Thursday, December 29, 2016

Tales Written in Leaves, Part II ~ Reading Insect Damage

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.

I would classify this leaf mining as the Guide’s DT43; the brief version of the Guide’s description reads:  “Short, serpentine, with linear margin; solid frass; expanding width.”  It should be remembered that any of these descriptions applies to the appearance of a DT in a fossil leaf compression.  (Frass is insect larvae excrement.)  DT43 is shown below.

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.]

I will close on a somewhat ironic note.  Though I think I’ve matched some of the present-day examples of insect damage to specific DTs in the Guide, I’m stumped by the damage highlighted in the fossil leaf at the beginning of this essay.  Which DT is it?

Saturday, December 10, 2016

Tales Written in Leaves, Part I ~ Blaming the Bolide

In which the blogger confirms, yet again, the dangers of assuming he knows something.
The process has nearly run its course, though oaks and beeches are holding on,  During November and very early December in this area of the northeastern U.S., deciduous trees let go of their leaves in numbers beyond imagination (well, my imagination, at least).  Given that such trees dominate many forests here, it’s not surprising that we were blanketed in leaves.  Metallic growls disturbed daylight hours as folks with leaf blowers tried to corral the fallen leaves, saving the users’ backs while sacrificing their hearing.  Being old school, I chose to sacrifice my back.

While creating my own piles of leaves, dragging a dog through the mounds of leaves that decorated curbsides, or traipsing through nearby woods, I puzzled over this question:  Why am I surrounded by deciduous trees?

A couple of weeks ago, in an instance of serendipity, as I sorted through a stack of recent Natural History magazines, I happened upon a brief review from 2014 of a research article apparently on just that question.  Science writer Ashley Braun posited that this research showed that the impact of the extinction event at the end of the Cretaceous period selected for deciduous plants with their faster growth and disposable leaves.  (Reading Tree Leaves, Natural History, November 2014.)

I wondered whether it was fair to blame the seemingly never-ending cascade of leaves here principally on the Chicxulub bolide that burned through the atmosphere about 65 million years ago and smashed into the shoreline of the Yucatan.  (For many of the writers I’m currently reading, bolide seems to be the term of art for this extraterrestrial object, be it asteroid, comet, what have you.)  The atmospheric consequences of this impact (including an impact winter) are widely believed to have brought the Cretaceous period to an end, causing the extinction of many, many groups of terrestrial and marine organisms, including non-avian dinosaurs.  In North America, over half of all plant species were extinguished.  I was suspicious of this assignment of responsibility, believing, as I do, that the workings of natural history are, more often than not, complex tales of myriad interplaying factors.  Blaming the bolide seemed too simple.

Cretaceous flora included gymnosperms (producers of “naked seeds,” including conifers) which, depending upon whom you read, either were dominant throughout this period or had already been shouldered aside before the bolide impact by the recently appearing angiosperms (flowering plants producing “seeds within a vessel,” including sycamores).  It's mostly (though not exclusively) angiosperms that are deciduous and so the sources today of these myriad throw-away leaves.  And, it should be noted, many angiosperms are also evergreen.

In the article Braun described, Plant Ecological Strategies Shift Across the Cretaceous-Paleogene Boundary (PLoS Biology, Volume 12, Issue 9, September 2014), ecologist Benjamin Blonder and his colleagues focused on fossil angiosperm leaves from two formations in North Dakota – Hell Creek (Upper Cretaceous period) and Fort Union (Lower Paleocene epoch).  By doing so, Blonder keyed in on a slightly more than 2-million-year period that straddles the End Cretaceous event.

To get a very general sense of the kinds of fossils he and his colleagues worked with, I have included a few pictures of material from both of those formations.  The first pictures below show leaves that are part of a slab of matrix from the Hell Creek Formation that is currently on display in the Last American Dinosaurs exhibit at the Smithsonian’s National Museum of Natural History.

