Invasive crayfish depress dragonflies and boost mosquitoes

Paradoxically, obliviousness and intense focus can be two sides of the same coin, as the following story highlights.  As a new graduate student at the University of Minnesota, I took a field ecology course at the University’s field station at Lake Itasca (famously known as headwaters of the Mississippi River).  One afternoon we watched dragonflies at a small pond; the male dragonflies were obviously patrolling territories and behaving thuggishly whenever intruders came by, and amorously whenever females of their species approached.  Surprisingly, territorial males chased off male intruders of any species, even though they posed no reproductive threat to them.  Why, I wondered…  So I sat there for many hours and kept very careful track of who chased whom, and for how long.  Big focus time. Ultimately, these observations blossomed into my doctoral dissertation.  Unfortunately, these observations also blossomed into the most virulent case of poison ivy known to humanity, as my intense focus on dragonflies obliviousized me to the luxurious patch of poison ivy, which served as my observation perch.

Anax junius Henry Hartley

Anax junius dragonflies in copula.  The male has the bright blue abdomen.  Credit: Henry Hartley.

Despite this ignoble incident, dragonflies remain one of my favorite animal groups.  They are strikingly beautiful, brilliant flyers, and fun to try to catch. In addition, they have so many wonderful adaptations, including males with penises that are shaped to scoop out sperm (previously introduced by another male) from their mate’s spermatheca, and females who go to extremes to avoid repeated copulation attempts, for example, by playing dead when approached by a male. Thus I was delighted to come across research by Gary Bucciarelli and his colleagues that highlighted the important role dragonflies play in stream ecosystems just west of Los Angeles, California.

Back Camera

Captured dragonfly nymph.  Dragonflies require from one to four years to develop in aquatic systems, before they metamorphose into terrestrial winged adults. As nymphs, they are fearsome predators on aquatic invertebrates. As adults, they specialize on winged insects, though there are stories of them killing small birds. Credit: Gary Bucciarelli

Bucciarelli and his colleagues came up with their research question as a result of working in local streams with students on a different project.  They wanted to know if invasive non-native crayfish (Procambarus clarkii) affect the composition of stream invertebrates and whether removal of crayfish could lead to rapid recovery of these invertebrate communities.

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Invasive crayfish, P. clarkii, sits on the stream bottom. Credit: Gary Bucciarelli

The researchers collected stream invertebrate samples and noticed a dramatic pattern – in all the streams with crayfish there were numerous mosquito larvae, but in all of the streams without crayfish there were no mosquito larvae and much greater numbers of dragonfly nymphs. This led them to formulate and test two related hypotheses. First, dragonfly nymphs (Aeshnaspecies) are more efficient predators on mosquitoes (Anopheles species) than are the invasive crayfish. Second, crayfish interfere with dragonfly predation on mosquitoes in streams where crayfish and dragonflies are both present.

Field Sampling

Student researchers collect stream samples. Credit: Gary Bucciarelli

Bucciarelli and his colleagues systematically sampled 13 streams monthly from March to October 2016 in the Santa Monica Mountains. Eight streams have had crayfish populations since the 1960s, while four streams never had crayfish, and one stream had crayfish removed as part of a restoration effort in 2015. Overall, streams with crayfish had a much lower number of dragonfly nymphs than did streams without crayfish.  In addition, streams with crayfish had substantial populations of Anopheles mosquitoes, while streams without crayfish (but much higher dragonfly populations) had no Anopheles mosquitoes in the samples.

BuccTable1

Number of mosquito larvae (MSQ) and dragonfly nymphs (DF)  by month in streams with crayfish (CF – top row of data) or without crayfish (CF Absent – bottom row)

This field finding supports both of the hypotheses, but the evidence is purely correlational.  So the researchers brought the animals into the laboratory to test predation under more controlled conditions.  They introduced 15 mosquito larvae into tanks, and exposed them to one of four treatments: (1) a single crayfish, (2) a single dragonfly nymph, (3) one crayfish and one dragonfly nymph, or (4) no predators. The researchers counted the numbers of survivors periodically over the three day trials. As the graph below indicates, dragonflies are vastly superior consumers of mosquito larvae compared to crayfish.  However, when forced to share a tank with crayfish, dragonflies stop hunting, either huddling in corners or actually perching on the crayfish.  By 36 hours into the experiment, all of the dragonflies had been eaten by the crayfish.  After three days, mosquito survival was similar when comparing tanks with crayfish alone with tanks that had both a crayfish and a dragonfly.

