The buzz on trophic cascades

May 11, 2023 by fredsingerecology

Herbivores, by their nature, damage plants in natural ecosystems and in agricultural systems. And predators, by their nature, do a lot of damage to herbivores, either by eating them, or by harassing them in ways that cause them to change their behavior, or in some cases change their morphology or physiology (these are called nonconsumptive effects). The indirect effect of a trophic cascade in which predators damage herbivores which damage plants, is that predators can benefit plants by their detrimental effect on herbivores.

Much of the research on nonconsumptive effects has focused on aquatic systems because the predator cues are easy to manipulate in the laboratory. Simply let a predator hang out in a water tank for a while, and then add the predator tank water to a tank with a possible prey item, and study the prey’s response. But there has been little work on nonconsumptive effects in terrestrial systems. While there has been some research on how auditory cues emitted by terrestrial predators affect vertebrate herbivores, there has been almost no work on how auditory cues affect invertebrate herbivores. This is surprising, because invertebrates cause enormous damage to agricultural systems. Evan Preisser and his students wondered whether the beet armyworm caterpillar, Spodoptera exigua, a voracious herbivore on many commercially important crops, responded to buzzing emitted by an important predator, the caterpillar-hunting paper wasp (Mischocyttarus sp.). More important, they tested whether the response was substantial enough to have an impact on caterpillar mortality, and subsequent plant development.

Four *Spodoptera* caterpillars chomp on a soybean leaf. Credit: Michasia Dowdy, University of Georgia, Bugwood.org

Perhaps the biggest challenge was technical. The researchers needed to come up with a mechanism for delivering an auditory cue to one group of caterpillars that would not be detected by any other nearby group. They tried various conformations, including separating the cages with soundproofing foam, which, unfortunately, was not soundproof to wasp buzzes.

One of the failed attempts at auditory isolation. Unfortunately, the auditory stimulus was detectable up to two boxes away from the source. Credit: Zachary Lee.

Nothing worked until one of the students suggested using boxes that dry ice was shipped in, reasoning correctly that it should have good insulating properties. The decibel meter failed to detect any sound from adjacent boxes.

Having solved the soundproofing problem, the researchers raised 36 groups of five caterpillars in small cups filled with 25 grams of caterpillar diet. Each cup was placed in a box and subjected to one of three treatments: no-sound control, recorded buzzing of a non-predatory mosquito, or recorded buzzing of a predatory wasp. The volume was the same for both sound treatments. Each tape went for 12 hours per day, with 2 seconds on, followed by 6 seconds off. The researchers found that survival was substantially lower for caterpillars that received the wasp treatment (top graph below). Also, caterpillars that survived the wasp treatment took, on average, longer to develop (bottom graph below), though that difference was not statistically significant.

Survival (top graph ), weight (middle) and time to pupation (bottom) of *Spodoptera* caterpillars subjected to no sound (green bar), mosquito buzz (yellow) and wasp buzz (red). Different letters above bars indicated statistically significant differences between treatments.

Preisser’s graduate student, Zachary Lee, took the lead in organizing the field experiment. The researchers wanted to know whether the negative effect of wasp buzzes that they detected in the laboratory had real consequences for agricultural systems. They surrounded each tomato plant (72 in all) with a mesh bag (to keep the caterpillars in and other insects out), and placed an average of 96 newborn caterpillars on each plant. Each group of four plants surrounded a speaker that emitted either no sound (control), mosquito buzzing, or wasp buzzing, which were broadcast at levels that caterpillars would experience when an insect was 5 cm away from them. Each sound was played in a loop of 1 minute on, followed by 10 minutes off, for 12 hours per day. Lee and his colleagues let the experiment run for 3 weeks, by which time all caterpillars had either pupated or died. They harvested each plant, and calculated the percentage of leaves that were damaged by caterpillars. Then they dried each plant, including the roots, and weighed them.

Field experiment with four tomato plants positioned equidistant from one central speaker. Each group of four received one of the experimental treatments. Credit: Zachary Lee.

Plant leaves associated with wasp buzzing received the least damage, leaves on control plants received the most damage, and leaves on plants with mosquito buzzing received intermediate damage. Aboveground mass was greater in wasp treated plants than in controls, so the sound of wasp buzzing helps to protect the tomato plants against voracious caterpillar herbivores.

Indirect effects of no sound (green bar), mosquito buzz (yellow) and wasp buzz (red) on tomato plants, via the effects of these treatments on *Spodoptera* herbivory. Different letters above bars indicated statistically significant differences between treatments.

The researchers did not study caterpillar behavioral changes because these caterpillars are easily disturbed, either freezing or dropping off of plants when approached. Lee and his colleagues point out that we know very little about how invertebrates, in general, respond to sound cues, as their survey of the literature on prey response to sound cues showed that 181/183 experiments used vertebrate prey. Given how widespread invertebrates are in agricultural systems, and in ecosystems in general, we need more studies to get a better handle on how invertebrates respond to sound, and most important, how their response influences agricultural systems and ecosystem structure and functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Lee, Z.A., Cohen, C.B., Baranowski, A.K., Berry, K.N., McGuire, M.R., Pelletier, T.S., Peck, B.P., Blundell, J.J. and Preisser, E.L., 2023. Auditory predator cues decrease herbivore survival and plant damage. Ecology, p.e4007. https://doi.org/10.1002/ecy.4007. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.

Ants and acacias: friends, foes or frenemies?

February 8, 2023 by fredsingerecology

In his massive elegy, “In Memorium A. H. H.”, Alfred, Lord Tennyson laments the death of his friend, Arthur Henry Hallam, at 22 years old. Tennyson writes,

“Who trusted God was love indeed

And love Creation’s final law

Tho’ Nature, red in tooth and claw

With ravine, shriek’d against his creed”

Thus Tennyson accuses the natural world of being rife with strife and violence.

It would be wrong to dispute Tennyson’s complaint outright, but ecologists can present mutualisms, interactions in which both species benefit, as a counterpoint to his argument. One of the best studied is the ant/acacia tree mutualism, in which acacia trees provide food and living accommodations to ants, which protect their home tree against herbivores, including immense creatures such as elephants and giraffes! Previous research had shown that acacias usually grew better if they harbored a colony of protective ants, even though they were providing the ants with costly resources. These resources included swollen thorns (domatia) which ants may use as homes or fungal gardens, and specialized structures (nectaries) which provide ants with sugar.

Swollen thorns (domatia) on an *Acacia drepanolobium* tree that is hosting ***Crematogaster nigriceps*** ants. Credit: Patrick Milligan.

