Tropical trophic cascade slows decomposers

In the rough and tumble natural world, consumers such as lions, lady bugs, llamas and lizards get most of the press, while producers such as peas, pumpkins and phytoplankton come in a close second.  Consumers earn their name because they get their energy from consuming other organisms, while producers produce their own energy (using photosynthesis or chemosynthesis) from inorganic molecules.  Often ignored in this ecosystem structural scheme are decomposers, which get their energy from breaking down the tissue of dead organisms.  They should not be ignored.  Much of the energy transferred through ecosystems passes through decomposers.

One reason they are overlooked is that most decomposers are tiny. Some of the largest decomposers are detritivores, which actually eat the dead materials (detritus), in contrast to other microbial decomposers such as bacteria and fungi.  Shredders are detritivores commonly found in streams and rivers; these aquatic insects eat portions of dead leaves and, in the process, shred them into much smaller pieces that energize other decomposers. Many researchers had noted that shredders were relatively rare in tropical streams, in part because there are many other larger consumers in the ecosystem that are willing to eat dead leaves and any shredders associated with them. Thus Troy Simon and his colleagues expected that shredders, such as the caddisfly, Phylloicus hansoni, would play, at best, a minor role in the streams they studied in the Northern Range Mountains in Trinidad.

stream

A typical headwater stream located in the Northern Range mountains of Trinidad. Waterfalls in the uppermost reaches of these streams act as a barrier to the upstream movement of guppies, but not killifish and crabs, which can move over land during periods of heavy rain. Credit: Joshua Goldberg.

We will discuss interactions between several species in these aquatic systems.  Trees are important producers as they shed leaves into the streams; these leaves are broken down by shredders such as the aforementioned caddisflies and also microbial decomposers.   The major consumers are omnivorous crabs, Eudaniela garmani, which eat leaves and caddisflies (and many other items), and two fish species. Killifish, Anablepsoides hartii, eat caddisflies, other invertebrates and also the occasional small fish (including fish eggs).

killifish

Hart’s killifish (Anablepsoides hartii) are primarily insectivorous and major consumers of leaf‐shredding caddisflies. Credit: Pierson Hill.

Guppies, Poecilia reticulata, are much smaller than killifish, maxing out at 32 mm long in comparison to the killifish maximum length of 100 mm.  But guppies are much more omnivorous, feeding on leaves, leaf-shredding insects and even killifish eggs and larvae.

guppies

Male (left) and female (right) Trinidadian guppy (Poecilia reticulata). Guppies are omnivorous, feeding broadly on detritus as well as plant and animal prey, including young killifish. Credit: Pierson Hill.

Amazingly, killifish can disperse over land, as can crabs (less amazingly).  This allows them to bypass barrier waterfalls during wet periods, which results in them being the only large consumer species above waterfalls in many Trinidad streams.  Guppies lack killifish dispersal abilities, so they are often confined to stream reaches below significant waterfalls.  These species, and their consumption patterns are highlighted in the figure below.

SimonFig1

Diagram of the two detrital-based food webs.  Above the waterfall is the KC reach, named after its two important consumers, killifish and crabs.  Below the waterfalls is the KCG reach, named after its three important consumers, killifish, crabs and guppies. Arrows show direction of energy flow within the ecosystem.

Simon and his colleagues wanted to know how interactions among all of these species influenced the rate of leaf decomposition.  The researchers constructed identical-size leaf packs of recently fallen leaves of the Guarumo tree, Cercropia peltata, and attached them to copper wire frames within each reach of the stream.  They periodically harvested a subset of the packs and measured the amount of decomposition by drying and weighing the leaves, and comparing this weight to the starting weight of the leaf pack.  In addition, they collected all invertebrates > 1 mm long from each leaf pack and identified them to species or genus.

To control the consumers involved in each interaction, Simon and his colleagues constructed underwater electric exclosures which created an electric field that convinced all fish and crabs to exit (and stay out) within 30 seconds of being turned on, but did not influence invertebrates in any detectable way.  Killifish are active day and night, guppies only during the day, and the researchers believed that crabs were active primarily at night. The researchers set up four treatments: control (C) with 24 hour access to consumers, experimental (E) with 24 hour exclusion of consumers, day-only exclusion (D) and night-only exclusion (N).  The researchers expected that the day-only exclusion treatments would selectively exclude guppies, while night-only exclusion would selectively exclude crabs. They then placed the leaf packs into each exclosure, turned on the current, and ran the experiment for 29 days.  Five replicates of each treatment were done above and below the waterfalls.

simonexperiment

Electric exclosures established in the stream. Leaf packs were tied to the copper frame and periodically harvested over the 29 days of the experiment. Rectangular tiles shown in treatment frames were part of a separate study. Credit: Troy N. Simon.

We’re finally ready for some data.  The two graphs on the left represent the downstream reach below the waterfalls, where killifish, crabs and guppies are naturally present (KCG).  The two graphs on the right represent the upstream reach above the falls, where only killifish and crabs are naturally present.  There was no evidence in the downstream reach that excluding consumers influenced decomposition rates (top left graph).  However, when consumers were present (C treatment) in the upstream reach, decomposition rates were reduced by about 40% in comparison to treatments when consumers were partially (D and N) or completely (E) excluded (top right graph).

SimonFig3

Mean (+SE) for (a,b) decay rate of Cecropia peltata leaves (percentage of mass lost per day) and (c,d)  biomass of Phylloicus hansoni (milligrams of dry mass per gram of Cecropia). 24-hour treatments allow full macroconsumer access [control (C)] or completely exclude macroconsumers [electric (E)]. Twelve-hour treatments exclude access to either diurnally active [day (D)] or nocturnally active [night (N)] macroconsumers. Different letters above the bars indicate statistically significant differences between the treatments.