BuccFig2A

Mean number of surviving mosquito larvae in tanks with a lone dragonfly (DF), a lone crayfish (CF), one crayfish and one dragonfly (CF+DF) in comparison to controls with no predators.

Bucciarelli and his colleagues conclude that dragonfly nymphs are much more efficient predators of mosquito larvae than are crayfish. But when placed together with crayfish, dragonfly foraging efficiency plummeted. Field surveys showed a negative correlation between crayfish abundance and dragonfly larvae, and much greater mosquito larva populations in streams with crayfish.  This supports the conclusion that invasive crayfish cause mosquito populations to increase sharply by depressing dragonfly populations and foraging efficiency.  This is a complex trophic cascade because crayfish increase mosquito populations despite eating a substantial number of mosquito individuals.

The researchers argue that crayfish probably relegate dragonfly larvae to inferior foraging habitats, thereby limiting their efficiency as mosquito predators. As such, ecosystem services provided by dragonflies to humans are greatly diminished.  Recently, several new mosquito species that are disease vectors have moved into California.  Thus the loss of dragonfly predation services could pose a public health threat to the human population.  Bucciarelli and his colleagues recommend removing the invasive crayfish to restore the natural community of predators, including dragonflies, which will then naturally regulate the increased number of potential disease vectors.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Bucciarelli, G. M., Suh, D. , Lamb, A. D., Roberts, D. , Sharpton, D. , Shaffer, H. B., Fisher, R. N. and Kats, L. B. (2019), Assessing effects of non‐native crayfish on mosquito survival. Conservation Biology, 33: 122-131. doi:10.1111/cobi.13198. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Quoll vs. toad: a toxic brew

A native of Central and South America, the cane toad, Rhinella marina, was introduced to Australia in 1935 with great fanfare. The plan was for the voracious cane toad to eat all of the grey-backed cane beetles that were plaguing sugar cane plantations in northern Australia (a similar introduction had been successful in Puerto Rico).  But the plan failed, in part because there was no cover from predators, so the toads were not enthusiastic about hanging out in sugar cane plantations, and in part because adult beetles live primarily near the tops of sugar cane, and cane toads are poor climbers.

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A cane toad. Credit: Ben Philips

So now, northern Australia has a cane toad plague, which is wreaking havoc on ecosystems, and threatening many native species, including the northern quoll, Dasyurus hallucatus. These omnivorous marsupials eat fruit, invertebrates and small vertebrates.  Unfortunately, their long list of food items includes cane toads, which are highly toxic to most consumers, having poison glands that contain bufotoxin, a composite of several very nasty chemicals.  If a northern quoll eats a cane toad, it’s bye bye quoll.

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A northern quoll. Credit: Ella Kelly.

Unfortunately most quolls have not gotten the message; huge numbers are dying, and populations are going extinct.  As toads continue their invasion from north to south, more quoll populations, particularly those in northwestern Australia, will be at risk.

KellyFig1

Map of Australia showing past (light shading) and recent (dark shading) northern quoll distribution, and present (solid line) and future (dashed line) cane toad distribution.

Some quolls show “toad-smart” behavior and don’t eat toads. Ella Kelly and Ben Phillips are trying to understand how this happens. This is particularly important because a few quoll populations have managed to survive the cane toad plague by virtue of being toad-smart (though 95% of quoll populations have gone extinct in the wake of the cane toad wave). The researchers reason that if there is a genetic basis to toad-smart behavior, it might be possible to introduce toad-smart individuals into populations that have not yet been overrun by cane toads.  These individuals with toad-smart genes would breed and spread their genes through their adopted population.  This strategy of targeted gene flow would give the recipient population the genetic variation needed, so that some individuals (those with toad-smart genes) would be more likely to survive the cane toad invasion.  Over time toad-smart behavior would spread throughout the population via natural selection.

Targeted gene flow requires the trait to be influenced by genes.  To test for a genetic basis to the toad-smart trait, Kelly and Phillips designed a common-garden experiment, capturing some quolls that had survived the cane toad invasion (toad-exposed), and others from regions that had not yet been exposed (toad-naïve).  At Territory Wildlife Park, Northern Territory, Australia, the researchers bred these quolls to create three lines of offspring: Toad-exposed x toad-exposed, toad-exposed x toad-naïve (hybrids), and toad-naïve x toad-naïve.  They raised these three lines under identical conditions at the park. Kelly and Phillips then asked, are there behavioral differences in how these three lines respond to cane toads?

