Stress frequency structures communities

COVID-19 has amplified our experience of stress, but even in a COVID-free world, we share with most other organisms a continuously stressful existence, highlighted by situations affecting our survival (e.g. getting food and not becoming someone else’s food) and our reproductive success.  Today we will discuss organisms that live in a very stressful environment – the subtidal zone off of the Galapagos islands – located just below the line demarcating the furthest extent of low tide.  One serious stress for subtidal organisms is coping with dramatically fluctuating ocean currents.  The speedy surgeonfish uses its powerful pectoral fins and slender, disc-shaped body to minimize drag, permitting feeding in high flow conditions brought about by powerful ocean waves.  In contrast, the broad-bodied torpedo-shaped parrotfish is unable to do so; for it, fast water is too much of a drag.


Yellowtail surgeonfish (Prionurus laticlavius) stand out as voracious herbivores that can feed even in the most wave-swept coastlines of the Galapagos Islands. Credit: Dr. Alejandro Perez-Matus.

Waters near the Galapagos Islands are enriched by upwelling equatorial currents, which provide nutrients to a diverse community of plankton and benthic (attached to the ocean bottom) algae.  These in turn support a high diversity of macroinvertebrates and herbivorous fish that feed on them, including the pencil urchin, Eucidaris galapagensis, a voracious feeder on algae, barnacles and coral. This species wedges itself among rocks and crevices during the day, and emerges to feed at night.  It attaches itself (and moves very slowly) using its tube feet.  Robert Lamb, Franz Smith and Jon Witman hypothesized that given the weak attachment strength of the pencil urchin’s tube feet, it might only be an effective feeder in locations where wave action was minimal.


Robert Lamb bolts experimental cages to the rock as Eucidaris urchins stand guard at the sheltered side of Caamaño. Credit: Salome Buglass.

To explore how wave action might affect the subtidal community, the researchers set up two research locations at Caamaño and Las Palmas – both off the Galapagos Island of Santa Cruz.


Effect of wave action (exposed – dark bar, sheltered – light bar) on abundance of some of the important members of the subtidal community off of the island of Santa Cruz.


At each location, they chose an exposed site with strong wave action and a sheltered site that had much reduced wave action.  Mean flow speed was more than twice as fast at exposed sites than in sheltered sites. As you can see in the figure to your left, site differences in mean flow speed corresponded to differences in the subtidal community. Crustose coralline algae (red algae firmly attached to corals) were more common in sheltered sites (Figure A), while a variety of red and green macroalgae were more common at exposed sites (Figure B).  Surgeonfish (Figure C) and parrotfish (Figure D) were much more abundant in exposed areas, while pencil urchins were much more abundant in sheltered sites (Figure E).






Lamb and his colleagues wanted to know why these differences exist. They set up a series of exclosures within each of these sites using wire mesh cages to either allow fish, but not urchins (+ fish treatment), allow urchins but not fish (+ urchins), or exclude both groups of herbivores (- all).  They also had a control treatment that allowed all herbivores (+ all).


In one experiment the researchers created sandwiches made up of the delectable green algae Ulva.  For five days, they ran six replicates of each treatment at exposed and sheltered sites at Caamaño and Las Palmas. Lamb and his colleagues then harvested the sandwiches, weighed them, and calculated the percent remaining of each sandwich.


An Ulva sandwich

At exposed locations, urchins (without fish) consumed very little Ulva, while fish (without urchins) consumed about 2/3 of the Ulva (when compared to the –all controls). In contrast, at sheltered locations, urchins took some mighty significant bites from the Ulva sandwiches, while fish also ate substantial Ulva at Caamaño, but not at Las Palmas.


Percent of Ulva biomass remaining after five days of the Ulva sandwich experiment. Error bars are 1 SE.

In a related experiment, the researchers used the same cages to explore how macroalgal communities assemble themselves in the presence or absence of urchin and fish herbiores under different flow rates.  If this was not enough to consider, they also ran these experiments both during the cool season, when nutrient-rich ocean currents lead to high production, and during the warm season when production is usually lower.  Lamb and his colleagues bolted two 13 X 13 cm polycarbonate plates to the bottom of each cage, and after two months measured the abundance and type of algae that colonized each plate.

