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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.

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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.

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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)

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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.