Seaweed defense – location, location, location.

If you’re ever feeling sorry for yourself, you should know that things could have been much worse; you could have been the brown seaweed, Silvetia compressa. So many problems!  Ocean waves come crashing over you, threatening to pull you off your life-sustaining substrate.  Ocean tides recede, exposing you to harsh sun and dangerously dry conditions. Perhaps worst of all, the fearsome predator Tegula funebralis eats away at your body, and you are powerless to defend yourself from its savage ravages.

MoatCreek_SilvetiaTegula

Tegula snails chomp away on Silvetia seaweed in northern California. Credit: Emily Jones.

As it turns out, Silvetia is not so powerless after all.  After being partially grazed by Tegula, the seaweed can induce defenses that reduce its palatability.  From prior work, Emily Jones noticed that seaweed from northern California shorelines was much more sensitive to grazing than was seaweed from southern California shorelines.  It took fewer grazing snails to elicit palatability reduction in northern Silvetia than it did in southern Silvetia. She decided to focus her PhD work with Jeremy Long on documenting these geographic differences, and figuring out why they exist.

MoatCreek_surveys

Emily Matthews (near) and Grace Ha (far) survey snails and seaweed in a northern California site. Credit: Emily Jones.

Environmental conditions vary along the California coast.  Northern seaweed populations experience cooler temperatures (air ~5-20 °C; water ~10-12 °C) and more nutrients (nitrate levels up to 40 umol/L) than do southern populations (air 5-37 °C; water ~14-20 °C; nitrate levels < 2 umol/L). In addition, Jones and Long surveyed Tegula abundance at three northern California and three southern California sites, counting every snail in 20 quadrats placed in the low, mid and high intertidal zone at each of the six sites (360 0.25 X 0.25m quadrats in total) .  They discovered that seaweed was much more likely to encounter Tegula along northern coastlines.

JonesFig1

Percent of plots with Tegula snails in northern sites (Stornetta, Moat Creek and Sea Ranch – blue bars) and southern sites (Coast, Calumet and Cabrillo – orange bars). High, Mid and Low refer to location within the intertidal zone (high is closest to shore and regularly exposed at low tide).

Given these differences in snail abundance, we can now understand why Silvetia is more sensitive in its northern range to Tegula grazing.  But how strong are these differences in sensitivity? Jones and Long developed a simple paired-choice feeding preference assay to test for differences in palatability. At each location (north and south), the researchers gave test snails a choice between feeding on seaweed that had been previously grazed by either 1, 4, 7, 10 or 13 Tegula snails, or to feed on seaweed with no grazing history.  The test snails grazed for five days, and the researchers measured the amount of seaweed consumed for each group. They discovered that even a little bit of previous grazing (the 1-snail treatment) made northern test snails prefer non-grazed northern Silvetia, while only high levels of previous grazing (the 10 and 13-snail treatments) had similar effects on southern snails tested on southern Silvetia.

JonesFig2

Amount of previously-grazed and non-grazed Silvetia eaten by Tegula in paired choice tests. (Top) Northern Selvetia, (Bottom) Southern Silvetia. Error bars are 1SE. * indicates significant differences in consumption rate.

These findings raised the question of whether the cooler and more nutrient-rich environmental conditions at the northern site were somehow causing this difference in consumption of previously-grazed seaweed.  The researchers designed a series of common garden experiments at the Bodega Marine Laboratory, in which seaweed from both locations were tested in the same environment.  Silvetia was exposed to grazing by two snails, or by no snails for 14 days. When test snails were given the choice of non-grazed or previously-grazed northern Silvetia, they much preferred eating non-grazed Silvetia. In contrast, they showed no preference when given a similar choice between non-grazed or previously-grazed southern Silvetia. This indicates that seaweed from the north are responding more to grazing by reducing palatability than are seaweed from the southern locations.

JonesFig5

Amount of previously-grazed and non-grazed northern and southern Silvetia eaten by Tegula in paired choice tests.

In theory, there could be a tradeoff between induced defenses, such as reduction in palatability in response to grazing, and constitutive defenses, which an organism expresses all of the time.  Examples of constitutive defenses are thorns or spines in plants, and cryptic coloration or body shape in many insects.  Jones and Long found no evidence for such a tradeoff; in contrast southern Silvetia actually had lower levels of constitutive defenses, as both northern and southern Tegula strongly preferred eating southern Silvetia in paired choice tests.

JonesFig6

Amount of northern and southern Silvetia eaten by northern and southern Tegula in paired choice tests.

