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.

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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.

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

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

Field Sampling

Student researchers collect stream samples. Credit: Gary Bucciarelli

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

BuccTable1

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

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

BuccFig2A

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

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

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

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

Invasive engineers alter ecosystems

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

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

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

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

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

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

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

HaramFig1

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

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

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

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

HaramFig2

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

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

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

note: the paper that describes this research is from the journal Ecology. The reference is Haram, L. E., Kinney, K. A., Sotka, E. E. and Byers, J. E. (2018), Mixed effects of an introduced ecosystem engineer on the foraging behavior and habitat selection of predators. Ecology, 99: 2751-2762. doi:10.1002/ecy.2495. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.