such compressions is that they record an ancient interaction of then-living organisms, offering an opportunity to explore that once dynamic relationship. As paleobotanist Peter Wilf has written, "Plant fossils, uniquely in the fossil record, present abundant and diverse information about at least two, and sometimes more (when there is evidence of predation) levels of a food web.” (Insect-Damaged Fossil Leaves Record Food Web Response to Ancient Climate Change and Extinction, New Phytologist, volume 178, 2008.)
For example, the Paleocene fossil leaf from the Fort Union formation, which appeared in Part I of this post (previously published), exhibits several areas with insect damage. The full fossil is shown below on the left with one area of damage marked; that same marked area is shown magnified on the right.
There is much to learn from such fossilized traces of past activity. Consider, for example, the recent study which concluded that not only had animals and plants of the southern latitudes experienced widespread extinctions at the end of the Cretaceous Period (66 million years ago) as did their counterparts in northern latitudes, but that the southern biotas recovered more rapidly. The basis for these findings? Insect damage to leaves.
Geosciences doctoral student Michael P. Donovan and his colleagues compared (1) the diversity of insect damage in fossil leaves recovered from sites in North Dakota that straddle the end-Cretaceous, to (2) the diversity of damage on fossil leaves from sites in Patagonia, Argentina, covering a similar time period. (Rapid Recovery of Patagonian Plant-Insect Associations After the End-Cretaceous Extinction, Nature Ecology & Evolution, Volume 1, 2016.)
To measure insect damage diversity, Donovan et al. identified instances of “damage type” occurring in the fossil leaves using the Guide to Insect (and Other) Damage Types on Compressed Plant Fossils (Conrad C. Labandeira et al., Version 3.0, Spring, 2007 – I refer to this subsequently as the Guide). The current published version of the Guide identifies 150 distinct damage types (DTs) falling primarily into these categories: hole feeding, margin feeding, skeletonization, surface feeding, piercing and sucking, oviposition, mining, and galling. (More on some of these categories later.) Paleoentomologist Labandeira and his colleagues note that each DT “is defined by a diagnostic suite of characters and is unambiguously separated from the other DTs.”
I will return to the Guide in a bit (it’s really quite a special work), but, first, it’s important to consider a premise upon which Donovan’s analysis rested: that the diversity of insect damage is positively related to the diversity of the insects inflicting that damage. This is a great example of a fossil-mediated intersection of past and present. In assessing the impact of environmental change in the past, paleontologists have used the degree of insect damage diversity found in fossils from specific sites as a proxy for the richness of the diversity of insects that were present at the same time at those same sites. Using traces of insect activity as a gauge of the mixture of insects active at a site in deep time is a function of necessity. As Labandeira has noted elsewhere, plant fossils with evidence of insect activity are much more prevalent in the fossil record than insect body parts (Assessing the Fossil Record of Plant-Insect Associations: Ichnodata Versus Body-Fossil Data, SEPM Special Publication No. 88, 2007).
Were it to be shown that, in reality, the diversity of insect damage types in fossils from particular locations bore little or no relationship to the diversity of insects there, then various findings regarding past impact of climate change on flora and fauna would be called into question. But, in an instance of research on the past driving research in the present (of benefit to different groups of researchers), botanist Mónica R. Carvalho and her colleagues tested that specific premise by analyzing present-day forests (Insect Leaf-Chewing Damage Tracks Herbivore Richness in Modern and Ancient Forests, PLOS ONE, Volume 9, Issue 5, May, 2014). As she noted, “Here, for the first time, we test directly for a quantitative relationship between the numbers of leaf-chewing insect species and the DT richness induced by the same sampled insects under observation, among single host-plant species.”
Using cranes in two tropical rain forest sites in Panama, they collected insects from the canopies of dominant angiosperms along with data on external damage types on canopy leaves. Their findings: insect species richness and damage type richness are, indeed, very strongly correlated. “Insect-feeding damage, especially with specialized damage included, is likely to be a robust indicator of relative changes in herbivore diversity and composition in fossil and, of great potential importance, in living forest.” Ah, things seem to work both ways - a tool used by paleontologists to gauge the impact of climate and other environmental changes in the past might have significant applications for tracking biodiversity changes today with clear implications for the future.
I would note that Carvalho used the Guide to quantify the leaf-chewing damage diversity she found in leaves collected in the rainforest canopies. Yes, she was testing a paleontological hypothesis and, so, I guess, it made sense to apply the same quantifiable measures, based on the Guide, to contemporary leaves. Is there a counterpart to the Guide that might be applied to evidence of insect damage found in living or recently fallen leaves? Turns out there isn’t. There are works that describe the traces of insect activity that one might find on today’s plants (a good one is discussed below), but the categorization of damage types that is the Guide’s seminal strength, allowing for quantitative analysis, is apparently unique to it.
Similarly, when biologist Jonathan M. Adams and his colleagues sought to assess in today's forests the validity of conclusions from paleontological studies that the diversity of insect damage types in leaves increased as temperatures increased (as measured through various proxies), they used the Guide (Present-Day Testing of a Paleoecological Pattern: Is There Really a Latitudinal Difference in Leaf-Feeding Insect-Damage Diversity?, Review of Palaeobotany and Palynology, Volume 162, 2010). As they noted, “The damage type system [as delineated in the Guide] was developed entirely from fossil examples because there is no similarly detailed classification in standard ecological and entomological literature” (emphasis added). From their research, they concluded that, by and large, the paleontological pattern generally held for contemporary forests, a finding with potential implications for today’s warming world: “It appears possible that with warming, ecologists, foresters and farmers will observe a greater range of types of insect attacks on plants.”