These geographic differences in seaweed sensitivity to grazing are probably due to long-term differences in environmental history.  Southern Silvetia seaweeds live in stressful conditions (high temperatures and low nutrients), and the physiological cost of mounting an induced defense against low and moderate levels of grazing may be too high to be worthwhile. We also don’t know what the overall grazing rates are in the north versus the south, and importantly, how variable the grazing rates are in each location.  Highly variable grazing rates would select for a strong set of induced responses, which could be turned on and off as needed, allowing seaweed, or any plant, to defend itself against new or more hungry herbivores moving into their environment.

note: the paper that describes this research is from the journal Ecology. The reference is Jones, Emily and Long, Jeremy D. 2018. Geographic variation in the sensitivity of an herbivore-induced seaweed defense. Ecology. doi: 10.1002/ecy.2407. 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.

Indirect effects of the lionfish invasion

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.

Lionfish

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.

Basslets

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

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.

KindingerFig12A

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.

KindingerFig1BC

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.

KindingerFig2BC

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. Ecology99(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.

Mangroves partner with rats in China

Many of us have seen firsthand the havoc that invasive plants can wreak on ecosystems.  We are accustomed to think of native plants as unable to defend themselves, much like a skinny little kid surrounded by a group of playground bullies. ‘Not so fast’ says Yihui Zhang.  As it turns out, many native plants can defend themselves against invasions, and they do so with the help of unlikely allies.

In southern China, mangrove marshes are being invaded by the salt marsh cordgrass, Spartina alterniflora, which is native to the eastern USA coastline. Cordgrass seeds can float into light gaps among the mangroves, and then germinate and choke out mangrove seedlings.  However, intact mangrove forests can resist cordgrass invasion.  Zhang and his colleagues wanted to know how they resist.

mangrove-Spartina ecotone

Cordgrass (pale green) meets mangrove (bright green) as viewed from space. Credit: Yihui Zhang.

Cordgrass was introduced into China in 1979 to reduce coastal erosion.  It proved up to the task, quickly transforming mudflats into dense cordgrass stands, and choking out much of the native plant community.  Dense mangrove forests grow near river channels that enter the ocean, and are considerably taller than their cordgrass competitors.  The last player in this interaction is a native rat, Rattus losea, which often nests on mangrove canopies above the high tide level. At the research site (Yunxiao), many rat nests were built on mangroves, using cordgrass leaves and stems as the building material.

zhangnest.png

Rat nest constructed from cordgrass shoots rests upon a mangrove tree.  Credit Yihui Zhang.

Zhang and his colleagues suspected that cordgrass invasion into the mangrove forest was prevented by both competition from mangroves and herbivory by rats on cordgrass.

Baby rat in the nest

Baby rats in their nest. Credit Yihui Zhang.

 

To test this hypothesis, they built cages to exclude rats from three different habitats: open mudflats (primarily pure stands of cordgrass), the forest edge, and the mangrove forest understory, (with almost no cordgrass). They set up control plots that also had cages, but that still allowed rats to enter.

zhangregenshoot

Arrow points to resprouting cordgrass. Credit Yihui Zhang.

The researchers planted 6 cordgrass ramets (genetically identical pieces of live plant) in each plot and then monitored rodent grazing, resprouting of original shoots following grazing, and shoot survival over the next 70 days.

They discovered that the cages worked; no rats grazed inside the cages.  But in the control plots, grazing was highest in the forest understory and lowest in the mudflats (Top figure below).  Most important, both habitat type and exposure to grazing influenced cordgrass survival.  In the understory, rodent grazing was very important; only one ramet survived in the control plots, while 46.7% of ramets survived if rats were excluded.  In the other two habitats, grazing did not affect ramet survival, which was very high with or without grazing (Middle figure). Rodent grazing effectively eliminated resprouting of ramets in the understory, but not in the other two habitats (Bottom figure).

Zhangfig2

Impact of rat grazing on cordgrass in the field study in three different habitats.  Top figure is % of stems grazed, middle figure is transplant survival, and bottom figure is resprouting after grazing (there was no grazing in the rodent exclusion plots). Error bars are 1 standard error. Different letters above bars indicate significant differences between treatments.

The researchers suspected that low light levels in the understory were preventing cordgrass from resprouting after rat grazing. This was most easily tested in the greenhouse, where light conditions could be effectively controlled.  High light was 80% the intensity of outdoor sunlight, medium light was 33% (about what strikes the forest edge) and low light was 10% the intensity of outdoor sunlight (similar to mangrove understory light).  Rat grazing was simulated by cutting semi-circles on the stembase, pealing back the leaf sheath, and digging out the leaf tissue. Cordgrass ramets were planted in large pots, exposed to different light and grazing treatments, and monitored for survival, growth and resprouting following grazing.

