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In a globally warming world, insects act locally to manipulate their own microclimate
Thursday, 2019/03/28 | 07:36:06
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Michael Kaspari PNAS March 19, 2019 116 (12) 5220-5222
A key challenge, as CO2 accumulates and Earth warms, is to predict the responses of ecological systems—the suite of interacting populations embedded in the abiotic arena of temperature, moisture, and biogeochemistry. Thermal performance theory (1⇓–3) has come to the fore as a powerful approach toward understanding such biotic change. Thermal performance theory posits that a suite of organismal traits like thermal minima, maxima, and optima—all underlain by physiology—translate gradients of an organism’s thermal environment into gradients of its performance. “Performance” in this case is an ecoevolutionary catchall that ultimately translates into reproduction, growth, and, at bare minimum, survival. Thermal performance theory’s underlying logic—one used by global change scientists—is that temperature constrains the abundance and distribution of populations and communities: The abiotic predicts the biotic. Toward developing that understanding, students of thermal performance theory have been keenly aware of the importance of natural history, the diversity of ways that organisms experience temperature. In PNAS, Pincebourde and Casas (4) report how seven arthropod species that feed on leaves in the same French apple orchard engineer widely different microclimates for themselves in the process. By flipping the arrow between abiotic and biotic, the authors show how species do not just occupy their thermal niches, they create them.
It is relatively straightforward to measure the thermal environment of large organisms like lizards, birds, and tortoises (2). In the shade, one measures air temperature; in the sun, one adds the effect of radiant heat. For the first generation of biotic change models, climatologists provided the necessary data on mean air temperature and number of hours of sun from the world’s weather stations. Thus began the early marriage of thermal performance theory and climatology (5).
At the same time, microclimatologists (often agronomists interested in the temperature and humidity experienced by leaves) were documenting fine-scale differences between the temperatures of surfaces and the well-mixed air just millimeters above them (6, 7). These boundary-layer environments existed as a thin film of air, a few millimeters thick, which on windless days could superheat in the sun and supercool in the shade relative to the surrounding air. Boundary-layer environments would exist as an interesting side note save for the fact that a large fraction of Earth’s terrestrial life, including its plants, frequently experience boundary-layer temperatures.
Global change biology has retained a reliance on the well-mixed atmosphere measured by your generic weather station.* Still, much of the thermal ecology of insects makes little sense when weather station temperatures are used as inputs. For example, in a tropical forest, the ants that travel through the boundary layer have upper thermal tolerances of 40 to 57 °C, far in excess of the ecosystem’s warmest air temperatures but approached with regularity on a sunny, still day on forest surfaces (8). Large portions of the tropical canopy occasionally superheat, causing ants to retreat to the shade.
Pincebourde and Casas (4) introduce us to an even more complex challenge for thermal performance theory and, hence, global change biology: the phyllosphere—the sum total of the leaf surfaces found in a given ecosystem. The phyllosphere is unique and deserving of attention. First, it is very big, far exceeding the surface of terrestrial Earth in most ecosystems: There may be 4 ha of corn phyllosphere for every hectare of cornfield, and double that for a managed tree plantation (9). Which is also to say that the phyllosphere is edible and supports the largest group of terrestrial animals, the herbivores. Moreover, unlike the relatively inert branch that an ant traverses, leaves actively thermoregulate (10). A key way is via transpiration, when leaf hydraulics open stomata, releasing water and promoting evaporative cooling. As a thermal environment, the phyllosphere is very much alive.
Pincebourde and Casas (4) explore the thermal ecology of some of the most abundant animals of the phyllosphere—the small herds of aphids and spider mites that colonize and exploit the leaves of apple trees. These arthropods are functional parasites, obtaining food and shelter from their host without typically killing it. They are also relatively immobile, affixing themselves to leaves by plunging into leaves, digging into the epidermis, or tunneling through the mesophyll. These parasites thus experience, over hours and days, their host’s range of temperatures from their particular spot on the leaf. This sets up the potential conflict between a leaf’s chosen temperature and that of their parasites. And as parasites so often do (11), some of these arthropods manipulate their host.
The authors begin with quantifying upper thermal limits. Each species is run through a course of temperatures in a controlled laboratory setting (sitting on a plucked leaf at 100% humidity). After an hour, the moribund are tallied and, for each species, an LD50 is calculated. The seven arthropods reveal an 8 °C range in upper thermal limit, remarkable given that they appear to occupy the same macroenvironment: apple tree leaves. For perspective, this range for arthropods from a single orchard is close to the range of thermal maxima recorded globally for all of Drosophila, a model taxa in thermal ecology. However, this result is consistent with a growing number of studies that show a large fraction of the global diversity in thermal traits can be found in any given community (8). What generates this diversity?
This is where microclimatology meets parasitology. Pincebourde and Casas (4) demonstrate that the different feeding methods of the apple tree’s parasites have direct consequences for the host plant’s hydraulics. Rosy apple aphids, for example, tend to colonize new succulent leaves, slip a stylet into a phloem vessel, and drink the solution, extracting compounds and secreting sugary honeydew. Aphids actually enhance the photosynthesis rate of leaves beyond that of control leaves—in a similar way, perhaps, to the manner in which anticoagulants in mosquito saliva force its host to part with its blood supply. And all that excreted excess water enhances transpiration by nearly 200% over controls, significantly cooling the leaves to temperatures below those of uninfested leaves. It should come as no surprise that this aphid has the lowest thermal tolerance (around 37 °C). The aphid modifies its host environment to better suit its own upper thermal limit.
See more: https://www.pnas.org/content/116/12/5220 |
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