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.


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.


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.


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)


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.

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.


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.


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.


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)


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.


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


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.