Greenhouse setup

Cordgrass growing in greenhouse under different light treatments. Credit: Yihui Zhang.

Zhang and his colleagues found that simulated grazing sharply reduced cordgrass survival from 85% to 7% at low light intensity, but had no impact on survival at medium or high light intensities.  Cordgrass did not resprout after simulated grazing at low light intensity, in contrast to approximately 50% resprouting at medium and high light intensity.

ZhangFig4

Survival (top) and resprouting (bottom) of cordgrass following simulated grazing in the greenhouse experiment.

The researchers conclude that grazing by rats and shading by mangroves are two critical factors that make mangroves resistant to cordgrass invasion. Rats tend to build their nests near the mangrove forest edge, so it is not clear how far into the forest the rat effect extends. Rats do prefer to forage in the understory (rather than right along the edge), presumably because the understory helps to protect them from predators.  In essence, mangroves compete directly with cordgrass by shading them out, and also indirectly by attracting cordgrass-eating rats. Conservation biologists need to be aware of both direct and indirect effects when designing management programs for protecting endangered ecosystems such as mangrove forests.

note: the paper that describes this research is from the journal Ecology. The reference is Zhang, Y. , Meng, H. , Wang, Y. and He, Q. (2018), Herbivory enhances the resistance of mangrove forest to cordgrass invasion. Ecology. Accepted Author Manuscript. doi:10.1002/ecy.2233. 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

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.

LaForgiaSeedlings

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.

 

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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.

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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.

LaForgiaFig1

(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.

LaForgiaFig2

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.

Too much of a good thing is killing Monarch butterflies

There was a time in the mid-Pleisticine when a photo of an ecological event was an awesome novelty, and a movie of an ecological event even more so.  Dodderers of an ecological bent (myself included), can vividly recall viewing a series of photos or a movie, either in a seminar or in an ancient ecology text, of a blue jay consuming a monarch butterfly, Danaus plexippus.  Consumption is immediately followed by explosive vomiting, as the cardenolides within the monarch butterfly claim another victim.  The monarch sequesters these cardenolide toxins from its larval food (milkweed), and incorporates them into its tissues as a means of protecting itself from predators – presumably blue jays learn from this very aversive experience.  I should point out that the individual sacrificial butterfly enjoys no fitness from this learning event – which raises some evolutionary questions we will not explore at the present.

Karen Oberhauser

Five instars (stages of development) of monarch caterpillars on a milkweed leaf. Credit: Karen Oberhauser

Rather we turn our attention to the relationship between milkweed, monarchs, and climate change. In several places in this blog we’ve talked about how climate change has influenced the behavior or physiology of a single species. For example, my first blog (Jan 31, 2017) discusses how increasing temperatures create more females in a loggerhead turtle population. But there are fewer studies that explore how climate change influences the ecological landscape, ultimately affecting interactions between species.  Along these lines, Matt Faldyn wondered if increased air temperature would change the chemical constitution of milkweed in a way that might influence monarch populations.  As he describes, “With milkweed toxicity, there is a ‘goldilocks’ zone where monarchs prefer to feed on milkweed that produce enough toxins in order to sequester these (cardenolide) chemicals as an antipredator/antiparasite defense, while also avoiding reaching a tipping point of toxicity where feeding on very toxic milkweeds negatively impacts monarch fitness.” He expected that at higher temperatures, milkweed would become stressed, and be physiologically unable to sustain normal levels of cardenolide production.

Faldynnative

Monarch butterfly feeds on a native milkweed, Asclepias incarnata. Credit: Teune at the English Language Wikipedia.

For their research, Faldyn and his colleagues worked with two milkweed species.  Asclepias incarnata is a common, native milkweed found throughout the monarch butterfly’s range in the eastern and southeastern United States.  Asclepias curassavica is an exotic species that has become established in the southern United States.  In contrast to A. incarnata, A. curassavica does not die back over the winter months; consequently some monarch populations are no longer migratory, relying on A. curassavicato provide them with a year round food supply.