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Northern quoll captured in Northern Territory, Australia. Credit: Ella Kelly.

The researchers set up two experiments.  First they asked, which would a quoll (that had never before experienced a cane toad) prefer to investigate if given the choice: a dead cane toad or a dead mouse? It turned out that the quoll offspring with two toad-exposed parents were somewhat more interested in mice than in cane toads.  The same was true for the hybrids.  However, the toads with two toad-naïve parents showed little preference.

Second, and more important, the researchers gave quolls from the three lines the opportunity to eat a toad leg (which does not have enough poison to harm the quoll). The results of this experiment were striking; offspring of toad-naïve parents were twice as likely to eat the toad leg than were offspring of toad-exposed parents, or hybrids with one parent of each type.

KellyFig4

Proportion of toad-naive (both parents toad-naive), hybrid and toad-exposed (both parents toad-exposed) quoll offspring that ate a cane toad leg. Error bar = +/- 1 SE.

Kelly and Phillips conclude that toad-smart behavior is a genetically-based trait that has been under strong natural selection in populations of quolls that survived the cane toad invasion.  Hybrid offspring behave similarly to the offspring of two toad-exposed parents, suggesting that toad-smart behavior has a dominance inheritance pattern. The researchers propose using targeted gene flow, in this case introducing toad-adapted individuals into populations prior to the arrival of cane toads. Recently, Kelly and Phillips released 54 offspring with toad-smart genetic backgrounds onto Indian Island, which is about 40 km from Darwin.  The island has a large cane toad population, so the researchers will follow the introduced quoll population to see whether it is genetically equipped to survive in the presence of the cane toad scourge.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Kelly, E. and Phillips, B. L. (2019), Targeted gene flow and rapid adaptation in an endangered marsupial. Conservation Biology, 33: 112-121. doi:10.1111/cobi.13149. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Invasive engineers alter ecosystems

Ecosystem engineers  change the environment in a way that influences the availability of essential resources to organisms living within that environment.  Beavers are classic ecosystem engineers; they chop down trees and build dams that change water flow and provide habitat for many species, and alter nutrient and food availability within an ecosystem. Ecologists are particularly interested in understanding what happens when an invasive species also happens to be an ecosystem engineer; how are the many interactions between species influenced by the presence of a novel ecosystem engineer?

For her Ph.D research Linsey Haram studied the effects of the invasive red alga Gracilaria vermiculophylla on native estuarine food webs in the Southeast USA. She wanted to know how much biomass this ecosystem engineer contributed to the system, how it decomposed, and what marine invertebrates ate it. She was spending quite a lot of time in Georgia’s knee-deep mud at low tide, and became acquainted with the shorebirds that zipped around her as she worked. She knew that small marine invertebrates are attracted to the seaweed and are abundant on algae-colonized mudflats, and she wondered if the shorebirds were cueing into that. If so, the non-native alga could affect the food web both directly, by providing more food to invertebrate grazers, and indirectly, by providing habitat for marine invertebrates and thus boosting resources for shorebirds.

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A least sandpiper forages on a red algae-colonized mudflat. Credit: Linsey Haram.

Since the early 2000’s, Gracilaria vermiculophylla has dramatically changed estuaries in southeast USA by creating novel habitat on mudflats that had previously been mostly bare, due to high turbidity and a lack of hard surface for algal attachment.  But this red alga has a symbiotic association with a native tubeworm, Diopatra cuprea, that attaches the seaweed to its tube so it can colonize the mudflats.  This creates a more hospitable environment to many different invertebrates, providing cover from heat, drying out, and predators, while also providing food to invertebrates that graze on the algae.

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Closeup view of the red alga Gracilaria vermiculophylla, an invasive ecosystem engineer.  Credit: Linsey Haram

Haram and her colleagues decided to investigate how algae presence might be influencing bird distribution and behavior.  They realized that this influence might be scale-dependent; on a large spatial scale birds may see the algae from afar and be drawn to an algae-rich mudflat, while on a smaller spatial scale, differences in foraging behavior may lead to differences in how a particular species uses the algal patches in comparison to bare patches.

To explore large scale effects, the researchers counted all shorebirds (as viewed from a boat) on 500 meter transects along six bare mudflats and six algal mudflats.  They also measured algal density (even algal mudflats have large patches without algae), and invertebrate distribution and abundance both on the surface and buried within the sediment. These surveys showed that shorebirds, in general, were much more common on algal mudflats. As you can see, this trend was stronger in some shorebird species than others, and one species (graph f below) showed no significant trend.