The two bottom graphs above look at the biomass of the caddisfly, Phylloicus hansoni, which was easily the most abundant macroinvertebrate within the leaf packs.  There was no significant difference in caddisfly abundance below the waterfall regardless of treatment (bottom left graph above).  Above the waterfalls, caddisfly abundance was severely depressed in the controls (C) where killifish were free to feed on them (bottom right graph).

One piece of evidence that killifish ate caddisflies and depressed their abundance was that surviving caddisflies were much smaller in the control treatment leaf packs than in any of the experimental treatment leaf packs.  This suggests that  killifish with unimpeded access to caddisflies were picking off the largest individuals.

SimonFig4

Mean (+SE) caddisfly length in mm (y-axis) for each treatment, 

These findings support the hypothesis that a trophic cascade prevails in the KC reach, in which killifish eat caddisflies, thereby slowing down decomposition. But in the KCG reach, guppies eat killifish eggs and larvae and compete with them for resources, thereby reducing killifish abundance, and interfering with the establishment of a trophic cascade.

Lastly, the researchers explored whether the same trophic cascade operated in upper reaches but not in lower reaches of other streams in the area. Surveys of six streams indicate a definite “yes” answer, with Cecropia decay rate and caddisfly biomass much lower in the upper reaches.

SimonFig6

(Top) Mean (+SE) decay rate for Cecropia peltata
leaves (percentage of mass lost per day) and (b) caddisfly biomass (milligrams of dry mass per gram of Cecropia) in the landscape study (n = 6 streams). Different letters above bars indicate statistically significant differences  between treatments.

Surveys of each stream indicated that killifish were much more abundant in the upper reaches where guppies were not found, but guppies were much more prevalent in the lower reaches than were killifish.  These findings indicate that this detrital-based trophic cascade, with killifish eating caddisflies and thereby slowing down decomposition, is a general pattern in the upper reaches of these tropical streams.  However, Simon and his colleagues caution us that different streams will have different groups of organisms playing different ecological roles.  Thus the presence of detrital-based trophic cascades will depend on the particulars of which species are present and how abundant they are in a particular stream.

note: the paper that describes this research is from the journal Ecology. The reference is Simon, T. N., A. J. Binderup, A. S. Flecker, J. F. Gilliam, M. C. Marshall, S. A. Thomas, J. Travis, D. N. Reznick, and C. M. Pringle. 2019. Landscape patterns in top-down control of decomposition: omnivory disrupts a tropical detrital-based trophic cascade. Ecology 100(7):e02723. 10.1002/ecy.2723. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

 

Mystifying trophic cascades

Within ecosystems, trophic cascades may occur when one species, usually a predator, has a negative effect on a second species (its prey), thereby having a positive effect on its prey’s prey. Today’s example considers the interaction between a group of predators (including several fish species, a sea snail and a sea star) their prey (the sea urchin Paracentrotus lividus) and sea urchin prey, which comprise numerous species of macroalgae that attach to the shallow ocean floor. These predators can negatively affect sea urchin populations either by eating them (consumptive effects), or by scaring them so they forage less efficiently (nonconsumptive effects). If sea urchins are less abundant or less aggressive foragers, the net indirect effect of a large population of fish, sea snails and sea stars will be an increase in macroalgal abundance.

Maldonado Halo

A large sea urchin grazing in a macroalgal community.  Notice the white halo surrounding the urchin, indicating that it has grazed all of the algae within that region. Credit: Albert Pessarrodona.

Many humans enjoy eating predatory fish, and we have overfished much of the ocean’s best fisheries including the shallow temperate rocky reefs (4 – 12 m deep) in the northwest Mediterranean Sea. Removing these predators has caused sea urchin populations to explode, overgrazing their favorite macroalgal food source, and ultimately leading to the formation of urchin barrens – large areas with little algal growth, low productivity and a small nondiverse assemblage of invertebrates and vertebrates.

DCIM112GOPRO

A sea urchin barrens whose macroalgae have been overgrazed by sea urchins. Credit: Albert Pessarrodona

Albert Pessarrodona became interested in this trophic cascade after years of diving in the Mediterranean. He noticed that in Marine Protected Areas, predatory fish abound and there are few visible urchins and lots of macroalgae. In nearby unprotected areas where fishing is permitted, urchins graze out in the open brazenly, and urchin barrens are common. He also wondered whether a second variable – sea urchin size – might play a role in this dynamic. Were large sea urchins relatively immune from predation by virtue of their large size and long spines, allowing them to forage out in the open even if predators were relatively common?

Urchinfig1

Interactions investigated in this study.  (a) Predators consume either small (left) or large (right) sea urchins (consumptive effects). (b) Sea urchins eat macroalgae. (c) Predators scare small or large sea urchins, reducing their foraging efficiency (nonconsumptive effects). (d) Predatory fish indirectly increase macroalgal abundance.

Pessarrodona and his research team used field and laboratory experiments to explore the relationship between sea urchin size and their survival and behavior in high-predator-risk and low-predator-risk conditions. High-risk was the Medes Islands Marine Reserve, which has had no fishing since 1983 and boasts a large, diverse assemblage of predatory fish, while low-risk was the nearby Montgri coast, which has a similar habitat structure, but allows fishing. The researchers tethered 40 urchins of varying sizes to the sea bottom (about 5m deep) in each of these regions, left them for 24 hours, and then collected the survivors to compare survival in relation to body size in high and low-risk conditions. They discovered that large urchins were much less likely to get eaten than were small urchins, and that the probability of getting eaten was substantially greater in the high-risk site.