The next image shows a single leaf which was found in an outcropping of the Fort Union Formation in Montana.  It comes from my fossil collection.

At the outset of his article, Blonder noted that he was generating quantitative evidence relevant to a qualitative analysis from 1987 by paleobotantist Jack A. Wolfe about the appearance of the deciduous trait in plants across the boundary at the end of the Cretaceous.  It’s helpful to see what Wolfe outlined nearly three decades earlier (Late Cretaceous-Cenozoic History of Deciduousness and the Terminal Cretaceous Event, Paleobiology, Volume 13, Number 3, 1987).  Broad-leaved deciduous plants, Wolfe posited, evolved the deciduous trait to cope with climates that included “periods unfavorable to growth.”  It made evolutionary sense in those situations to speed up the production of leaves, disposable ones at that, emerging quickly to capture sunlight and dropping away before needing to be protected from freezing temperatures.

The global climate from the Late Cretaceous through the Eocene was, Wolfe described it, “generally warm and equable,” a climate that should not have favored deciduous plants.  Not unexpectedly, in the Late Cretaceous, “broad-leaved deciduous plants were of low diversity,” but a change in the composition of the flora marked the epochs (Paleocene and Eocene) immediately following the Cretaceous.  By the Paleocene, the Northern Hemisphere featured a “high diversity of broad-leaved deciduous plants . . . .”  Something or some things, he concluded had selected for the deciduous habit in Northern Hemisphere vegetation between the Cretaceous and Paleocene.  Wolfe suggested the “change resulted from a brief low-temperature excursion, probably an ‘impact winter.’”

Enter Blonder.  He analyzed changes in two key leaf variables during this narrow time period – leaf mass per area and minor vein density.  The first gauges plants’ investment in leaf construction (mass per area); the second relates to the transportation of water and carbon (vein density).  Variations in these investments fall across a spectrum from evergreen, “slow-return” leaves that are long lived with significant carbon tissue (relatively high mass per area and low vein density) to deciduous, “high-return" leaves that are shorter lived with less carbon tissue (relatively low mass per area and high vein density).

With results supporting Wolfe's analysis, Blonder found that, across the end-of-the-Cretaceous boundary, leaf mass per area fell while minor vein density rose.  The decline in leaf mass per area apparently resulted from the extinction of species abundant during the Cretaceous with high leaf mass per area; the rise in vein density across the boundary was affected primarily by the loss of species with low vein density.  In other words, overall changes were in the direction of increasing deciduousness.  In the impact and immediate post-impact period, fast growing plants were favored as deciduous species were selected for while evergreen species were selected against.  Rapid growth with disposable leaves was apparently the ticket to deal with this unstable environment.  Blonder has observed,
This tells us that the extinction was not random, and the way in which a plant acquires resources predicts how it can respond to a major disturbance. And potentially this also tells us why we find that modern forests are generally deciduous and not evergreen.  (As quoted by Daniel Stolte in Meteorite That Doomed Dinosaurs Remade Forests, University of Arizona, UA News, September 16, 2014.)
So, I guess that's where I end up in this post, where I started.  Though none of this suggests how challenging I found this whole exercise.  I became mired in the debate within the scientific community over whether angiosperms dominated Cretaceous flora or, instead, were widespread but marginalized.  Compounding my frustration was that it took me  much too long to realize that I was essentially equating angiosperm with deciduousness which made the conflicting positions on angiosperm dominance all the more confusing.

In closing, I hesitate to note that there’s some dissent (of course there is) from the position that angiosperms hold sway today.  See, for example, Timothy J. Brodribb et al., Elegance Versus Speed:  Examining the Competition Between Conifer and Angiosperm Trees (International Journal of Plant Sciences, Volume 173, Number 6, July/August 2012).  But I won't get into it.

[In a second post, tentatively titled Tales Written in Leaves, Part II ~ The Damage Done, I will turn to the stories that can be read on leaves about the travails of the summer just past, or of summers gone by millions of years ago.]

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