HaramFig1

Field surveys of shorebird density (#/ha) on six bare mudflats compared to six mudflats colonized by Gracilaria vermiculophylla. * indicates weak trend (0.05 < P < 0.10), ** indicates a stronger difference (P < 0.05).  Bold horizontal bars are median values. Common names of species are (b) dunlin, (c) small sandpipers, (d) ruddy turnstone, (e) black-bellied plover, (f) semipalmated plover, (g) willet, (h) short-billed dowitcher.

Algal mudflats had a much greater abundance and biomass of invertebrates living on the surface, particularly isopods and snails, which presumably attracted some of these birds.  However, below the surface, there were no significant differences in invertebrate abundance and biomass when comparing mudflats with and without algae.

Having shown that on a large spatial scale shorebirds tend to visit algal mudflats, Haram and her colleagues then turned their attention to bird preferences on a smaller spatial scale. First, they conducted experiments on an intermediate scale, observing bird foraging preferences on 10 X 20 plots with or without algae.  They then turned their attention to an even smaller scale, by observing the foraging behavior on a <1mscale.  On each sampling day, the researchers observed individuals of seven different shorebird species on a mudflat with algal patches, to see whether focal birds spent more time foraging on algal patches or bare mud.  During each 3-minute observation, researchers recorded the number of pecks made into algal patches vs. bare mud, and compared that to the expected peck distribution based on the observed ratio of algal-cover to bare mud (which was a ratio of 27:73).

On the smallest scale, two of the species, Calidras minutilla and Aranaria interpres, showed a very strong preferences for foraging in algae, while a third species, Calidris alpine, showed a weak algal preference. In contrast, Calidris species (several species of difficult-to-distinguish sandpipers) and Charadrius semipalmatus strongly preferred foraging in bare mud, while the remaining two species showed no preference.

HaramFig2

Small-scale foraging preferences  (x–axis) of shorebirds. Solid blue curve is the strength of population preference (in terms of probability – y-axis) for mudflats, while solid red curve is the strength of population preference for algae.  Dashed curves are individual preferences.  Red arrows at 0.27 indicates the proportion of the mudflat that is covered with algae, while the blue arrow at 0.73 represents the proportion of bare mudflat (and hence indicate random foraging decisions).  Filled arrows are significantly different from random, shaded arrows are slightly different from random, while unfilled arrows are random. Common names of species are: (a) dunlin, (b) least sandpiper, (c) small sandpipers, (d) ruddy turnstone, (e) semipalmated plover, (f) willet, (g) short-billed dowitcher.

If you compare the two sets of graphs above, you will note that in some cases shorebird preferences for algae are similar across large and small spatial scales, but for other species, these preferences may vary with spatial scale.  For example, Arenaria interpres was attracted to algal mudflats on a large scale, and once present, these birds foraged exclusively amongst the algae, shunning any mud that lacked algae.  Small sandpipers (Calidris species) also were attracted to algal mudflats on a large scale, but in contrast to Arenaria interpres, these sandpipers foraged exclusively in bare mud, rather than in the algae.

The researchers conclude that different species have different habitat preferences across spatial scales in response to Gracilaria vermiculophylla. Most, but not all, species were more attracted to mudflats that harbored the invasive ecosystem engineer.  But once there, shorebird small-scale preference varied in response to species-specific foraging strategy.  For example, the ruddy turnstone (Arenaria interpres) discussed in the previous paragraph, forages by turning over stones (hence its name) shells and clumps of vegetation, eating any invertebrates it uncovers.  Accordingly, it forages primarily in algal clumps.  In contrast, willets (Tringa semipalmata), short-billed dowitchers (Limnodromus griseus) and dunlins (Calidris alpine) were all attracted strongly to algal mudflats, but showed basically random foraging on a small spatial scale, showing little or no preference for algal clumps.  The researchers explain that these three species use their very long beaks to probe deeply beneath the surface, using tactile cues to grab prey. So unlike the ruddy turnstone and some other species that forage for surface invertebrates, they don’t use the algae as a cue that food is available below.  Thus species identity, and consequent morphology, behavior and foraging niche are all important parts of how a community responds to an invasive ecosystem engineer.

note: the paper that describes this research is from the journal Ecology. The reference is Haram, L. E., Kinney, K. A., Sotka, E. E. and Byers, J. E. (2018), Mixed effects of an introduced ecosystem engineer on the foraging behavior and habitat selection of predators. Ecology, 99: 2751-2762. doi:10.1002/ecy.2495. 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.