UrchinFig3a

Probability of being eaten in relation to sea urchin size (cm) in high-risk (blue line) and low-risk (green line) habitats.

Pessarrodona and his colleagues followed this up by investigating whether the relatively predation-resistant large urchins were less fearful, and thus more likely to forage effectively, even in high-risk sites. Previous studies showed that sea urchins can evaluate risk using chemical cues given off by other urchins injured in a predatory attack, or given off by the actual predators. To explore the relationship between these cues and sea urchin behavior, the researchers put either large or small sea urchins into partitioned tanks with an injured sea urchin. Water flowed from one partition to the other, so the experimental sea urchins received chemical cues from the injured urchins. They also had a group of sea urchins placed in similar tanks without any injured sea urchins as controls. The experimental sea urchins were given seagrass to feed on, and the researchers calculated feeding rates based on how much food remained after seven days.

Small sea urchins were not deterred by the presence of an injured urchin (left graph below), while large sea urchins drastically reduced their feeding rates in response to the presence of an injured urchin (middle graph). This was startling as it flew in the face of the commonsense expectation that small sea urchins (most susceptible to predation) should be most fearful of predator cues. The researchers repeated the experiment (under slightly different conditions) placing an actual predator (a fearsome sea snail) on the other side of the partition. Again, large urchins showed drastically reduced foraging rates (right graph below).

UrchinFig4

Sea urchin responses to predation risk cues in the laboratory. When exposed to injured urchins – symbolized as having a triangle cut out – (A) small urchins did not reduce their grazing rate, while (B) large urchins drastically curtailed grazing. (C) When exposed to a predatory snail on the other side of a partition, large urchins sharply curtailed grazing. n.s = no significant difference, **P<0.01.

It turns out that large sea urchins are the critical players in this trophic cascade because they do much more damage to algal biomass than do the smaller urchins (we won’t go through the details of that research). The question then becomes how this plays out in natural ecosystems. Do consumptive and non-consumptive effects of predators in high-risk sites reduce sea urchin abundance and reduce the foraging levels of large sea urchins so that macroalgal cover is greatly enhanced? Pessarrodona and his colleagues surveyed high-risk and low-risk sites for sea urchin density and algal abundance. They set up 45 quadrats (40 X 40 cm) at each site, measured each sea urchin’s diameter, and estimated the abundance of each type of algae by harvesting a 20 X 20 cm subsample from each quadrat and drying and weighing the sample.

The findings were striking. Small and large sea urchins were much less abundant at high-risk sites than at low-risk sites (left graph below). At the same time, macroalgae were much more abundant at high-risk sites than at low-risk sites (right graph below).

UrchinFig5bc

(Left graph) Density of small and large sea urchins in high-risk and low-risk habitats. (Right graph) Biomass of macroalgae of different growth structures in high-risk and low-risk habitats. Canopy algae are taller than 10 cm, while turf algae are lower stature. Codium algae are generally not grazed by sea urchins. **P<0.01, ***P<0.001.

UrchinFig6a

Summary of interactions.  Arrow width indicates relative importance.

To summarize this system, predators reduce small sea urchin abundance by eating them (consumptive effects), and reduce large sea urchin foraging by intimidating them (nonconsumptive effects). The net indirect effect of predators on macroalgae is a function of these two effects. Large sea urchins are the major macroalgae consumers, but, of course, large sea urchins develop from small sea urchins.

The $64 question is why large sea urchins fear predators so much, while small (more vulnerable) urchins do not. The quick answer is that we don’t know. One possibility is that small sea urchins may be bolder in risky environments since they are more vulnerable to starvation (have fewer reserves), and also have lower reproductive potential since they are likely to die before they get large enough to reproduce. In contrast, large sea urchins can survive many days without food because of their large reserves. In addition, large urchins are close to sexual maturity, and thus may be unwilling to accept even a small risk to their well-being, which could interfere with them achieving reproductive success.

note: the paper that describes this research is from the journal Ecology. The reference is Pessarrodona, A.,  Boada, J.,  Pagès, J. F.,  Arthur, R., and  Alcoverro, T. 2019.  Consumptive and non‐consumptive effects of predators vary with the ontogeny of their prey. Ecology  100( 5):e02649. 10.1002/ecy.2649. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

Invasive crayfish hit the self-destruct button

One important feature of a biological invasion is that invaders can change an entire ecosystem in a substantial way.  A possible outcome of this change is that, in theory, an invasive species could inadvertently make an ecosystem less suitable as a habitat for itself.  Does this happen, and if so, under what circumstances?  One reason invasive species are so successful is that they usually can increase in population size very quickly.  Ecologists have discovered that species with the potential to increase very quickly may also have the potential to decline equally rapidly and then increase again, going through repeated boom-bust cycles of population size.  Thus if an invasive species starts to decline, it does not always mean that this decline will continue over time. Consequently, monitoring a biological invasion for only a few years may give a misleading picture of long-term prognosis for the invasive species and the ecosystem.

Eric Larson was able to address these problems when he began his postdoctoral research with David Lodge at the University of Notre Dame in 2014. Lodge (and John Magnuson before him) has studied the rusty crayfish (Faxonius rusticus) invasion in 17 northern Wisconsin lakes since the 1970s, using the same bait (beef liver) and the same traps on the same days each year.