In a very limited and rather idiosyncratic way, I've done a little of my own marrying of the past (fossils) with the present, as I've explored some of the insect damage done to the leaves that cascaded down around me this past Fall. It's mostly been just an exercise in finding examples of insect damage. As I describe below, I've been using a handbook to explore some of the background for traces left by insects and other invertebrates on leaves today, But, I also wondered how difficult it would be to use the fossil-based Guide to match its DTs to some of the instances of damage I've found, as Carvalho and Adams did. No, I'm not engaged in any quantitative analysis, the kind of research for which the Guide was developed, nevertheless it seemed an interesting exercise. Turns out I may have been able, in some limited way, to actually apply its precise descriptions and depictions of the kinds of damage insects did to damage they still do.
Initially, I was drawn to this whole effort by the following lines in a flyer I came upon from a local group that works to protect a nearby creek:
This time of year, on each “imperfect” leaf, we see the signatures left by critters who drank or ate, or who sheltered between the very surfaces of the leaf, or who stashed their unborn against the day. Innumerable and often unknown, these small critters are each one part of the whole – eating and being eaten, living and dying . . . (Laura Mol, The Eco-Contemplative Opportunity of Imperfect Leaves, a flyer issued by Friends of Sligo Creek, October 20, 2016.)At Laura Mol’s suggestion, I began my exploration of insect damage to present-day leaves with Tracks & Sign of Insects and Other Invertebrates: A Guide to North American Species (2010) by naturalists Charley Eiseman and Noah Charney. It’s a picture-rich introduction to the broad sweep of traces of insects (and other invertebrates) one might happen upon. For leaves, in particular, it does a wonderful job of describing and showing myriad, often horrifying, modes of chewing, puncturing, egg laying, sucking, infesting, and otherwise abusing leaves. I have to keep reminding myself that insects are in pursuit of their own good cause, the propagation of their species.
The damage insects do may be restricted primarily to the interior of the leaf (endophytic damage) or may involve all layers of the leaf. From a number of leaves that I collected during the downpour of leaves of several weeks past, I found some nice examples of both kinds of leaf damage and show some of them below. Most of these involve oak leaves because those are the trees that are most at hand. My discussion of the possible origins of these different examples of insect damage is based largely on the Tracks & Sign handbook. When I think I might have found a DT in the Guide that applies to the example in question, I provide the image of a fossil leaf compression from the Guide showing that DT. (In a personal communication, Dr. Labandeira indicated that the Guide is in the public domain.)
I was particularly pleased to come upon a leaf from a Tulip tree (Liriodendron tulipifera) featuring the circuitous path tunneled out by a leaf miner. This is the only example below that doesn't come from an oak. This kind of tree is often called a Tulip Poplar around here, but it’s not a close relative of true Poplars.
I find leaf mining particularly interesting, so will indulge myself and consider it somewhat at length. In leaf mining, a principal example of interior damage, insect larvae spend their time until maturity sheltered between two epidermal layers, eating the tissue they find there. These leaf miners are typically the larvae of moths and flies. Identification is aided immeasurably by that fact that, in many cases, different taxa of leaf miners create distinctive tunnels and specialize in particular kinds of trees. Some mines remain narrow throughout their course, others start linear and end in blotches (broad areas in which the tissue is consumed), still others create mostly blotchy mines, sometimes with digit-like extensions. Often fecal pellets line some portions of these mines. Overall, the coupling of mine patterns and the host plant can be diagnostic of the insect behind the damage.
A portion of the mine in the Tulip tree leaf is shown below. Given the specific tree host and the linear nature of the mine, this might be the work of a larva of the moth Phyllocnistis liriodendronella.
Galls are another example of what is endophytic damage despite sometimes being very visible on the leaf surface. Leaf galls are generated when leaves react to various kinds of foreign organisms including insect eggs. Most apparently are prompted by mites and insects, particularly gall wasps or cynipids. Here is a small section of a Pin Oak leaf (Quercus palustris) with several prominent galls.
I will hazard a guess that this is an example of DT80 (shown below), described in the Guide as follows: “Small, hemispherical; thoroughly carbonized; diameters ~ 0.1 – 1.0 mm; 1˚ and 2˚ veins avoided.” Are the galls in the Pin Oak leaf above avoiding those veins?
I’m not certain whether skeletonizing damage should be considered endophytic since there are various definitions of what constitutes the phenomenon. In the one I've followed here, skeletonization need not go through all of the leaf layers. Some insects or insect larvae skeletonize a leaf by consuming one side, leaving the vein network and the outermost layer of the leaf intact. As a result, the skeletonized portions of such leaves, covered with the thin remaining layer, can be stunningly translucent when seen in just the right light or under magnification.
I was quite please with the pictures below which show a small skeletonized section of a leaf from a Northern Red Oak (Quercus rubra). Each image is magnified 10 times: the one on the left shows a portion of the skeletonized upper surface of the leaf – the mostly still complete outermost layer is evident; the one on the right is roughly this same area viewed from the underside, the veins stand out in stark relief, not covered at all and seemingly undamaged. Clearly, the skeletonizing organism did its thing on the underside.
I’m uncertain about the DT applicable to this damage, but it may be DT16 (shown below): “Interveinal tissue removed; reaction rim poorly developed.” (Reaction rim is, I think, the margin around the damage and reflective of how vigorously the plant responded to the damage.)
Insects may puncture holes in leaves for many different reasons and in myriad configurations. That the pattern of holes in this White Oak leaf (Quercus alba) is roughly circular may be a good clue as to the culprit, but neither of my references seem to be of much help. [Later edit: I should clarify that both sources provide many examples of insect damage involving holes, just no examples with the a pattern similar to that shown below.]