Intertidal tussles: a shifting balance

As an omnivore with a research-oriented palate, I delight in consuming many different food types.  High on my list are crustaceans – in particular the American lobster, Homarus americanus.

BaillieLobster

A juvenile American lobster, Homarus americanus. Credit: C. Baillie.

However, another crustacean, the invasive Asian shore crab, Hemigrapsus sanguineus, threatens to disrupt my epicurean delight, by interfering with the growth and development of juvenile lobsters in the low intertidal zone in the north Atlantic. Christopher Baillie and Jonathan Grabowski have explored interactions between these lobsters and crabs to unravel how they might be influencing each other.

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The invasive Asian shore crab, Hemigrapsus sanguineus. Credit: Rhode Island Marine and Estuarine Invasive Species Site.

The Asian shore crab was first detected off the New Jersey coast in 1988 and quickly spread from North Carolina to Maine. Their increase has coincided with a sharp decrease in the abundance of their rival green crabs over the same range. Baillie and Grabowski were concerned that the Asian shore crab could also be adversely affecting lobster populations. They did monthly surveys (May-October) of both lobster and crab densities in Dorothy Cove in Masachusetts, USA, between 2013 and 2017, and discovered that crab populations were increasing sharply at the same time that lobster populations were decreasing steadily.

BaillieFig1

Annual average densities of Asian shore crabs (dark gray) and American lobsters (light gray) from surveys at Dorothy Cove, Nahant, Massachusetts, USA, between 2013 and 2017. Error bars are 1 standard error.

The researchers wanted to know whether the increased number of Asian shore crabs was responsible for the lobster decline. Perhaps the two species competed with each other for shelter. Baillie and Grabowski set up experimental tanks, each containing a wire mesh bottom with a rectangular opening cut in the center, so that a burrow could be excavated.  They then introduced a single lobster or crab to the tank, and allowed it to dig a burrow in the cutout center (we’ll call this individual the resident).

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In one shelter experiment, the researchers compared the behavior of larger (mean carapace length = 24.7 cm) and smaller (mean carapace length = 9.3 cm) juvenile lobsters in the presence and absence of a variable number of crabs. They discovered that both larger and smaller lobsters spent most of the time in their burrow when no crabs were in the tank. However, introducing crabs was a major disruptor to their mellow existence, with both lobster size classes being more likely to abandon their residences when crabs were present.

BaillieFig3final

Mean (+ standard error) percentage of time spent in shelter by large juvenile lobsters (top graph) and small juvenile lobsters (bottom graph) in relation to absence (Control) or presence of different numbers of crabs.  Different letters above the bars indicate that the means are statistically different from each other.

The reasons for the decline in residence time were very different for large vs. small lobsters.  In an experiment with one large lobster pitted against one crab, resident lobsters initiated an average of 18.00 attacks against crabs, while resident crabs initiated an average of only 0.20 attacks against lobsters. Even if crabs were allowed to establish residency, when a lobster was introduced, it usually picked a fight with the resident crab. So large resident lobsters left their burrows to challenge intruding crabs. Lobsters managed to kill and eat two intruding crabs.

In contrast, smaller lobsters had a much different experience. Crabs attacked resident small lobsters and were able to displace them from their burrow. This was particularly the case when a greater number of crabs were added to the tank.  When eight crabs were added, the poor lobster was kicked out of its burrow, on average, almost 20 times within a six-hour trial.  Under these conditions, crabs attacked the resident lobster almost 40 times per trial.

BaillieFig4

Crab behavior towards a resident lobster in relation to the number of crabs (heterospecific competitors) introduced into the tank. (A) Mean number of times the lobster is displaced. (B) Mean number of fights initiated by an intruder crab. Error bars are 1 standard error. Different letters above the bars indicate that the means are statistically different from each other.