As an undergraduate at the University of Florida, Patrick Mulligan learned about how ecology could be thought of as the study of the economy of nature. Keeping with the economic metaphor, Mulligan recognized that the tiny ants and relatively large trees trade in the same currency: carbon. He realized that tree growth is simply a measure of how much carbon a tree has to spend on itself. So he asked if ants might be influencing how much carbon is available for both themselves and the tree.

*Acacia drepanolobium*, the dominant tree in the savanna. Credit Patrick Milligan.

In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host plants, the dominant woody plant in the savanna (see photo above). These ants differ in several traits including how much protection they actually provide, whether they consume tree-produced nectar, how they modify the tree, and how they influence a tree’s water relations (see photo and table below). If a tree can’t get enough water, it is forced to close the stomata on its leaf surface to reduce water loss from transpiration. When stomata are closed, carbon dioxide import is drastically curtailed, and photosynthetic rates (and carbon production) are reduced.

The four ants species studied by Patrick Milligan and his colleagues are *Crematogaster sjostedti*, *C, mimosae*, *C. nigriceps* and *Tetraponera penzigi*. Credit: Todd Palmer.

To determine how the four ant species influence carbon fixation and water relations in these acacias, Milligan and his colleagues set up a five-year ant-removal experiment between 2013-2018. They found 48 matched pairs of trees that harbored each ant species (12 pairs of trees per ant species), and then removed all of the ants from one of the two trees by fogging with a short-lived insecticide. The researchers restricted ant recolonization by applying to the base of each tree an annoyingly sticky substance that ants generally avoid.

After five years (in 2018), Milligan and his colleagues measured photosynthesis and transpiration rates in leaves of each tree, using tools that were specialized for those purposes. They then extrapolated from these leaf measurements to photosynthetic and water exchange rates for the entire tree crown (where most of the action is). They discovered that trees with C. mimosae (Cm) and T. penzigi (Tp) had substantially higher photosynthetic rates than trees with C. sjostedti(Cs) and C. nigriceps (Cn). But trees that had their ants removed were statistically indistinguishable in their photosynthetic rates (graph (a) below). In other words, removing ants caused Cm and Tp-trees to reduce their photosynthetic rates, and Cs and Cn tree to increase their photosynthetic rates, so they were equivalent after five years of ant removal.

(Graph a) Mean (+SE) photosynthetic rate at the tree crown and (Graph b) transpiration rate at the tree crown for acacia trees with ants present or removed. The letters to the side of each data point indicate when two species have statistically significant differences in their value. For example, in graph a, comparing the case where ants were present, the photosynthetic rates for Cm and Tp are not different from each other, but both are significantly greater than the photosynthetic rates for Cn and Cs. However, Cn and Cs have similar photosynthetic rates.

Looking at the table above, you will note that both Cs and Cn do some major alterations to the trees that might compromise carbon production. Though Tp does remove nectaries, it also consumes no nectar, so that interaction may be a wash. Based on these observations, we might suspect that Cs and Cn are actually tree parasites, while while Cm and Tp are closer to true mutualists that actually benefit the host trees. Supporting this idea, removing Cs sharply increased leaf area and also increased water exchange rate (graph (b) above). And trees that were continuously occupied by Cn also showed reduced leaf area, lower photosynthetic rates (graph a above) and water exchange rates (graph b above) at the tree crown than Cm or Tp. But there is more to the story.

Cn is an aggressive defender against would-be herbivores. However, it also eats large portions of the tree it inhabits focusing on the nectaries (which produce sugars) and the reproductive structures. One puzzling consequence of this behavior is that Cn-occupied trees are significantly better than other ant-occupied trees at bringing up subsurface water, perhaps helping the tree to survive droughts. The researchers plan to measure the root systems of all the trees in hopes of seeing whether Cn-occupation actually alters root development in a way that improves water uptake.

Complicating the story further is a consideration of carbohydrate production. Trees hosting Cs (the stem excavator) had much less starch in their stems than did trees hosting the other species. Starch is an important source of energy for all plants; in fact trees with Cs removed still had low starch levels after five years. Presumably the trees that were freed from hosting Cs prioritized growing new branches, or repairing cavities and defending against beetle infestation, over producing more starch for storage.

Trees occupied by Cm (a nectar consumer) had much higher glucose levels than trees hosting the other three species. Removing Cm caused the glucose levels to drop sharply (see graph below). Trees hosting the other nectar consumer (Cn) did not show this increase in glucose, possibly because Cn prunes the leaves and eats the flowers, leaving the host tree with insufficient nutrients to increase glucose levels.

Mean (+SE) glucose levels in the stems of trees hosting each ant species. Notice the sharp drop in glucose concentration five years after Cm removal.

I asked Patrick Milligan how trees get occupied by a particular ant species. He responded that there are battles for occupancy both between ant species, and sometimes within ant species. An ant from one colony locks in a death grip with an ant from another colony, they then fall from a branch and kill each other on the ground. So the bigger colony wins a battle by virtue of having some surviving ants to colonize the tree. One exception is Cs, which has slightly larger and presumably stronger ants, and will sometimes survive a head-to-head battle. Currently, Milligan and his colleagues are investigating how a tree may adjust its leaf physiology when paired with a new ant species, perhaps by activating different genes in response to the novel species. Though trees cannot choose their ant colonizers, they may be able to adjust to whichever species uses their services.

note: the paper that describes this research is from the journal Ecology. The reference is Milligan, P.D., Martin, T.A., Pringle, E.G., Prior, K.M. and Palmer, T.M., 2023. Symbiotic ant traits produce differential host‐plant carbon and water dynamics in a multi‐species mutualism. Ecology, 104(1), p.e3880. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2023 by the Ecological Society of America. All rights reserved.

Finding fish fluorescently

June 25, 2018 by fredsingerecology

Very early in my teaching career at Carleton College in Minnesota, I was thrust into the position of teaching students about things that I knew very little about. I quickly learned that things went well, so long as I confessed my ignorance – the very bright students at that college were always happy to help me with my education. My ignorance of things biological stemmed from my undergraduate training in psychology, which had only a smattering of biology and chemistry in the coursework. So when we extracted chlorophyll from a plant, shone a bright high-energy (probably UV) light on it, and it glowed a beautiful red, my reaction was “wooo…, that’s cool.” My colleague, who was much more broadly trained, explained that this process, biofluorescence, occurred because the chlorophyll’s electrons were excited by the high energy light, and that they emitted the red light when they returned to a lower-energy state.

Robust ghost pipefish, Solenostomus cyanopterus, is cryptic in ambient daylight (left), but biofluoresces red when lit at night by a high-intensity LED torch (right).