Gantz_BeefLiver

Crysta Gantz prepares to bait a trap with beef liver, which the crayfish love, but she – not so much! Credit: Eric R. Larson.

Three graduate students (the other co-authors of the paper) had continued data collection and done extensive mapping of the lake bottoms.  When Larson joined the research program he had about 40 years of data and 17 well-described lakes.  He knew that rusty crayfish were declining in some lakes and not others, and he and his colleagues were ready to explore whether these declines could be tied in to some environmental variable that the crayfish were influencing in some lakes, but not others.

AllequashLake

Allequash Lake. Credit Eric R. Larson

As an avid fisherman (more in my mind than in actuality), I have, on many occasions, caught a nice bass only to have it regurgitate the contents of its stomach, which usually includes bits of crayfish.  As it turns out, predacious fish such as bass love to eat crayfish, and crayfish are more likely to survive in environments that provide hiding places such as rocks or luxurious macroalgae that grow in sand or muck. The problem is that crayfish enjoy dining on macroalgae, so they can do themselves a disservice by eating their shelter from predators, effectively changing their environment so that their invasion is no longer sustainable.  Does this actually happen?

rusty_crayfish

Two rusty crayfish discuss the issues of the day. Credit: Eric R. Larson.

Larson and his colleagues continued collecting data on 17 lakes, and used their long-term data set to evaluate whether rusty crayfish populations were not declining (steady or increasing), declining or occupying an ambiguous gray zone where there was no clear trend in how the population was changing. The analysis showed that three lakes were not declining since the rusty crayfish invasion, eight lakes had declined substantially and six lakes were ambiguous.

LarsenFig1

The researchers turned their attention to the lake-bottom substrate.  Were rusty crayfish more successful in rocky bottom lakes that gave them continuous predator protection?  Their analysis indicated that the three lakes where the invasion was going strong had the rockiest substrate, while the eight lakes experiencing population declines after the rust crayfish invasion were significantly less rocky.

LarsenFig2

Proportion rocky substrate in lakes whose rusty crayfish populations are in decline (red), have an ambiguous trend (black) or are not in decline (blue). The horizontal line within each box is the median value, box bottom and top are 25th and 75th percentile, and whiskers are the 10th and 90th percentile. Non-overlapping letters above the bars (a and b) indicate significant differences between the groups.

The researchers conclude that in the absence of rocky substrate, the rusty crayfish is eating the aquatic macrophytes that grow from the sandy lake bottom, thereby exposing itself to predators.  Larson and his colleagues recommend simultaneous surveys of crayfish populations and density of aquatic macrophytes to see whether lakes may oscillate between states dominated by one or the other.

rusty_trap1

Captured crayfish. Photo Eric R. Larson

Researchers want to know how commonly invasive species modify habitat in a self-destructive way.  A literature review of invasive species declines failed to find much evidence, but there are not enough long-term data sets to get a sense of how frequently this occurs. The problem is that researchers need to monitor the invasive species population and the relevant habitat variables for an extended time period.  The jury is still out on this question and only time (and careful data collection) will tell.

note: the paper that describes this research is from the journal Ecology. The reference is Larson, E. R.,  Kreps, T. A.,  Peters, B.,  Peters, J. A., and  Lodge, D. M.  2019.  Habitat explains patterns of population decline for an invasive crayfish. Ecology  100( 5):e02659. 10.1002/ecy.2659. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

A saltier Great Salt Lake supports a shifting ecosystem

In science, like many other fields, “who you know” can be critical to success. Eric Boyd from Montana State University was introduced to the Great Salt Lake (GSL) ecosystem by his colleague Bonnie Baxter, a professor at Westminster College and the Great Salt Lake Institute in Salt Lake City, Utah.  Baxter was fascinated by microbialites- deposits of carbonate mud of diverse shape and structure, that harbor an impressive diversity and abundance of microorganisms.  Some of these microorganisms are photosynthetic, using dissolved organic carbon from the water to build carbohydrates; as such they are the primary producers which feed the rest of the ecosystem. Baxter impressed upon Boyd the need to understand the ecosystem, which feeds huge populations of two consumer species, the brine fly Ephydra gracilis and the brine shrimp Artemia franciscana. Up to 10 million birds, representing about 250 species, feed on these two species over the course of a year.

dsc_0279.jpg

Eric Boyd collects samples from the north arm of GSL. Credit: Bonnie Baxter.

In 1959 a railroad causeway was built that divided GSL into a south and north arm, which differ from each other in one critical way.  The south arm receives freshwater input from three rivers, while the north arm’s only freshwater input is rain and snowmelt.  Both arms are hypersaline; the south arm is 4-5 times saltier than typical ocean water, while the north arm is about twice as salty as the south arm. Boyd and Baxter recognized that these salinity differences were probably impacting the microbial communities in the two arms; in fact preliminary observations indicated that microbialite communities were no longer forming in the north arm.  So when Melody Lindsay began her doctoral research with Boyd, she elected to investigate how salinity was influencing the microbialite communities in the lake.

DSC_0040

Melody Lindsay (right) and Bonnie Baxter (left) planning to sample in the south arm of GSL.  Credit: Jaimi Butler.

Lindsay and her colleagues collected samples of microbialite mats from the south arm of the lake where the salinity of the water measured 15.6% (as a comparison, typical ocean water is about 3.5%).  At each of six salinity levels (8, 10, 15, 20, 25 and 30%), the researchers set up three microcosms of 150 ml of lakewater, which they then inoculated with 10 grams of homogenized microbial mat. They then sampled microbial diversity and abundance four and seven weeks after beginning the experiment.