Baillie and Grabowski also conducted feeding trials – but only with a larger lobster pitted against an individual crab (a blue mussel – a preferred food item for both species – was the prey).  Lobsters were much more successful feeders than crabs, and actually increased their feeding rates in the presence of crabs, presumably having no interest in sharing the mussel with its competitor. Taken together, the shelter and feeding experiments suggest a reversal in dominance structure occurs over the course of lobster development.  The abundant Asian shore crab outcompetes small juvenile lobsters for shelter, but once lobsters attain a certain size, they can outcompete crabs for both shelter and food. We still don’t know, for sure, whether the decline in lobsters in the low intertidal zone at the study site was caused by the increase in crabs; the Asian shore crab may still be expanding its range, so it may be possible to more directly study changes in distribution at other sites both north and south of its current range. Fortunately for lobsters (and for lobster consumers), juveniles can also grow and flourish in deeper ocean waters, where Asian shore crabs are much less of a threat.

note: the paper that describes this research is from the journal Ecology. The reference is Baillie, C. J. and Grabowski, J. H. (2018), Competitive and agonistic interactions between the invasive Asian shore crab and juvenile American lobster. Ecology, 99: 2067-2079. doi:10.1002/ecy.2432. 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.

Mustard musters its troops

North American forests are being invaded. The invading forces use chemical warfare to attack the native inhabitants and to repel counterattacks by hostile enemies. As it turns out, the invader is the humble garlic mustard, Alliaria petiolata, which releases toxic chemical compounds into the soil that reduce the growth rate of many native plant species, and has strong chemical defenses that makes it unpalatable to most herbivores.

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Garlic mustard invasion. Credit Pam Henderson

Lauren Smith-Ramesh wondered why garlic mustard was not even more successful as an invader. Its chemical arsenal should allow it to overrun an area, but she (and many other researchers before her) observed that garlic mustard invasions often decline after a while. As part of her investigations into garlic mustard’s use of chemicals to inhibit native plants, Smith-Ramesh collected seeds from plants from different populations. While shaking these seeds into bags, she noticed that web-building spiders often colonized the garlic mustard’s seed-bearing structure (silique). Were these spiders somehow behind the garlic mustard’s surprising lack-of-success?

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Garlic musard silique with web. Credit Lauren Smith-Ramesh

Spiders can benefit plants in several ways. As important predators in food webs, spiders can kill large numbers of herbivorous insects that might otherwise attack a plant. In addition the decaying corpses of their insect prey can add vital nutrients to soils. Garlic mustard does not enjoy these potential spider-associated benefits, because spiders colonize the garlic mustard after it has already gone into decline, and also because garlic mustard is already well-protected (chemically) against herbivorous insects.

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About 60% of the spiders were this species – Theriodiosoma gemmosum. Credit Tom Murray.

Smith-Ramesh first wanted to understand the relationship between seed structures (siliques) and spider abundance. She established three different types of plots that measured 2 X 2 meters: (1) S+, which had mustards with intact siliques, (2) S-, which had mustards with siliques removed, and (3) N, which had no garlic mustard plants at all in 2015. After several months, she collected all spiders from the middle square meter of each plot. Plots with garlic mustard with intact siliques (S+) had, by far, the highest spider density. S- plots had a somewhat higher spider density than N plots, which Smith-Ramesh attributes to spiders wandering in from just outside the S- plots (which tended to have more silique-bearing garlic mustard plants nearby than did the N plots). Based on this experiment Smith-Ramesh concluded that garlic mustard siliques were dramatically increasing spider density.

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But did increased spider density in S+ plots reduce the number of herbivorous insects, thereby benefiting nearby native plants? Smith-Ramesh set up insect traps that collected insects over two 48 hour time periods – once in August and again in September – in each of the S+, S- and N plots. Both surveys showed fewest herbivorous insects in the S+ plots. This supports Smith-Ramesh’s hypothesis that native plants are benefitting from higher spider density associated with garlic mustard siliques.

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Next, Smith-Ramesh wanted to know whether the decrease in herbivorous insects benefitted native plant growth. To test this directly, she transplanted three types of native plants into her S+, S- and N plots. One of the species, the Hairy Wood Mint Blephilia hirsuta, enjoyed a 50% biomass boost in S+ plots compared to S- plots. The other two native plants species showed very little effect.

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Smith-Ramesh collecting data with three siliques in the foreground. Credit: Lauren Smith-Ramesh.

Garlic mustard plants with intact siliques also benefitted the soils by increasing the amount of available phosphorus by approximately 60%. This phosphorus may have originated with insect carcasses that made their way into the soil and released their nutrients. In theory, soils with higher phosphorus availability could help support the growth of native plants. Smith-Ramesh plans to explore other plant communities that are suffering from different invasive plants, to see whether these invaders are also inadvertently providing resources or conditions that may undermine the success of their invasion.

note: the paper that describes this research is from the journal Ecology. The reference is Smith‐Ramesh, L. M. (2017). Invasive plant alters community and ecosystem dynamics by promoting native predators. Ecology98(3), 751-761. 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.