Many threatened or endangered marine species are cryptic, providing challenges to conservation biologists who must assess the abundance of these species. Usually, marine biologists use underwater visual censuses to measure abundance and distribution of marine species, but small or cryptic species are often missed or undercounted. Maarten de Brauwer reasoned that conservation biologists could use biofluorescence as a tool to find small or cryptic marine organisms. He knew from a paper that recently came out in the literature, and from his own experience as a diver, that a number of cryptic species do fluoresce. But how large is that number?

A diver searches for biofluorescent species. Credit: J. A. Hobbs

DeBrauer, working with five other researchers, surveyed reef fish at four locations in Indonesia, as well as two locations outside Indonesia (Christmas Island and the Cocos Islands). Indonesia was a conservation priority as it contains the world’s greatest abundance of marine fish species. Using high-energy LED torches, the researchers surveyed 31 sites at the six locations, assessing each fish they detected for whether it was cryptic or non-cryptic, and whether it fluoresced. Of 95 cryptic species, 83 fluoresced. In contrast, only 12 of 135 non-cryptic species fluoresced.

Number of cryptic and non-cryptic species showing biofluorescence in the survey.

Why are cryptic species more likely to biofluoresce? As it turns out, we don’t know the answer to this question. De Brauwer suggests that some small species, like gobies and triplefins, may use flourescence, which is particularly well-defined around the head region, as a way of communicating without predator detection. These species fluoresce in red, a very-short-range light, so predators won’t see them unless they are very close. Some species of scorpionfish that live in algae and seagrass also fluoresce red, which allows them to blend in well with the red fluorescence emitted by the algal and seagrass chlorophyll.

Having shown that cryptic species tend to bioflouresce, the next challenge was to see whether bioflourescence surveys worked better than standard underwater visual censuses. First, the researchers focused their efforts on two species of pygmy seahorses (Hippocanpus bargibanti and H. denise) that live on seafans, searching for two minutes, either with or without a flourescence torch. They followed with a similar study on two species of reef fish, the largemouth triplefin (Ucla xenogrammus) and the highfin triplefin (Enneapterygius tutuilae); but this time surveying 20m x 2m transects, either with or without a fluorescence torch.

A diver searches a seafan for pygmy seahorses. Credit: J. A. Hobbs.

Unfortunately, the pygmy seahorses are tiny (as you might suspect from their name) and probably rare, so only 32 H. bargibanti and 7 H. denise were detected. These seahorses fluoresce red primarily in their tail region and green from their eyes.

Two cryptic pygmy seahorses “seen” under ambient light (left, circled in red) and in the underwater biofluorescence census (right).

The numbers of H. denise were too small to include in the analysis. But for the other three species, the bioflourescence surveys detected more individuals than did the underwater visual surveys.

Mean number of individual H. bargibanti (left), U. xenogrammus (center) and E. tutuilae (right) detected with underwater visual surveys (UVC) vs. underwater biofluorescence surveys (UBC).

The researchers discovered that bioflourescence is very common in these cryptic and rare species, which means this technique can be used to assess abundance in species most likely to be overlooked using standard underwater visual surveys. The International Union for the Conservation of Nature, which (among other tasks) is responsible for assessing the extinction risk of species worldwide, has only been able to do so for less than 44% of fish belonging to three large cryptic families of reef fish. Of 2000 species in these three families, 21% are listed as data-deficient because they have been so difficult to survey. This novel approach should help inform conservation biologists about species that are in dire straits, so they can focus conservation efforts in a productive and useful direction.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Brauwer, M., Hobbs, J. A., Ambo‐Rappe, R., Jompa, J., Harvey, E. S. and McIlwain, J. L. (2018), Biofluorescence as a survey tool for cryptic marine species. Conservation Biology, 32: 706-715. doi:10.1111/cobi.13033. You should also check out Dr. De Brauwer’s blog at crittersresearch.com. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. All rights reserved.

Indirect effects of the lionfish invasion

May 28, 2018 by fredsingerecology

I’m old enough to remember when ecological studies of invasive species were uncommon. Early on, there was a debate within the ecological community whether they should be called “invasive” (which conveyed to some people an aggressive image akin to a military invasion) or more dispassionately “exotic” or “introduced.” Lionfish (Pterois volitans), however, fit this more aggressive moniker. Native to the south Pacific and Indian Oceans, lionfish were first sighted in south Florida in 1985, and became established along the east Atlantic coast and Caribbean Islands by the early 2000s. They are active and voracious predators, consuming over 50 different species of prey in their newly-adopted habitat. Many population ecologists study the direct consumptive effects of invasive species such as lionfish. In some cases they find that an invasive species may deplete its prey population to very low levels, and even drive it to extinction.

A lionfish swims in a reef. Credit: Tye Kindinger

But things are not always that simple. Tye Kindinger realized that lionfish (or any predator that feeds on more than one species) could influence prey populations in several different ways. For the present study, Kindinger considered two different prey species – the fairy basslet (Gramma loreto) and the blackcap basslet (Gramma melacara). Both species feed primarily on zooplankton, with larger individuals monopolizing prime feeding locations at the front of reef ledges, while smaller individuals are forced to feed at the back of ledges where plankton are less abundant, and predators are more common. Thus there is intense competition both within and between these two species for food and habitat. Kindinger reasoned that if lionfish depleted one of these competing species more than the other, they could be indirectly benefiting the second species by releasing it from competition.

Fairy basslet (top) and blackcap basslet (bottom). Credit Tye Kindinger.

For her PhD research, Kindinger set up an experiment in which she manipulated both lionfish abundance and the abundance of each basslet species. She created high density and low density lionfish reefs by capturing most of the lionfish from one reef and transferring them to another (a total of three reefs of each density). She manipulated basslet density on each reef by removing either fairy or blackcap basslets from an isolated reef ledge within a particular reef. This experimental design allowed her to separate out the effects of predation by lionfish from the effects of competition between the two basslet species. Most of her results pertained to juveniles, which were about 2 cm long and favored by the lionfish.

KindingerTable

Alex Davis captures and removes basslets beneath a ledge. Credit Tye Kindinger.

Kindinger measured basslet abundance in grams of basslet biomass per m² of ledge area. When lionfish were abundant, juvenile fairy basslet abundance decreased over the eight weeks of the experiment (dashed line) but did not change when lionfish were rare (solid line). In contrast, juvenile blackcap basslet populations remained steady over the course of the study, whether lionfish were abundant or rare. Kindinger concluded that lionfish were eating more fairy basslets.