Faldynexotic

The exotic milkweed, Asclepias curassavica. Credit: 2016 Jee & Rani Nature Photography (License: CC BY-SA 4.0)

To protect against herbivory, milkweeds have two primary chemical deterrants: (1) the already-mentioned cardenolides, which are toxic steroids that disrupt cell membrane function, and (2) release of sticky latex, which can gum up caterpillar mouthparts and actually trap young caterpillars.

field_noborderii.jpgThe researchers wanted to simulate climate change under field conditions, so they created open-top chambers with plexiglass plates that functioned much like mini-greenhouses, into which they placed one milkweed plant that was covered with butterfly netting.  This setup raised ambient temperatures by about 3°C during the day and 0.2°C at nighttime.  Control plots were single milkweed plants with butterfly netting. Half of the plants were native milkweed, and the other half were the exotic species.

For their experiments, Faldyn and his colleagues introduced 80 monarch caterpillars (one per plant) and allowed them to feed normally until they pupated.  Pupae were brought into the lab and allowed to metamorphose into adults.

MattGood

Matt Faldyn holds two monarch butterflies in the laboratory. Credit Matt Faldyn.

At normal (ambient) temperatures, monarchs survived somewhat better on exotic milkweed.  But at warmer temperatures, there is a strikingly different picture. Monarch survival is unaffected by warmer temperatures on native milkweed, but is sharply reduced by warmer temperatures on exotic milkweed (top graph below). The few that managed to survive warm temperatures on exotic milkweed grew much smaller, based on their body mass and forewing length (middle and bottom graph below)

FaldynFig1

Survival (top), adult mass (middle) and forewing length (bottom) of monarch butterflies raised under normal (ambient) and warmed temperatures.  Error bars are 95% confidence intervals.

Both milkweed species increased production of both types of chemicals over the course of the experiment. But by the end of the experiment, the exotic species released 3-times the quantity of latex and 13-times the quantity of cardenolides than did the native milkweed species.

FaldynFig2

Average amount of latex released at the beginning and end of the experiment.  Error bars are 95% confidence intervals.

FaldynFig2

Average cardenolide concentration at the beginning and end of the experiment.

The researchers argue that the exotic milkweed, Asclepias curassavica, may become an ecological trap for monarch butterflies, in that it attracts monarchs to feed on it, but will, under future warmer conditions, result in dramatically reduced monarch survival. Interestingly, these results are not what Faldyn originally expected; recall that he anticipated that temperature-stressed plants would reduce cardenolide production. The tremendous increase in cardenolide production in exotic milkweed at warmer temperatures may simply be too much toxin for the monarchs to process. The researchers predict that as climate warms, milkweed ranges will expand further north into Canada, and lead to northward shifts of monarch populations as well.  They urge nurseries to emphasize the distribution of native rather than exotic milkweed, so that monarchs will be less likely to become victims of this ecological trap.

note: the paper that describes this research is from the journal Ecology. The reference is Faldyn, M. J., Hunter, M. D. and Elderd, B. D. (2018), Climate change and an invasive, tropical milkweed: an ecological trap for monarch butterflies. Ecology. doi:10.1002/ecy.2198. 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.

Fungi attack plants – insects respond!

As she was preparing to do her dissertation research on the interactions between the Asian chestnut gall wasp, the chestnut blight disease and the European chestnut, Pilar Fernandez-Conradi read a lot of papers about fungal-insect-plant interactions.  She was impressed by the diversity of outcomes that resulted when plants were attacked by both insects and fungi, and wondered whether there were any generalities to glean from these research findings. She asked two basic questions. First, if a plant is infected by a fungus, is it more or less likely to be attacked by insects than is an uninfected plant?  Second, does an insect that attacks a fungal-infected plant perform better or worse than it would have on an uninfected plant?

D. Kuriphilus+Gnomo

Three-way interaction between the chestnut tree, the chestnut gall wasp, and the fungus Gnomopsis castanea. Female wasps induce the plant to create galls, which house developing larvae. Green globular galls (with a hint of rose-color) have not been infected by a fungus, while the very dark tissue is the the remains of a gall that was attacked by the fungus. Credit: Pilar Fernandez-Conradi.

Fernandez-Conradi and her colleagues thought they were more likely to discover a negative effect of fungal infection on the preference and performance of herbivorous insects.  Several studies had shown that nutrient quantity and quality of host plants is reduced by fungal infection, so it makes sense that insects would avoid infected plants.  But the researchers also knew that fungal infection can, in some cases, actually increase the sugar concentration of some plants, so insects might prefer those plants and also develop more rapidly on them. In addition, fungal infection can induce chemical defenses in plants that might make them less palatable to insects, or alternatively, fungal infection could weaken plant defenses making them more palatable to attacking insects.