DSC_0033

Exposed microbialites along the south arm’s shoreline.  Credit: Eric Boyd.

This experiment was conceptually simple, but technically a bit of a challenge.  Microorganisms are difficult to identify and count; and in fact it is likely that some of the species were new to science. Fortunately, researchers can use molecular approaches (quantitative PCR) to measure the quantity of each type of 16S rRNA gene in each microcosm. Each species of microorganism has distinct rRNA genes, so different base sequences indicate different microorganisms.  This allows researchers to estimate how much of each species is present. One restriction is that closely related species will have almost identical rRNA genes, so they may be difficult to distinguish from each other.

Overall, microorganism abundance was 152% greater after four weeks and 128% greater after seven weeks at the 15% salinity. Recall that these samples came from microbialites associated with 15.6% salinity, so this finding indicates good growth at the salinity which the microorganisms have recently experienced.  Interestingly, microorganisms thrived even better at 10% salinity.  But higher salinity levels, particularly  25% and 30%, were very detrimental to microbial growth.

LindsayFig2

Change in abundance of 16S rRNA gene from microcosms incubated for four and seven seeks in comparison to abundance at week 0 for each salinity.  Significant differences are comparisons with abundance at week 0. NS = no significant difference, * P<0.1, ** P<0.01, *** P<0.001, **** P<0.0001. Error bars = 1SE.

The researchers broke down their results into taxonomic Orders, based on the 16S rRNA sequence of each gene. The two most common Orders were Sphingobacteriales and Spirochaetales, which both grew best at low salinity. The next most common Orders were a cyanobacterium from the Order Croococcales, and an alga from the Order Naviculales.  Species from these two taxonomic Orders are foundational to the ecosystem, because they are photosynthetic and relatively large. These dominant producers either directly, or indirectly, feed the rest of the ecosystem. Croococcales grew best at intermediate salinities (10-20%), while Naviculales did best at 8-15%, but also reasonably well at 20% salinity (see the figure below for a summary of the most common Orders).

LindsayFig3

Abundance of taxonomic Orders of Microorganisms incubated at different salinities at 4 and 7 weeks, in comparison to initial abundance (week 0 = yellow square). Darker green squares indicate a greater increase, and darker brown squares indicate a greater decrease in abundance.  The most common Orders are on top, least common are on the bottom. Het = heterotroph, PP = primary producers, PhH = photoheterotroph.

Overall, primary productivity, as measured by how much dissolved organic carbon was taken up by the photosynthesizers, was greatest at 10 and 15%, and declined sharply above 20% salinity.  In addition, brine shrimp, one of the two important animal consumers of microorganisms, hatched and survived best at the lowest salinities.

Mating brine shrimpHans Hillewaert

Two mating brine shrimp under the watchful eyes of an observer. Credit: Hans Hillewaert.

Lindsay and her colleagues conclude that conditions in the south arm are conducive to microbialite communities and the consumers they support.  However, the north arm has much lower productivity, with salinity levels so high that salt is spontaneously crystalizing out of solution in some areas. Given that climate change models predict increased drought severity over the next century in the GSL region, it is very likely that salinity levels will rise throughout the lake.  Over the same time period, humans are expected to increase water usage from the rivers that flow into the lake, which will further drop water levels in the lake, increase salinity in GSL, and dry out many of the microbial mats. This loss of ecosystem production is expected to cascade up the ecosystem, reduce brine shrimp abundance and ultimately the abundance and diversity of migratory birds that feed on them.

note: the paper that describes this research is from the journal Ecology. The reference is Lindsay, M. R.,  Johnston, R. E.,  Baxter, B. K., and  Boyd, E. S.  2019.  Effects of salinity on microbialite‐associated production in Great Salt Lake, Utah. Ecology  100( 3):e02611. 10.1002/ecy.2611. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

Fewer infections found in forest fragments

As human populations expand, we are converting ecosystems from one state to another.  In the case of tropical forests, conversion of forest to cropland may leave behind fragments of relatively undisturbed forest surrounded by a matrix of cropland or other forms of development.  Conservation ecologists are exploring whether ecological processes and ecosystem structure in these fragments work pretty much like normal forested regions, or whether fragments behave differently.  To do this, in a few locations around the world such as the Wog Wog Fragmentation Experiment in New South Wales, Australia, researchers have systematically created forest fragments of various sizes.  They can then ask a variety of questions comparing fragments vs. intact forest. For example,  how does species diversity, or how do processes such as competition, predation and mutualism differ in the two landscapes?

aerial photo2

Aerial photo of Wog Wog Fragmentation Experiment at the time the experiment began in 1987. Credit: Chris Margules.

Julian Resasco was working as a postdoctoral associate in Kendi Davies’ lab at the University of Colorado on a study that looked at changes in invertebrate communities in response to fragmentation at Wog Wog. Beginning in 1985, researchers had set up a network of pitfall traps, which are cups that are buried with their tops level to the ground, so that any careless organism that wanders in will be trapped in the cup.  Some pale-flecked garden skinks, Lampropholis guichenoti, also had the misfortune to become entrapped and became subjects for the study. The invertebrates, and the 186 unfortunate skinks were preserved in alcohol and stored as part of the Australian National Wildlife Collection.

Museumspec

Skink museum specimens at the Australian National Wildlife Collection. Credit: Julian Resasco.