Abundance of juvenile fairy basslets (left) and blackcap basslets (right) as measured as change in overall biomass. Triangles represent high lionfish reefs and circles are low lionfish reefs.

Competition is intense between the two basslet species, and can affect feeding position and growth rate. Kindinger’s manipulations of lionfish density and basslet density demonstrate that fairy basslet foraging and growth depend primarily on the abundance of their blackcap competitors. When competitor blackcap basslets are common (approach a biomass value of 1.0 on the x-axis on the two graphs below), fairy basslets tend to move towards the back of the ledge, and grow more slowly. This occurs at both high and low lionfish densities.

Change in feeding position (top) and growth rate (bottom) of fairy basslets in relation to competitor (blackcap basslet) abundance (x-axis) and lionfish abundance (triangles = high, circles = low)

In contrast, blackcap basslets had an interactive response to fairy basslet and lionfish abundance. Let’s look first at low lionfish densities (circles in the graphs below). You can see that blackcap basslets tend to move towards the back of the ledge (poor feeding position) at high competitor (fairy basslet) biomass, and also grow very slowly. But when lionfish are common (triangles in the graphs below), blackcap basslets retain a favorable feeding position and grow quickly, even at high fairy basslet abundance.

Change in feeding position (top) and growth rate (bottom) of blackcap basslets in relation to competitor (fairy basslet) abundance (x-axis) and lionfish abundance (triangles = high, circles = low)

By preying primarily on fairy basslets, lionfish are changing the dynamics of competition between the two species. The diagram below nicely summarizes the process. Larger fish of both species forage near the front of the ledge, while smaller fish forage further back. But there is an even distribution of both species. Focusing on juveniles, they are relatively evenly distributed in the rear portion of the ledge (Figure B). When fairy basslets are removed experimentally, the juvenile blackcap basslets move to the front of the rear portion of the ledge, as they are released from competition with fairy basslets (Figure D). Finally, when lionfish are abundant, fairy basslets are eaten more frequently, and juvenile blackcaps benefit from the lack of competition (Figure F)

KindingerFig3

Kindinger was very surprised with the results of this study because she knew the lionfish were generalist predators that eat both basslet species, so she expected lionfish to have similar effects on both prey species. But they didn’t, and she does not know why. Do lionfish prefer to eat fairy basslets due to increased conspicuousness or higher activity levels, or are blackcap basslets better at escaping lionfish predators? Whatever the mechanism, this study highlights that indirect effects of predation by invasive species can influence prey populations in unexpected ways.

note: the paper that describes this research is from the journal Ecology. The reference is Kindinger, T. L. (2018). Invasive predator tips the balance of symmetrical competition between native coral‐reef fishes. Ecology, 99(4), 792-800. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Plant communities bank against drought

May 3, 2018 by fredsingerecology

Many plants shed their young embryos (seeds) into the soil where they may accumulate in a dormant (non-growth) state over years before germinating (resuming growth and development). Ecologists describe this collection of seeds as a seed bank. Marina LaForgia describes how scientists were able to germinate and grow to maturity some 32,000 year old Silene stenophylla seeds that was stashed, probably by an ancient squirrel, in the permafrost! With increased climatic variation predicted by most climate models, she wanted to know how environmental variability might affect germination of particular groups of species within a community. In addition, she and her colleagues recognized that most ecological studies investigate community responses to disturbances by looking at the aboveground species. It stands to reason that we should consider the below-surface seed bank as a window to how a community might respond in the future.

Some seedlings coming up from the seed bank. Credit:Marina LaForgia.

Seed banks can be viewed as a bet-hedging strategy that spreads out germination over several (or many) years to reduce the probability of catastrophic population decline in response to one severe disturbance, such as drought, flood or fire. In some California annual grassland communities, species diversity is dominated by annual forbs – nonwoody flowering plants that are not grasses. Many forbs produce seeds that can lie dormant in the seed banks for several years. Though these forbs are the most diverse group, there are also about 15 species of exotic annual grasses that dominate the landscape in abundance and cover. These grasses dominate because they produce up to 60,000 seeds per m², they grow very quickly, and they build up a layer of thatch that suppresses native forbs. However, seeds from these grasses cannot lie dormant in the seed bank for very long.

Area of field site dominated by Delphinium (purple flower) and Lasthenia (yellow flower). Looking closely you can also see some tall grasses rising. Credit Marina LaForgia.

How is drought affecting these two major components of the plant community? LaForgia and her colleagues answered this question by collecting seeds from a northern California grassland at the University of California McLaughlin Natural Reserve in fall 2012 (beginning of the drought) and fall 2014 (near the end of the drought). They used a 5-cm diameter 10-cm deep cylindrical sampler to collect soil and associated seeds from 80 different plots. The researchers also used these same plots to estimate aboveground-cover, and to identify the aboveground species that were present. The research team germinated and identified more than 11,000 seeds.

Plants germinating in the greenhouse. Credit Marina LaForgia.

The researchers knew from previous work on aboveground vegetation that exotic annual grasses declined very sharply in response to drought. In contrast, the native forbs did relatively well, in part depending on their specific leaf area (SLA) – a measure of relative leaf size, with low SLA plants conserving water more efficiently. It seemed reasonable that these same patterns would be reflected belowground. Recall that most grass seeds are incapable of extended dormancy, while many forbs can remain dormant for several years. Consequently, LaForgia and her colleagues expected that grass abundance in the seed bank would decline more sharply than would forb abundance. In addition, they expected that high SLA forbs would not do as well as low SLA forbs during drought.

The researchers discovered very sharp differences between the two groups over the course of the drought. Exotic annual grasses declined sharply in the seed bank, while native annual forb abundance tripled. Aboveground cover of grasses declined considerably, while aboveground cover of forbs increased modestly. Clearly the exotic grasses were suffering from the drought, while the forbs were doing quite well.

(a) Seed bank abundance of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). (b) Percent cover of grasses (red circles) and forbs (blue triangles) at beginning of drought (2012) and near end of drought (2014). Data are based on samples from 80 plots. Error bars indicate one standard error.

We can see these differences on an individual species basis, with most of the grasses declining modestly or sharply in abundance, while most of the forbs increased.

Mean change in seed bank abundance per species based on 15 exotic grass species and 81 native forb species.

It is not surprising that the grasses do so poorly during the drought. Presumably, less water causes poorer germination, growth, survival and seed production. In addition, because grass seeds have a low capacity for dormancy, grass abundance will tend to decrease in the seed bank very quickly with such a low infusion of new seeds.