To resolve this conundrum, Fernandez-Conradi and her colleagues did a meta-analysis, of the existing literature, identifying 1113 case studies based on 101 papers.  To be considered in the meta-analysis, all of the studies had to meet the following criteria: (1) report insect preference or performance on fungal-infected vs. uninfected plants, (2) report the Genus or species of the plant, fungus and insect, (3) report the mean response and a measure of variation (standard error, standard deviation or variance). The measure of variation allows researchers to calculate the effect size, which calculates the strength of the relationship that is being explored. The researchers found that, in general, insects avoid and perform worse on infected plants than they do on uninfected plants.

Fernandez-conradi-myfig

Mean effect size of insect preference and performance (combined) in response to fungal infection infection.  Error bars are 95% confidence intervals (CIs).  In this graph, and the next two graphs as well, a solid data point indicates a statistically significant effect.  You can also visually test for statistical significance by noting that the error bar does not cross the dashed vertical line that represents no effect (at the 0.0 value). The negative value indicates that insects respond negatively to fungal infection.

Fernandez-Conradi and her colleagues then broke down the data to explore several questions in more detail. For example, they wondered if the type of fungus mattered.  For their meta-analysis, they considered three types of fungi with different lifestyles: (1) biotrophic pathogens that develop on and extract nutrients from living plant tissues, (2) necrotrophic pathogens that secrete enzymes that kill plant cells, so they can develop and feed on the dead tissue, and (3) endophytes that live inside living plant tissue without causing visible disease symptoms.

Fernandez-conradiFig1

Effect of fungus lifestyle on insect performance.  k = the number of studies.  Different letters to the right of CIs indicate significant differences among the variables (lifestyles).

The meta-analysis showed an important fungus-lifestyle effect (see the graph to your left).  Insect performance was strongly reduced in biotrophic pathogens and endophytes, but not in necrotrophic pathogens, where insect performance actually improved slightly (but not significantly). The researchers point out that biotrophic pathogens and endophytes both develop in living plant tissues, while necrotrophic pathogens release cell-wall degrading enzymes which can cause the plant to release sugars and other nutrients.  These nutrients obviously benefit the fungus, but can additionally benefit insects that feed on the plants.

To further explore this lifestyle effect, Fernandez-Conradi and her colleagues broke down insect response into performance and preference, focusing on chewing insects, for which there were the most data. Insects showed lower performance on and reduced preference (i.e. increased avoidance) for plants infected with biotrophic pathogens. They also performed equally poorly on endophyte-infected plants, but did not avoid endophyte-infected plants (see graph below). This was surprising since you would expect natural selection to favor insects that can choose the best plants to feed on. The problem for insects may be that endophytic infection is basically symptomless, so the insects may, in many cases, be unable to tell that the plant is infected, and likely to be less nutritionally rewarding.

Fernandez-conradiFig2

Effects of fungal infection on preference and performance of chewing insects.  k = the number of studies.  Different letters to the right of CIs indicate significant differences among the variables. Variables that share one letter have similar effect sizes. 

Many ecological studies deal with two interacting species: a predator and a prey, or a parasite and its host.  Fernandez-Conradi and her colleagues remind us that though two-species interactions are much easier to study, many important real-world interactions involve three or more species. Their meta-analysis highlights that plant infection by pathogenic and endophytic fungi reduces the performance and preference of insects that feed on these plants. But fungus lifestyle plays an important role, and may have different effects on performance and preference. Their meta-analysis also suggests other related avenues for research.  For example, how are plant-fungus-insect interactions modified by other species, such as viruses, bacteria and parasitoids (an animal that lives on or inside an insect, and feeds on its tissues)? Or, what are the underlying molecular (hormonal) mechanisms that determine the response of the plant to fungal infection, and to insect attack?  Finally, how does time influence both plant and insect response?  If a plant is recently infected by a fungus, does it have a different effect on insect performance and preference than does a plant that has suffered from chronic infection.  There are very few data on these (and other) questions, but they are more likely to get pursued now that some basic relationships have been uncovered.

note: the paper that describes this research is from the journal Ecology. The reference is Fernandez‐Conradi, P., Jactel, H., Robin, C., Tack, A.J. and Castagneyrol, B., 2018. Fungi reduce preference and performance of insect herbivores on challenged plants. Ecology, 99(2), pp.300-311. 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

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.

Daniel Winkler - Saguaro Photo 1

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.

Daniel Winkler - Saguaro Photo 2

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.

nesthole

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.

Daniel Winkler - Saguaro Photo 4

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).

WinklerFig1

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.

WinklerFig2

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.