Much later, Resasco arrived and began dissecting skink guts to analyze the prey items for a study that looked at how the skinks shifted prey consumption (their feeding niche) in response to fragmentation. While dissecting the skink guts, he noticed that some of the skinks had worms (nematodes) inside their guts.  These nematodes were relatively common among skinks from continuous eucalypt forests, rare among skinks from eucalypt fragments, and absent from skinks in the cleared, pine plantation matrix.

ResascoFig1

Top. The study area in southeast Australia, showing location of continuous forest, forest fragments and surrounding matrix.  Dots indicate locations of pitfall traps. The matrix was planted in pine seedlings soon after fragmentation.  Bottom. The pale-flecked garden sunskink Lampropholis guichenotti. Credit: Jules Farquar

As it turned out, the nematode was a new species, which Resasco and a colleague (Hugh Jones) named Hedruris wogwogensis. Nematodes in the genus Hedruris use crustaceans as intermediate hosts, which alerted Resasco and his colleagues that the terrestrial amphipod Arcitalitrus sylvaticus, which was very common in the pitfall traps, was probably an important intermediate host.  When amphipods from pitfall traps were examined microscopically, a small portion of them were infected with Hedruris wogwogensis. The researchers concluded that amphipods became infected when they ate plants that harbored nematode eggs or young nematodes, which then developed in amphipod guts, and were passed on to skinks that ate the amphipods.  Thus somewhat inadvertently, one aspect of the study transitioned into the question of how fragmentation can influence the transmission of parasites.

After concluding their skink dissections, Resasco and his colleagues discovered that skinks in continuous forest had five times the infection rate as did skinks in fragmented forest.  In addition, no skinks collected in the matrix were infected. Infected skinks harbored a similar number of nematodes, whether they lived in continuous forest or fragments (see the Table below). Lastly, amphipods were considerably more common in skink guts and pitfall traps from continuous forest, less so in fragments, and least in the matrix.

ResascoTab1good

Summary of data collected by Resasco and his colleagues. Nematode intensity is the mean number of nematodes per infected skink. Nematode abundance is the mean number of nematodes per skink (infected and uninfected). 

The researchers put these findings together in a structural equation model.  The boxes in the model below represent the variables, while the numbers in smaller boxes over the arrows are the regression coefficients, with larger positive numbers (in black) indicating stronger positive effects, and larger negative numbers (in red) indicating stronger negative effects.  The model revealed three important findings.  First, habitat fragmentation strongly reduced amphipod abundance.  High amphipod abundance was associated with high nematode abundance (that is the +0.20 in the model), so lower amphipod abundance from fragmentation reduced nematode abundance. Second, habitat fragmentation positively affected skink abundance – more skinks were captured in fragments than in intact forest, but this increase had no effect on nematode abundance in skinks.  Finally, note the direct arrows connecting “Fragmentation” to “Log nematode abundance in skinks”.  This indicates that other variables (beside amphipod abundance) are reducing infection rates in skinks that live in fragments and the matrix.

ResascoFig3

Structural equation model showing effects of fragmentation on nematode infection in skinks. Amphipods are the intermediate host.  Black arrows indicate significant positive effects of one variable on the other, while red arrows indicate significant negative effects. Solid lines represent fragments compared to controls and dashed lines represent the matrix compared to controls. Thicker lines are stronger effects.

At this point, we still have an incomplete understanding of the system.  We know that fragmentation reduces amphipods, which require a moist and shaded environment to thrive.  Reduced amphipod abundance leads to lower nematode infection rates in skinks.  But we know that other variables are important as well; perhaps nematodes survive more poorly in fragment and matrix soils. Interestingly, pine trees were planted in the matrix and are beginning to mature and shade out the matrix environment. Amphipod abundances are on the rise, so the researchers predict that nematode infection rates will begin to increase accordingly.  Those studies have begun.

IMG_2646

Eucalypt forest canopy at Wog Wog. Credit: Julian Resasco.

Looking at the bigger picture, it is clear that fragmentation may decrease (as in this study) or increase the abundance of an intermediate host. As an example of fragmentation increasing intermediate host abundance, the researchers describe a study in which fragmentation increased the abundance of the white footed mouse, an intermediate host for black-legged ticks (that host the bacteria that causes Lyme disease). We need to unravel the connections between landscape factors and the various species they influence, so we can begin to understand how human changes to the landscape can influence the transmission of diseases.

note: the paper that describes this research is from the journal Ecology. The reference is Resasco, J.,  Bitters, M. E.,  Cunningham, S. A.,  Jones, H. I.,  McKenzie, V. J., and  Davies, K. F..  2019. Experimental habitat fragmentation disrupts nematode infections in Australian skinks. Ecology  100( 1):e02547. 10.1002/ecy.2547. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

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.

crayfish, egg masses, clutches

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.

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.

least-sandpiper-in-grac_signed.jpg

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.

2015-01-20 14.39.58

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.

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.

Tsujigazes

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.

TsujiFlowers

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.

Tsujiplates

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.

Tsuji2e

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.

Tsujifig2ab

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.

TsujiFig2cdnewnew

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.

Coral can recover (occasionally)

Coral reefs have amazing species diversity, which depends, in part, on a mutualism between the coral animal and a group of symbiotic algae that live inside the coral. The algae provide the coral host with approximately 90% of the energy it needs (from photosynthetic product).  In return, the algae are rewarded with a place to live and a generous allotment of nitrogen (mostly fecal matter) from the coral.  Unfortunately, coral are under attack from a variety of sources. Most problematic, humans are releasing massive amounts of carbon dioxide into the atmosphere, which is increasing ocean temperatures and also making the ocean more acidic.  Both processes can kill coral by causing coral to eject their symbiotic algae, making it impossible for the coral to get enough nutrients.