But why are the forbs actually doing better with less water available to them? One explanation is that grass abundance and cover declined sharply, causing the forbs to experience reduced competition with grasses that might otherwise inhibit their growth, development and reproductive success. The tripling of native forbs in the seed bank was much greater than the 14% increase in aboveground forb cover. The researchers reason that the drought caused many of the forb seeds to remain dormant, leading to them building up in the seed bank. This was particularly the case for low SLA forbs, which increased much more than did high SLA forbs in the seed bank.

We can understand exotic grass behavior in the context of their place of origin – the Mediterranean basin, which tends to have wet winters. In that environment, natural selection favored individuals that germinated quickly, grew fast and made lots of babies. Since their introduction to California in the mid 1800s, 2014 was the driest year on record. It will be fascinating to see if these exotic grasses can recover when, and if, wetter conditions return. Can we bank on it?

note: the paper that describes this research is from the journal Ecology. The reference is LaForgia, M.L., Spasojevic, M.J., Case, E.J., Latimer, A.M. and Harrison, S.P., 2018. Seed banks of native forbs, but not exotic grasses, increase during extreme drought. Ecology99 (4): 896-903. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Saguaro survival: establishing an icon

April 4, 2018 by fredsingerecology

Having grown up in the New York metropolitan area, my only contact with the saguaro cactus, Carnegiea gigantea, was from several TV westerns, which dubiously placed these mammoth cacti in New Mexico, Texas and Colorado. In fact, the saguaro is limited to the Sonoran Desert of northwestern Mexico, extreme southeast California and southern and central Arizona. You won’t find these cacti further north, because a freeze lasting more than 24 hours kills them. I still remember my first real sighting of these cacti; I was amazed at how distinct they seemed in comparison to the other vegetation, and I delighted in their abundance.

Dense patch of saguaros. Credit: Daniel Winkler

Many others delight in their abundance as well. The flowers, fruits and seeds feed many animals (including humans). They were an important food for the Tohono O’odham and Pima Indians – eaten fresh or converted into numerous products including wine, juice, jam and syrup.

Large saguaro with many fruits emanating from the apex of its branches. Credit: Daniel Winkler

Woodpeckers and flickers excavate nests in the saguaro’s trunk, which are subsequently occupied by other animals such as snakes, arthropods and small mammals.

Saguaro with nest cavity excavated near the top of its trunk. Credit: Daniel Winkler

Daniel Winkler also delighted in the saguaro’s awesomeness. As he describes “I fell in love with answering some basic ecology questions about the saguaro. I was surprised that scientists had been studying this wonderful plant for almost 100 years and there were still many basic questions about the species general biology and ecology that remained unanswered. Thus, I was hooked immediately and became obsessed with saguaro.”

Don Swann - Photo of D. Winkler with young saguaros

Daniel Winkler with young saguaros. Credit: Don Swann

Winkler and his colleagues wanted to know how moisture, temperature and habitat influence the establishment or survival of juvenile saguaro seedlings. Previous research had shown that saguaro height can be used to estimate saguaro age, given knowledge of previous rainfall in a particular area. So buoyed by an army of citizen scientists whom they recruited with the help of social media, student groups from schools and volunteers working at the Saguaro National Park, the research team estimated the age of every saguaro on 36 4-ha plots (1 ha = 10,000 m²).

Going into the study, the researchers knew that rainfall was a very important factor, with saguaros surviving better during wet periods. But they also knew that historically, some areas located near each other showed different establishment trends, thus they suspected that other variables, particularly land use and other landscape factors, might be important. They did their research in two different districts within the park: 21 plots in the Rincon Mountain District (RMD) on the east side of the park, and 15 plots in the Tucson Mountain District (TMD) to the west. They classified each plot as a particular habitat type based on slope, elevation and soil-type. Bajada was low elevation, flat and had gravelly porous soils. Foothills were intermediate elevation and intermediate slope, while sloped habitats had highest elevation, steepest slope, and the coarsest rockiest soils.

Panoramic view of Saguaro National Park showing diversity of habitats. Credit: Daniel Winkler.

Winkler and his colleagues calculated the Palmer Drought Severity Index (PDSI) for the years 1950-2003. The PDSI quantifies the water balance between precipitation and evapotranspiration, taking into account not only rainfall but also other factors such as temperature and cloud cover. The PDSI was estimated by assessing tree ring width for each year in nearby woodlands; wet conditions have wide tree rings (maximum PDSI value = +6), while dry years have narrow tree rings (minimum PDSI value = -6).

The researchers discovered a very strong association between the PDSI and seedling establishment. Low PDSI at the beginning and especially the end of the time frame was associated with low seedling establishment, while high PDSI (particularly in the 1980s was associated with high rates of seedling establishment (top graph below). But other patterns emerged as well. For example, establishment was higher in the TMD during the wettest years, but higher in the RMD during the most recent drought (bottom graph below).

Top. Total number of saguaros (left Y-axis) established per hectare from 1950-2003 in relation to PDSI (dashed line, right Y-axis). Bottom. Total number of saguaros established per hectare in the Tucson Mountain District (TMD – filled bars) and the Rincon Mountain District (RMD – open bars) from 1950-2003 in relation to PDSI (dashed line, right Y-axis).

Saguaro establishment increased in all habitats when conditions were relatively wet (more positive PDSI values). Under drought conditions, slopes had greatest saguaro establishment, while establishment increased more rapidly in foothills (and to a lesser extent in Bajadas) as moisture levels increased.

Model projecting number of saguaros established in the three major habitats in relation to PDSI. Shaded regions are 95% confidence intervals.

The researchers were surprised at how tight the connection was between drought and saguaro establishment. But landscape features are also important. The TMD is warmer and dryer than the nearby RMD, and had substantially lower establishment during the recent drought. The slopes in the RMD are steeper and rockier than sloped areas of the TMD, and may buffer saguaros from drought by capturing water in rock crevices and holding it for longer periods of time so it can be absorbed by saguaro roots. Nurse trees that provide shade to young saguaros may also be more common on the RMD slopes.

Winkler and his colleagues are concerned about the long-term impacts of climate change on saguaro populations, particularly in the drier areas of the TMD. They urge researchers to explore how long-term management of grazing and invasive species influences saguaro establishment across the landscape. They also encourage researchers to gather some very basic data about saguaros, such as how they access water and how human water use patterns influence the water’s availability to this iconic species.

note: the paper that describes this research is from the journal Ecology. The reference is Winkler, D. E., Conver, J. L., Huxman, T. E. and Swann, D. E. (2018), The interaction of drought and habitat explain space–time patterns of establishment in saguaro (Carnegiea gigantea). Ecology 99: 621-631. doi:10.1002/ecy.2124. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Parrotfish put on their big boy pants

March 21, 2018 by fredsingerecology

While it would be awesome if parrotfish were named for their conversational abilities, it turns out that they earn their moniker for their specialized teeth that are fused together for scraping algae from coral, thus resembling a parrot’s beak. Despite lacking verbal skills these fish are incredible. Approximately 100 species occupy reefs, rocky coastlines and eelgrass meadows in tropical and subtropical waters. Many species are sequential hermaphrodites, beginning life as females and then changing into males after reaching a certain size. While female reproductive success is limited by the number of eggs she can produce, male reproductive success can be much higher if he can fertilize the eggs of many females. So if a parrotfish transitions into a large male, and can control access to numerous females, he will enjoy greater reproductive success than if he had remained a female.