Several trends emerge.  First, macroalgae colonized much more effectively during the cool season.  Second, urchins profoundly reduced macroalgal colonization at sheltered sites, but had little effect at exposed sites.  In contrast, fish herbivory reduced macroalgal colonization at exposed sites at Caamaño but not Las Palmas, during the warm and cool season.


Effect of herbivores on macroalgal community assembly, as measured by amount of algae colonizing the polycarbonate plates after two weeks.

In addition, the researchers set up video cameras and were able to document herbivory by 17 fish species, with drastically higher herbivory rates at exposed sites.

Lamb and his colleagues conclude that the dominant herbivores switched between urchins in low flow sites and fish in exposed sites. Fish can leave the resource patch when stress (flow rate) is unusually high, and return when flow rate drops, while the slow-moving pencil urchins do not have that option. The researchers argue that in many ecosystems, consumer mobility in relation to the frequency of environmental stress can predict how consumers influence community structure and assembly.  They point out that the coupling of mobility effects with environmental stress is common throughout the natural world.  As examples, many shorebirds feed on marine organisms that become available during low tides, or also between crashing waves.  Large mammals in Africa can migrate long distances to escape drought-stricken areas, while smaller animals cannot undertake such long journeys.  In locally acidic regions of the Mediterranean Sea, many fish species can enter, feed and leave before experiencing toxic effects from the acid water, while slow-moving urchins are excluded from feeding in those habitats. Thus, while extreme environmental stress often decreases consumer activity, there are also times when it doesn’t.  In these cases, we need to understand how particular species will behave and perform in the stressful environment to predict how stress influences community structure and functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Lamb, R. W.,  Smith, F., and  Witman, J. D..  2020.  Consumer mobility predicts impacts of herbivory across an environmental stress gradient. Ecology  101( 1):e02910. 10.1002/ecy.2910. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2020 by the Ecological Society of America. All rights reserved.

Girl and boy flowers support different microbe communities.

Most of us are accustomed to thinking about sexual dimorphism in animals.  Male lions have manes, and male deer have antlers and generally larger bodies than female deer.  In many species, male birds have more complex sings and more colorful plumage. Perhaps less familiar is that female insects are generally larger than males of the same species.  But many of us are unaware that sexual dimorphism exists in some plant species as well.

As a child, Kaoru Tsuji spent considerable time watching insects on plants.  Later, as an undergraduate at Kyoto University in Japan, she noticed that larvae of a particular geometrid moth only visited male Eurya japonica plants, but not females. This led to her graduate work on how plant sexes affect herbivorous insects, and later, more broadly, on how plant sexual dimorphism affects other species in the community.


Kaoru Tsuji gazes at female Eurya emarginata plant. Credit: Noriyo Tsuji.

At the 2014 Ecological Society of America meetings, Tsuji heard Tadashi Fukami talk about microbial communities in flower nectar, and realized that she could learn to apply Fukami’s techniques to the microbial communities living within Eurya flowers.  After working three months in Tadashi’s lab, Tsuji was now ready to explore whether two plant species, Eurya japonica and Eurya emarginata, host different communities of bacteria and fungi in the flowers of male and female plants.


Male and female flowers of the two study species visited by pollinators.  These photos are not to scale; in actuality the male flower is substantially larger.  You can get a sense of this by noting that the same insect pollinator, the fly Stomorhina obsoleta, is pictured in figure a and near the top left of figure b.

For both species, male flowers tend to be larger, while female flowers tend to have sweeter nectar. Higher sugar levels will increase the chemical stress experienced by microbial organisms living in the nectar. Because the inside of a microbial cell has a lower sugar concentration (and thus a higher water concentration) than the sugar rich nectar environment, water tends to leave the microbial cell, leading to severe dehydration. Thus Tsuji and Fukami expected to find lower microbial abundance in female flower nectar.