Moorea Coral Reef LTER site

The coral reef at Mo’orea. Credit: Moorea Coral Reef LTER site.

But other factors threaten coral ecosystems as well. For example, the reefs of Mo’orea , French Polynesia (pictured above), were attacked by the voracious seastar, Acanthaster planci, between 2006-2010, which reduced the coral cover (the % of the ocean floor that is covered with coral when viewed from above) from 45.8% in 2006 to 6.4% in 2009.  Then, in Feb 2010, Cyclone Oli hit, and by April, mean coral cover had plummeted down to 0.4%.

Moorea swimmers

Researchers survey the reef at Mo’orea. Credit: Peter Edmunds.

Peter Edmunds has been studying the coral reef ecosystem at Mo’orea for 14 years, and has observed firsthand the sequence of reef death, and the subsequent recovery.  Working with Hannah Nelson and Lorenzo Bramanti, he wanted to document the recovery process, and to identify the underlying mechanisms.  Fortunately Mo’orea is a Long Term Ecological Research (LTER) site, one of 28 such sites funded by the United States National Science Foundation.  Consequently the researchers had long term data available to them, so they could document how coral abundance had changed since 2005.  Their analysis showed the decline in coral cover from 2007 to 2010, but a remarkable rapid recovery beginning in 2012 and continuing through 2017.

EdmundsFig1

% cover (+ SE) of all coral , Pocillopora coral (the species group that the research team focused on). and macroalgae at Mo’orea over a 13 year period based on LTER data. The horizontal bar with COTs above it represents the time period of maximum seastar predation.

What factors caused this sharp recovery? One general process that could be part of the answer is density dependence, whereby populations have high growth rates when densities are low and there is very little competition, and low growth rates when densities are high and there is a great deal of competition between individuals, or in this case, between colonies. The problem is that though density dependence makes intuitive sense, it is difficult to demonstrate, as other factors could underlie the coral recovery.  Perhaps after 2011 there was more food available, or fewer predators, or maybe the weather was better for coral growth.

EdmundsQuadrats

High density (top) and low density (bottom) quadrats of Pocillopora coral established by the research group.

To more convincingly test for density dependence, Edmunds and his colleagues set up an experiment, establishing 18 1m2 quadrats in April, 2016. The researchers reduced coral cover in nine quadrats to 19.1% by removing seven or eight colonies from each experimental quadrat (low density quadrats), and left the other nine quadrats as unmanipulated controls, with coral cover averaging 32.5% (high density quadrats).  They then asked if, over the course of the next year, more recruits (new colonies < 4cm diameter) became established in the low density quadrats.

Returning in 2017, the researchers discovered substantially greater recruitment in the low density quadrats than in the high density quadrats. This experiment provides strong evidence that the rapid recovery after devastation by seastars and Cyclone Oli was helped by a density dependent response of the coral population – high recruitment at low population density.

EdmundsFig3

Density of recruits just after (left), and one year after (right) the quadrats were established. Solid bars are means (+ SE) for high density quadrats, while clear bars are means (+ SE) for low density quadrats.

In recent years, many coral reef systems around the world have experienced declining coral cover, a loss of fish and invertebrate diversity and abundance, and an increase in abundance of macroalgae.  While many of these reefs continue to decline, others, such as the reefs at the Mo’orea LTER site, are more resilient, and are able to recover from disturbance.  The researchers argue that we need to fully understand the mechanisms underlying recovery – in other words what is causing the density dependent response? Is it simply competition between coral that cause high recruitment under low density, or may interactions between coral and algae be important?  And what types of interactions influence recruitment rates under different densities?  One possibility is that at high densities, coral are eating most of the tiny coral larvae as they descend from the surface after a mass spawning event.  This raises the important question of why many reefs around the world do not show this density dependent response.  Clearly there is much work remaining to be done if we want to preserve this critically endangered marine biome.

note: the paper that describes this research is from the journal Ecology. The reference is Edmunds, P. J., Nelson, H. R. and Bramanti, L. (2018), Density‐dependence mediates coral assemblage structure. Ecology, 99: 2605-2613. doi:10.1002/ecy.2511. 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.

Decomposition: it’s who you are and where you are

“Follow the carbon” is a growing pastime of ecologists and environmental researchers worldwide. In the process of cellular respiration, organisms use carbon compounds to fuel their metabolic pathways, so having carbon around makes life possible.  Within ecosystems, following the carbon is equivalent to following how energy flows among the producers, consumers, detritivores and decomposers. In soils, decomposers play a central role in energy flow, but we might not appreciate their importance because many decomposers are tiny, and decomposition is very slow.  We are thrilled by a hawk subduing a rodent, but are less appreciative of a bacterium breaking down a lignin molecule, even though at their molecular heart, both processes are the same, in that complex carbon enters the organism and fuels cellular respiration.  However. from a global perspective, cellular respiration produces carbon dioxide as a waste product, which if allowed to escape the ecosystem, will increase the pool of atmospheric carbon dioxide thereby increasing the rate of global warming. So following the carbon is an ecological imperative.

As the world warms, trees and shrubs are colonizing regions that previously were inaccessible to them. In northern Sweden, mountain birch forests (Betula pubescens) and birch shrubs (Betula nana) are advancing into the tundra, replacing the heath that is dominated by the crowberry, Empetrum nigrum. As he began his PhD studies, Thomas Parker became interested in the general question of how decomposition changes as trees and shrubs expand further north in the Arctic. On his first trip to a field site in northern Sweden he noticed that the areas of forest and shrubs produced a lot of leaf litter in autumn yet there was no significant accumulation of this litter the following year. He wondered how the litter decomposed, and how this process might change as birch overtook the crowberry.