Two Chlorurus spilurus parrotfish show off their teeth and colors. The large colorful fish on the right is a male, while the smaller darker fish to his left is a female. Credit: Brett Taylor.

Phenotypic plasticity describes the ability of an individual with a particular genetic makeup to vary in a variety of traits (such as what it looks like, or how it behaves) in response to different environmental conditions. About 15 years ago, Nick Gust’s PhD research on tropical reef fish revealed that tremendous variation in parrotfish traits existed over a distance of a few kilometers. But what causes this variation? When funding became available, Brett Taylor jumped at the opportunity to pinpoint the causes, focusing on the diverse parrotfish community in the Great Barrier Reef (GBR).

Eastern slope of the Great Barrier Reef hosts a diversity of fish and coral species. Credit: Brett Taylor.

Taylor and his colleagues surveyed 82 sites within 31 reefs across 6 degrees of latitude in the northern GBR. To standardize data collection, divers, armed with a multitude of cameras and GPS devices, swam at a standardized rate (about 20 meters/minute) for 40 minutes per survey, recording each parrotfish along a 5 m wide swath. They collected data about the habitat and the environment, about the physical traits of each individual parrotfish (such as size and sex), and about the type and abundance of parrotfish and their predators present at each site.

Researcher takes notes while conducting a dive. Credit Kendra Taylor.

The researchers wanted to identify what factors influenced growth rate, maximum body size, and the size at sex change, and how these factors related to the parrotfish mating system. Four species of parrotfish were sufficiently abundant across the GBR to allow researchers to do this type of analysis.

Four parrotfish species abundant along exposed outer shelf (yellow sites) and protected inner shelf (blue) regions of the Great Barrier Reef. Males are larger and more colorful.

The GBR varies structurally across a relatively small spatial scale of 40 – 100 km, with outer shelf regions (eastern) exposed to wave action, and inner shelf regions (western) relatively protected. All four species tended to change sex at a larger size in protected sites than they did at exposed sites. However, the differences are only compelling for two of the species: C. spilurus and S. frenatus. There were fewer data points for the other two species, so it is possible (but unknown) that they too would show a more pronounced trend if more data were available.

Proportion terminal phase (sex-changed males) in relation to body size (measured to the fork of the tail) in exposed (yellow) and sheltered (blue) sites.

Not surprisingly, parrotfish grew larger in protected areas. Presumably, less wave action provided a more benign environment for rapid growth, both of parrotfish and their preferred food items (algae growing on rocks and coral).

Standardized maximum size (Lmax) attained by parrotfish in sheltered vs. exposed sites.

The researchers were somewhat surprised that most other factors, such as latitude, coral cover, sea surface temperature, and predator abundance, had very little effect on the size at sex change. Rather, the size at sex change appears to be strongly influenced by the local size distribution. In protected habitats, parrotfish grow large and change sex at a large size, while in exposed habitats, parrotfish are smaller, and change sex at a smaller size.

But sex is never simple. Nick Gust’s PhD research showed that C. spilurus had different patterns of sexual allocation in protected vs. exposed areas. In protected areas, the mating system is haremic, with a large male defending a territory and servicing a harem of females. In exposed areas, the mating system is mixed; there still are large territorial males with their harems, but they compete with many more small males, and group spawning is much more prevalent. Theoretically, the presence of these small males may make it less worthwhile for a female to transition into a male, and may influence the optimal size for transitioning in exposed reefs. Given that we still don’t know the mating system details of the other parrotfish in this study, it will be fascinating to see if they too show similar patterns of haremic vs. mixed mating systems in relation to habitat structure.

note: the paper that describes this research is from the journal Ecology. The reference is Taylor, B. M., Brandl, S. J., Kapur, M., Robbins, W. D., Johnson, G., Huveneers, C., Renaud, P. and Choat, J. H. (2018), Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes. Ecology 99(3): 642-651. doi:10.1002/ecy.2127. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Snails grow large to fight fear

March 1, 2018 by fredsingerecology

In a recent post (Jan 12), I discussed research showing that song sparrow parents reduce provisioning to their offspring when threatened by predators, ultimately reducing offspring survival rates. But in a turnabout that highlights the natural world’s dazzling diversity, a recent study by Sarah Donelan and Geoffrey Trussell revealed a very different impact of fear on the development of snail offspring. Donelan had worked as Trussell’s laboratory technician for two years and became fascinated by the egg capsules laid by the carnivorous snail Nucella lapillus, an ecologically important species in rocky intertidal communities. Earlier work had shown that predator-induced fear reduced snail feeding and growth rates, so Donelan decided that for her PhD work she would see how predator-induced fear influenced offspring development.

Adult Nucella alongside ca. 100 egg capsules. Credit: Sarah Donelan.

The researchers recognized that the fear environment experienced by parents before or during reproduction, and by the embryos during early development, could influence growth and development of those embryos. At their research site along the Massachusetts, USA coast, the predatory green crab, Carcinus maenas, can be a source of fear for these adult and embryonic snails. Donelan and Trussell exposed snails to fear by housing separately one male and one female snail in adjacent protected perforated containers (with six blue mussels in each container to feed them) that were set within a large plastic bucket. This bucket also had a somewhat larger perforated container (the risk chamber) containing the dreaded green crab (and two snails to feed it). The control risk chamber had two snails, but no crab.

Experimental setup with buckets containing egg capsules in perforated cages experiencing different exposure to fear. Credit: Sarah Donelan.

In late spring of 2015 and 2016, field-collected female and male snails were matched to create a total of 80 parental pairs. Donelan and Trussell set up experiments to explore the effects of parental experience with predation risk, embryonic experience with predation risk, and duration of embryonic experience.

Parent snails were exposed to a risk chamber (with a crab in the experimental group, and without a crab in the control group) for three days, and then placed together for four days (without risk) to mate. If an egg capsule was laid, the researchers removed it, and immediately exposed it to an experimental or control risk chamber for a week. Embryonic risk duration was further manipulated by continuing to expose half of the egg capsules to risk for a total of six weeks. The table below summarizes the treatments received by parents and offspring.

