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.

Successful scavengers

Scavengers have a bad reputation. They reputedly eat foul smelly stuff, and are too lazy or incompetent to track down prey on their own, depending on “noble” beasts such as lions to kill prey, and then sneaking a few bites when the successful hunters are not looking (or after they’ve stuffed themselves). Of course the reality is that scavenging is simply one way that animals make a living. Many different species, including lions, will scavenge if given the opportunity, and from a human perspective, scavengers provide several important ecosystem services. As one example described by Kelsey Turner and her colleagues, ranchers in parts of Asia gave diclofenac, a non-steroidal anti-inflammatory drug, to their cattle, which had the unintended consequence of killing much of the vulture community. Losing vultures from the scavenging community increased the prevalence of rotting carcasses, which caused feral dog and rat populations to skyrocket, resulting in a sharp increase of human rabies cases in India. The take-home message is that we need to understand what factors influence scavenging behavior and scavenging success.


Golden eagle overwintering in South Carolina scavenges a pig carcass in a clearcut. Credit: Kelsey Turner.

Turner and her colleagues were particularly interested in whether the size of a carcass, the habitat in which an animal dies, and the time of year, influence scavenging dynamics.   The researchers varied carcass size by using three different species: rats (small), rabbits (medium) and pigs (large). Habitats were clearcuts, mature hardwood, immature pine, and mature pine forest. Time of year was divided into two seasons: warm (May – September) and cool (December – March). I should point out that the cool season was mild by many standards, as the research was conducted at the Savannah River Site in South Carolina, with a mean winter temperature of about 10 ° C.


Map of Savannah River Site showing the study sites and diverse habitats.

The researchers collected data by laying down carcasses of varying size in each of the habitats in both summer and winter. Each carcass was observed by a remote sensing camera that captured the scavenging events, allowing the researchers to identify the species of each scavenger and how long it took for the carcass to be detected and consumed.


Two coyotes captured by a remote sensing camera scavenging a pig carcass on a rainy day. Credit: Kelsey Turner.

Scavengers discovered 88.5% of the carcasses placed during the cool season, but only 65.4% of carcasses placed during the warm season. Carcass size was also important, with only 53.9% of rats detected, in contrast to 78.5% of rabbits and 97.8% of pigs detected. But habitat interacted with these general findings: for example scavengers consumed all (23) rabbits in clearcuts, but only about 70% of rabbits placed in the other three habitats.

Detection time also varied with carcass size; in general scavengers found pigs more readily than rats or rabbits. As the graphs below show, this relationship was quite complex. Pigs were detected much more quickly than the smaller carcasses in clearcuts, and somewhat more quickly in mature pine. Additionally, this difference between pigs and the other species is stronger in the warm season (left graph) than in the cool season (right graph). In fact, there is no difference in detection time of pigs, rabbits and rats placed in mature pine during the cool season.


Natural log of mean detection time (in hours) of rat, rabbit and pig carcasses in warm season (left) and cool season (right) in different habitats.  CC = clearcut, HW = mature hardwood, IP = immature pine, MP = mature pine.

Not surprisingly pigs tended to persist longer (before being totally consumed) than the other two species. More strikingly, persistence time for all three species was much greater in the cool season than in the warm season.


Natural log of mean carcass persistence time (in hours) of rat, rabbit and pig carcasses during the cool and warm seasons.

Turner and her colleagues identified 19 different scavenger species; turkey vultures, coyotes, black vultures, Virginia opossums, raccoons and wild pigs were the most frequent. The first scavengers to detect pig carcasses were usually turkey vultures (76.0%) or coyotes (17.3%). An average of 2.8 different species scavenged at pig carcasses, in contrast to 1.5 at rabbit carcasses and 1.04 at rat carcasses. As you might imagine, most scavengers made short work of rat carcasses, so there was not much opportunity for other individuals or species to move in. Carcasses that persisted longer generally had a greater diversity of scavengers; for example, carcasses scavenged by 1, 2 or 3 species persisted, on average, for 90.5 hours, while those scavenged by 4, 5 or 6 species persisted, on average for 216.5 hours.


A flock of turkey vultures in a clearcut surround and scavenge a pig carcass. Credit: Kelsey Turner.

Early ecologists viewed feeding relationships within an ecological community as a linear process in which plants extract nutrients from soils and calories from the air, which they pass onto herbivores and then to carnivores, with considerable energy being lost in each transfer. Now, we use a food web perspective, which considers the essential contributions of scavengers and decomposers (among others) to these feeding relationships. Carcasses decompose much more quickly during the warm season, returning calories and nutrients to lower levels of the food web. Microbial decomposers are, in essence, competing with vertebrates for carcasses, and being metabolically more active in warm months, are able to extract a greater portion of the resources from the carcass than they can during the winter. Slow decomposition in winter allows longer carcass persistence, leading to a greater number and greater diversity of scavengers. As a bonus for those who believe in human primacy, these same scavengers help to create a cleaner and healthier world.

note: the paper that describes this research is from the journal Ecology. The reference is Turner, K. L., Abernethy, E. F., Conner, L. M., Rhodes, O. E. and Beasley, J. C. (2017), Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology, 98: 2413–2424. doi:10.1002/ecy.1930. 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.