Complicating this situation, animal visitors, such as bees and flies, also influence the microbial community in at least two ways.  First, many nectar-colonizing microbes depend on animals to disperse them to new flowers. Second, the interaction of nectar production, water evaporation and consumption by bees and flies can change the concentration of sugar in the nectar.  If there are few (or no) animals drinking the nectar, water will evaporate, sugar will remain, and the nectar will become more and more concentrated (sweeter) as more nectar is secreted over time.  But if nectar gets consumed, the new secretions will simply replace the old nectar, and sugar levels should be relatively constant. Thus flowers without animal visitors should impose more chemical stress on microorganisms by virtue of being sweeter.

The researchers sampled nectar from 1736 flowers, and grew the nectar microbes on agar plates supplied with nutrients that would support either bacterial or fungal growth.  In addition, the researchers also placed small-mesh bags over a subset of these flowers (before they opened), to reduce animal visitation.  After five days they counted the number of colonies formed, to estimate microbial abundance. Unfortunately, microbes were rarely found in E. japonica, so most of the data are for E. emarginata flowers only.


Female flowers of Eurya emarginata visited by a fly, Stomorhina obsoleta. Agar plates showing isolated colonies of nectar-colonizing microbes are superimposed. Left and right plates have yeast and bacterial colonies, respecitevly, both isolated from E. emarginata nectar. Credit: Kaoru Tsuji and Yuichiro Kanzaki.

First, as expected, female flowers had higher nectar sugar levels than did male flowers (the Brix value measures sucrose concentration).  In addition, putting a fine mesh bag over the buds substantially increased sugar levels in nectar from flowers of both sexes.


Sucrose (Brix) concentration of exposed and bagged E. emarginata flowers of both sexes.  For box plots, the dark horizontal bar is the median value, while the box encloses the 25th and 75th percentile.

The proportion of flowers in which fungi and bacteria were detected was much greater in male flowers than in female flowers.  In male flowers only, bagging the flowers decreased fungal frequency but not bacteria frequency.


The proportion of exposed and bagged E. emarginata flowers whose nectar, when cultured in the appropriate medium, generated fungal colonies (top graph) and bacterial colonies (bottom graph).

The researchers used colony forming units (CFUs) – the number of viable colonies on the agar plate – as their measure of bacterial abundance.


Abundance of fungi (top) and bacteria (bottom) cultured in agar plates, that were swabbed with nectar derived from exposed and bagged E. emarginata flowers of both sexes. Note that the y-axis is log10 CFUs, so an increase from 3 to 4 (for example) is actually a tenfold increase in number of CFUs.

As expected, fungi were less abundant in female flower nectar than in male flower nectar.  In addition, bagging the flowers substantially reduced fungal abundance. Bacteria were also less abundant in female flower nectar than in male flower nectar.  Surprisingly, bagging the flowers substantially increased bacterial abundance, despite the increased chemical stress and decreased visitation by animal visitors.

Why did bacterial abundance increase when flowers were bagged?  The researchers hypothesize that reduced fungal dispersal from bagging caused competitive release of bacteria from the fungi.  Presumably the fungi and bacteria compete for essential resources (such as amino acids) in the nectar.  Because the bags reduce fungal abundance, there are fewer fungi to out-compete the bacteria, leading to an increase in bacterial abundance.

The researchers used DNA analysis to characterize which microbial species were found in female vs. male flowers.  They discovered major differences in species composition between the sexes.  Taken together with the data on frequency and abundance, it is clear that sexual dimorphism in these plants influences microbial communities in significant ways.  Tsuji and Fukami suggest that sexual dimorphism in many species may have profound community-wide consequences that researchers are only beginning to understand and uncover.

note: the paper that describes this research is from the journal Ecology. The reference is Tsuji, K. and Fukami, T. (2018), Community‐wide consequences of sexual dimorphism: evidence from nectar microbes in dioecious plants. Ecology, 99: 2476-2484. doi:10.1002/ecy.2494. 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.