DonelanTableGood

Mean (+ standard error) shell length (top graph) and tissue mass (bottom graph) of snail embryos exposed to predation risk. Parents were either exposed (solid circles) or not exposed (open circles) to risk before mating.

When parents were not exposed to risk, but their offspring were exposed, these offspring had shorter shells and reduced tissue mass compared to all other groups. When both parents and offspring were exposed to risk, offspring shell length increased by 8% and offspring mass increased by a whopping 40% over risk-exposed offspring whose parents were not exposed to risk (left data points in figures a and b). If embryos were not exposed to risk, parental exposure had no significant impact on embryonic development (right data points on figures a and b). Embryonic risk duration had no impact on development.

In addition, risk-exposed offspring of risk-exposed parents emerged from their egg capsules an average of 4.1 days sooner than other offspring.

Mean (+standard error) number of days until emergence of snail offspring that experienced the presence or absence of predation risk during early development. Their parents were exposed to risk (solid circle) or no risk (open circle) before mating.

What could be causing these differences in size and rate of development? Donelan and Trussell hypothesized that embryonic snails could grow larger and more quickly if they were somehow able to reduce their metabolic rate. With a reduction in metabolic rate, more energy could be diverted to growth and development, resulting in larger and faster-growing snails. The researchers used an oxygen meter to measure oxygen consumption rates of individual egg capsules (from the eight different treatments in the first experiment) six weeks after deposition, about a week before embryos would begin to emerge. They exposed some of the capsules to predation risk during the experiment (current risk graph below), and left other capsules unexposed. When tested under risky conditions, capsules from parents who were exposed to risk, and that experienced risk as embryos during early development, had 56% lower metabolic rates than the other three groups (left graph), and similarly low metabolic rates as capsules tested without risk (right graph).

Mean (+ standard error) respiration rate of egg capsules that were (left graph) or were not (right graph) exposed to current predation risk. During early development, the embryos in these capsules experienced risk or no risk, and were produced by parents exposed to risk (solid circles) or no risk (open circles) before mating.

Overall, parental experience with predation risk enhances offspring growth and development in the presence of risk. If the parents lack this exposure, risk-exposed offspring suffer the costs associated with small size and slower development. Currently Donelan and Trussell are trying to figure out what these costs are. Smaller snails have less energy reserves, may feed on a less diverse group of prey, and are less likely to remain in safer habitats than are larger juveniles. But we still don’t know whether these effects on early stages of life have lasting impacts as a snail gets older and larger. More generally, we don’t know whether there are similar types of interactions between parental and embryonic experiences of other stressors, most notably environmental stresses that are already being imposed by climate change.

note: the paper that describes this research is from the journal Ecology. The reference is Donelan, S. C. and Trussell, G. C. (2018), Synergistic effects of parental and embryonic exposure to predation risk on prey offspring size at emergence. Ecology, 99: 68–78. doi:10.1002/ecy.2067. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Homing in on the micro range

February 8, 2018 by fredsingerecology

I’ve always been fascinated by geography. As a child, I memorized the heights of mountains, the populations of cities, and the areas encompassed by various states and countries. I can still recite from memory many of these numbers – at least based on the 1960 Rand McNally World Atlas. Part of my fondness for geography is no doubt based on my brain’s ability to recall numbers but very little else.

Most geographic ecologists are fond of numbers, exploring numerical questions such as how many organisms or species are there in a given area, or how large an area does a particular species occupy? They then look for factors that influence the distribution and abundance of species or groups of species. Given that biologists estimate there may be up to 100 million species, geographic ecologists have their work cut out for them.

As it turns out, most geographic ecologists have worked on plants, animals or fungi, while relatively few have worked on bacteria and archaeans (a very diverse group of microorganisms that is ancestral to eukaryotes).

Two petri plates with pigmented Actinobacteria. Credit: Mallory Choudoir.

Until recently, bacteria and archaeans were challenging subjects because they were so small and difficult to tell apart. But now, molecular/microbial biology techniques allow us to distinguish between closely related bacteria based on the sequence of bases (adenine, cytosine, guanine, and uracil) in their ribosomal RNA. Bacteria which are identical in more than 97% of their base sequence are described as being in the same phylotype, which is roughly analogous to being in the same species.

As a postdoctoral researcher working in Noah Fierer’s laboratory with several other researchers, Mallory Choudoir wanted to understand the geographic ecology of microorganisms. To do so, they and their collaborators collected dust samples from the trim above an exterior door at 1065 locations across the United States (USA).

Dr. Val McKenzie collects a dust sample from the top of a door sill. Credit: Dr. Noah Fierer.

The researchers sequenced the ribosomal RNA from each sample to determine the bacterial and archaeal diversity at each location. Overall they identified 74,134 gene sequence phyloypes in these samples – that took some work.

On average, each phylotype was found at 70 sites across the USA, but there was enormous variation. By mapping the phylotypes at each of the 1065 locations, the researchers were able to estimate the range size of each phylotyope. They discovered a highly skewed distribution of range sizes, with most phylotypes having relatively small ranges, while only a very few had large ranges (see the graph below). As it turns out, we observe this pattern when analyzing range sizes of plant and animal species as well.

Mean geographic range (Area of occupancy) for each phylotype in the study. The y-axis (Density) indicates the probability that a given phylotype will occupy a range of a particular size (if you draw a straight line down from the peak to the x-axis, you will note that most phylotypes had an AOO of less than 3000 km²

Taxonomists use the term phylum (plural phyla) to indicate a broad grouping of similar organisms. Just to give you a feel for how broad a phylum is, humans and fish belong to the same phylum. Some microbial phyla had much larger geographic ranges than others. Interestingly, it was not always the case that the phylum with the greatest phylotype diversity had the largest range. For example, phylum Chrenarchaeota had the greatest median geographic range (see the graph below), but ranked only 19 (out of 50 phyla) in number of phylotypes (remember that a phylotype is kind of like a species in this study).

Box plots showing range size distribution for individual phyla. Middle black line within each box is the median value; box edges are the 25th and 75th percentile values (1st and 3rd quartiles). Points are outlier phylotypes. Notice that the y-axis is logarithmic.

With this background, Choudoir and her colleagues were prepared to investigate whether there were any characteristics that might influence how large a range would be occupied by a particular phylotype. We could imagine, for example, that a phylotype able to withstand different types of environments would have a greater geographic range than a phylotype that was limited to living in thermal pools. Similarly, a phylotype that dispersed very effectively might have a greater geographic range than a poor disperser.