ParkerView

One of the study sides in autumn: mountain birch forest (yellow) in the background, dwarf birch (red) on the left and crowberry on the right. Credit: Tom Parker.

Several factors can affect leaf litter decomposition in northern climes.  First, depending on what they are made of, different species of leaves will decompose at different rates.  Second, different types of microorganisms present will target different types of leaves with varying degrees of efficiency.  Lastly, the abiotic environment may play a role; for example, due to shade and creation of discrete microenvironments, forests have deeper snowpack, keeping soils warmer in winter and potentially elevating decomposer cellular respiration rates. Working with several other researchers, Parker tested the following three hypotheses: (1) litter from the more productive vegetation types will decompose more quickly, (2) all types of litter decompose more quickly in forest and shrub environments, and (3) deep winter snow (in forest and shrub environments) increase litter decomposition compared to heath environments.

To test these hypotheses, Parker and his colleagues established 12 transects that transitioned from forest to shrub to heath. Along each transect, they set up three 2 m2 plots – one each in the forest, shrub, and heath – 36 plots in all. In September of 2012, the researchers collected fresh leaf littler from mountain birch, shrub birch and crowberry, which they sorted, dried and placed into 7X7 cm. polyester mesh bags.  They placed six litter bags of each species at each of the 36 plots, and then harvested these bags periodically over the next three years. Bags were securely attached to the ground so that small decomposers could get in, but the researchers had to choose a relatively small mesh diameter to make sure they successfully enclosed the tiny crowberry leaves. This restricted access to some of the larger decomposers.

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Some litter bags attached to the soil surface at the beginning of the experiment. Credit: Tom Parker.

To test for the effect of snow depth, the researchers also set up snow fences on nearby heath sites.  These fences accumulated blowing and drifting snow, creating a snowpack comparable to that in nearby forest and shrub plots.

Parker and his colleagues found that B. pubescens leaves decomposed most rapidly and E. nigrum leases decomposed most slowly.  In addition, leaf litter decomposed fastest in the forest and most slowly in the heath.  Lastly, snow depth did not  influence decomposition rate.

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(Left graph) Decomposition rates of E. nigrum, B. nana and B. pubescens in heath, shrub and forest. (Right graph) Decomposition rates of E. nigrum, B. nana and B. pubescens in heath under three different snow depths simulating snow accumulation at different vegetation types: Heath (control), + Snow (Shrub) and ++ Snow (Forest) . Error bars are 1 SE.

B. pubescens in forest and shrub lost the greatest amount (almost 50%) of mass over the three years of the study, while E. nigrum in heath lost the least (less than 30%).  However, B. pubescens decomposed much more rapidly in the forest than in the shrub between days 365 and 641. The bottom graphs below show that snow fences had no significant effect on decomposition.

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Percentage of litter mass remaining (a, d) E. nigrum, (b, e) B. nana, (c, f) B. pubescens in heath, shrub, or forest. Top graphs (a, b, c) are natural transects, while the bottom graphs (d, e, f) represent heath tundra under three different snow depths simulating snow accumulation at different vegetation types: Heath (control), + Snow (Shrub) and ++ Snow (Forest) . Error bars represent are 1SE. Shaded areas on the x-axis indicate the snow covered season in the first two years of the study.

Why do mountain birch leaves decompose so much more than do crowberry leaves?  The researchers chemically analyzed both species and discovered that birch leaves had 1.7 times more carbohydrate than did crowberry, while crowberry had 4.9 times more lipids than did birch. Their chemical analysis showed much of birch’s rapid early decomposition was a result of rapid carbohydrate breakdown. In contrast, crowberry’s slow decomposition resulted from its high lipid content being relatively resistant to the actions of decomposers.

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Researchers (Parker right, Subke left) harvesting soils and litter in the tundra. Credit: Jens-Arne Subke.

Parker and his colleagues did discover that decomposition was fastest in the forest independent of litter type. Forest soils are rich in brown-rot fungi, which are known to target the carbohydrates (primarily cellulose) that are so abundant in mountain birch leaves.  The researchers propose that a history of high cellulose litter content has selected for a biochemical environment that efficiently breaks down cellulose-rich leaves. Once the brown-rot fungi and their allies have done much of the initial breakdown, another class of fungi (ectomycorrhizal fungi) kicks into action and metabolizes (and decomposes) the more complex organic molecules.

The result of all this decomposition in the forest, but not the heath, is that tundra heath stores much more organic compounds than does the adjacent forest (which loses stored organic compounds to decomposers).  As forests continue their relentless march northward replacing the heath, it is very likely that they will introduce their efficient army of decomposers to the former heathlands.  These decomposers will feast on the vast supply of stored organic carbon compounds, release large quantities of carbon dioxide into the atmosphere, which will further exacerbate global warming. This is one of several positive feedbacks loops expected to destabilize global climate systems in the coming years.

note: the paper that describes this research is from the journal Ecology. The reference is Parker, T. C., Sanderman, J., Holden, R. D., Blume‐Werry, G., Sjögersten, S., Large, D., Castro‐Díaz, M., Street, L. E., Subke, J. and Wookey, P. A. (2018), Exploring drivers of litter decomposition in a greening Arctic: results from a transplant experiment across a treeline. Ecology, 99: 2284-2294. doi:10.1002/ecy.2442. 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.