The researchers expected that aerobic microorganisms (that use oxygen for their metabolism) would have larger geographic ranges than nonaerobic microorganisms, which are actually poisoned by oxygen. The data below support this prediction quite nicely.

Geographic range size in relation to oxygen tolerance. In this graph, and the graphs below, the points have been jittered to the right and left of their bar for ease of viewing (otherwise even more of the points would be on top of each other).

Some bacterial species form spores that protect them against unfavorable environmental conditions. The researchers expected that spore-forming bacteria would have larger geographic ranges than non-spore-forming bacteria.

Geographic range in relation to spore formation (left graph) and pigmentation (right graph).

Choudoir and her colleagues were surprised to discover exactly the opposite; the spore forming bacteria had, on average, slightly smaller geographic ranges. Choudoir and her colleagues also expected that phylotypes that are protected from harsh UV radiation by pigmentation would have larger geographic ranges than unpigmented phylotypes – this time the data confirmed their expectations.

The researchers identified several other factors associated with range size. For example, bacteria with more guanine and cytosine in their DNA or RNA tend to have larger geographic ranges. Some previous studies have shown that a higher proportion of guanine and cytosine is associated with greater thermal tolerance, which should translate to a greater geographic range. Choudoir and her colleagues also discovered that microorganisms with larger genomes (longer DNA or RNA sequences) also had larger ranges. They reason that larger genomes (thus more genes) should correspond to greater physiological versatility and the ability to survive variable environments.

This study opens up the door to further studies of microbial geographic ecology. Some patterns were expected, while others were surprising and beg for more research. Many of these microorganisms are important medically, ecologically or agriculturally, so there are very good reasons to figure out why they live where they do, and how they get from one place to another.

note: the paper that describes this research is from the journal Ecology. The reference is Choudoir, M. J., Barberán, A., Menninger, H. L., Dunn, R. R. and Fierer, N. (2018), Variation in range size and dispersal capabilities of microbial taxa. Ecology, 99: 322–334. doi:10.1002/ecy.2094. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

“Notes from Underground” – cicadas as living rain gauges

January 31, 2018 by fredsingerecology

Given recent discussions between Donald Trump and Kim Jong-un about whose button is bigger, many of us with entomological leanings have revisited the question of what insects are most likely to dominate a post-nuclear world. Cicadas have a developmental life history that predisposes them to survival in the long term because some species in the eastern United States spend many subterranean years as juveniles (nymphs), feeding on the xylem sap within plants’ root systems. Magicicada nymphs live underground for 13 or 17 years, depending on the species, before digging out en masse, undergoing one final molt, and then going about the adult business of reproduction. This life history of spending many years underground followed by a mass emergence has not evolved to avoid nuclear holocausts while underground, but rather to synchronize emergence of billions of animals. Mass emergence causes predator satiation, an anti-predator adaptation in which predators are gastronomically overwhelmed by the number of prey items, so even if they eat only cicadas and nothing else, they still are able to consume only a small fraction of the cicada population.

Mass Magicicada emergence picturing recently-emerged winged adults, and the smaller lighter-colored exuviae (exoskeletons) that are shed during emergence. Credit: Arthur D. Guilani.

Less well-known are the protoperiodical cicadas (subfamily Tettigadinae) of the western United States that are abundant in some years, and may be entirely absent in others. Jeffrey Cole has studied cicada courtship songs for many years, and during his 2003 field season noted that localities that had previously been devoid of cicadas now (in 2003) hosted huge numbers of six or seven different species. He returned to those sites every year and high diversity and abundance reappeared in 2008 and 2014. This flexible periodicity contrasted with their eastern Magicicada cousins, and he wanted to know what stimulated mass emergence.

Protoperiodical cicadas studied by Chatfield-Taylor and Cole. Okanagana cruentifera (top) and Clidophleps wrighti (bottom). Credit Jeffrey A. Cole.

Cole and his graduate student, Will Chatfield-Taylor, considered two hypotheses that might explain protoperiodicity in southern California (where they focused their efforts). The first hypothesis is that cicada emergence is triggered by heavy rains generated by El Niño Southern Oscillation (ENSO), a large-scale atmospheric system characterized by high sea temperature and low barometric pressure over the eastern Pacific Ocean. ENSO has a variable periodicity of 4.9 years, which roughly corresponds to the timing Cole observed while doing fieldwork. The second hypothesis recognized that nymphs must accumulate a set amount of xylem sap from their host plants to complete development. Sap availability depends on precipitation, and this accumulation takes several years in arid habitats. So while ENSO may hasten the process, the key to emergence is a threshold amount of precipitation over a several year timespan.

Working together, the researchers were able to identify seven protoperiodical species by downloading museum specimen data (including where and when each individual was collected) from two databases (iDigBio and SCAN). They also used data from several large museum collections, which gave them evidence of protoperiodical cicada emergences back to 1909. Based on these data, Chatfield-Taylor and Cole constructed a map of where these protoperiodical cicadas emerge.

Maps of five emergence localities discussed in this study.

The researchers tested the hypothesis that protoperiodical cicada emergences follow heavy rains triggered by ENSO by going through their dataset to see if there was a correlation between ENSO years and mass cicada emergences. Of 20 mass cicada emergences since 1918, only five coincided with ENSO events, which is approximately what would be expected with a random association between mass emergences and ENSO. Scratch hypothesis 1.

Let’s look at the second hypothesis. The researchers needed reliable precipitation data between years for which they had good evidence that there were mass emergences of their seven species. Using a statistical model, they discovered that 1181 mm was a threshold for mass emergences, and that three years was the minimum emergence interval regardless of precipitation. Only after 1181 mm of rain fell since the last mass emergence, summed over at least three years, would a new mass emergence be triggered.

Cumulative precipitation over seven time periods preceding cicada emergence.

The nice feature of this model is that it makes predictions about the future. For example, the last emergence occurred in the Devil’s punchbowl vicinity in 2014. Since then that area has averaged 182.2 mm of precipitation per year. If those drought conditions continue, the next mass emergence will occur in 2021 at that locality, which is longer than its historical average. Only time will tell. Hopefully Mr. Trump and Mr. Jong-un will be able to keep their fingers off of their respective buttons until then.

note: the paper that describes this research is from the journal Ecology. The reference is Chatfield-Taylor, W. and Cole, J. A. (2017), Living rain gauges: cumulative precipitation explains the emergence schedules of California protoperiodical cicadas. Ecology, 98: 2521–2527. doi:10.1002/ecy.1980. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

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How new research expands our understanding of the natural world

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