Cottonwood genes and spider hostels

Back in my working days, people that I met would sometimes ask me what I did for my research. I usually told them that I studied spider sex, which, while true, was a bit misleading, as my interests were actually slightly broader. But studying spider sex was a good fit for my disposition, because, more than anybody I know, I can stare at something for a very long time and not get bored. And when spiders have sex, there can be very long periods, when, to our eyes, nothing is going on. As it turns out there is a great deal of pheromonal communication going on, and considerable vibrational activity as well, but it is not that easy for humans (even abnormally patient ones) to detect.


A spider and her three egg cases within a web she has built in a Taphrina blister. Credit Matt Barbour

The point is that I have a very soft spot in my heart for spiders, and was delighted to learn about an indirect process that provided a comfortable home for needy spiders. Heather Slinn got interested in her project while an undergraduate summer intern. Her colleague, Matt Barbour, pointed out that when he flipped over blistered black cottonwood leaves (Populus trichocarpa) he often found a spider hanging out in there. This observation led to her to study the relationship between cottonwood trees, cottonwood genetics, pathogens that make leaf blisters and spider occupancy rates.

Taphrina fungi form cup-like blisters in the leaves of Populous trees. But these trees vary in how susceptible they are to leaf blisters. The researchers wanted to answer three questions about this relationship. First, do spiders prefer to live in leaf-blisters as opposed to unblistered leaves? Second, are differences in tree susceptibility to Taphrina a result of genetic differences between the trees? And third can differences in Taphrina-resistance account for differences in spider density?

One of the keys to the experiment was establishing a garden with distinct clones of trees of known genetic makeup (genotypes). Slinn and her colleagues studied five different genotypes, with approximately 40 trees per genotype. They dutifully watered them throughout the summer, and then sampled up to 30 leaves from each tree for blister density, blister size, and spider residency, using a modified shop vac to suck up all of the spiders.


Black Cottonwood garden. Credit Matt Barbour

The researchers discovered that blistered leaves were 35 times more likely to have a spider and/or spider web than were unblistered leaves. Clearly spiders found blistered leaves to be highly attractive homes.

But there were pronounced differences among the five genotypes in blister density, blister size, spider density and the probability that a spider was occupying a blister. Graph A shows that genotypes 1 and 3 (G1 and G3) had the lowest mean density of blisters (about 2 or 3 per meter of plant), while G4 averaged about 20 blisters per meter. Although G3 had relatively few blisters, it did boast the largest blisters (see graph B). The researchers concluded that blister density and size were both under genetic control, but not linked to each other.


Mean (A) blister density (number per meter of plant) and (B) blister size, for the five tree genotypes.

But how did blister density and size influence spider residency? G4, the genotype with the greatest number of blisters per plant, also had the greatest number of spiders (graph C). But on a per blister basis, we can see that the two genotypes with the largest blisters (G2 and G3 – see graph B) also had the highest probability of housing a spider in their blisters (graph D). So when spiders make decisions about where to live, both size and number are important.


Mean (C) spider density and (D) probability a blister hosts a spider, for the five tree genotypes.

It is unclear why the spiders are attracted to blisters.  Some spider species have been shown to be attracted to structural complexity, because that provides more or better attachment points for web strands and egg cases.  Depressed blisters may also give protection from abiotic factors such as wind and precipitation.

Like most good studies, this research raises a host of related questions. Why is there so much genetic variation in Taphrina-resistance within this tree species? Slinn suggests that there may be tradeoff whereby investment into Taphrina-resistance might compromise a plant’s ability to invest in other functions such as cold-resistance, or rapid growth and/or high reproductive rates. A second question is how does spider presence influence other species – for example does hosting a spider reduce the number of herbivorous insects that might attack the tree? A third issue raised by the authors is that plants infected with Taphrina may be weaker and more susceptible to herbivores. In that case, the spiders may be present in blisters because they are attracted to the herbivores that are eating the leaves. And finally, herbivores eating the leaves may transmit other diseases affecting our forests, such as dutch elm disease, chestnut blight and white pine blister rust. Unraveling this complex chain of events will keep researchers busy for many years.

note: the paper that describes this research is from the journal Ecology. The reference is Slinn, H. L., Barbour, M. A., Crawford, K. M., Rodriguez‐Cabal, M. A., & Crutsinger, G. M. (2016). Genetic variation in resistance to leaf fungus indirectly affects spider density. Ecology 98(3): 875-881. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

Timely trophic cascades

While many of us appreciate oysters as delectable delights, we may underestimate the environmental benefits they also bring to the table. As filter feeders, they remove vast quantities of organic debris from the water, and as reef builders they protect our shorelines from violent wave action.


Oyster reef. Credit: WFSU, Public Media

Of course, humans are not the only animals to enjoy eating oysters. For example, along portions of the Florida coast dominated by the reef-building oyster Crassostrea virganica, the mud crab, Panopeus herbstii, is a major consumer of juvenile oysters. In some locations, the average abundance of these voracious crabs can exceed 10 adults/m2 of reef. But all is not food and gravy for these crabs, as lurking in nearby burrows are equally voracious crab-eating toadfish, Opsanus tau. When toadfish are detected, the mud crabs will hide within the protective matrix of oyster shells and sediment that form the reef.


A mud crab hiding among a cluster of oysters. Credit: WFSU, Public Media

By consuming mud crabs, toadfish are indirectly protecting oysters from being eaten. Ecologists call this a consumptive effect (CE). But David Kimbro and his colleagues have also shown than toadfish, by their mere presence, can also protect oysters by scaring the crabs into hiding. Since, in this case, they are not consuming the crabs, ecologists call this a non-consumptive effect (NCE). Together, CEs and NCEs should both increase oyster survival. More surviving oysters lead to higher overall feeding by oysters, which lead to more oyster poop, and more organic matter deposited into the sediment below. Ecologists call this type of relationship a trophic cascade, because the effects on one species cascades down through the ecosystem. In this case, increasing toadfish will decrease crabs, thereby increasing oysters and sediment organic matter. Conversely, decreasing toadfish should increase crabs, thereby decreasing oysters and sediment organic matter.


Toadfish/mud crab/oyster/sediment organic matter (SOM) cascade. Dotted arrows are indirect effects

Kimbro and his colleagues wanted to explore this trophic cascade in more detail. They set up an experiment with 24 artificial reefs (made out of natural materials, except for the surrounding fence), which included 35 L of live oysters. They supplied each reef with 0, 2, 4, 6, 8 or 10 live crabs, and provided half of the reefs with a caged toadfish. They then measured oyster survivorship in relation to crab density in the presence or absence of predators.


Setting up an artificial reef. Credit: WFSU, Public Media

The graphs below summarize their findings. The first thing to notice is that mud crabs were bad news for oysters, as survivorship plummeted when mud crabs were abundant. However, early in the experiment (graphs A and B) having a toadfish around helped out considerably. Oysters survived much better in the presence of toadfish (triangles and dotted curve) than they did without toadfish (circles and solid curve). But by the middle of the experiment (Graphs C and D), the toadfish no longer helped. Interestingly, by the end of the experiment (Graph E) the toadfish was once again helping the oyster’s cause, as survivorship was again greater in the presence of toadfish than in its absence. Realize that the difference between the dotted and solid curve is a measure of the NCE, as the toadfish are not eating the crabs (because they are caged). So we can conclude that there was a strong NCE early on, which waned in the middle of the experiment and then returned by the end of the experiment.


A second finding is that the reef grew (expanded) when there were no crabs present, but that even two crabs were enough to reduce reef growth to zero. In addition sediment organic matter was greatest when there were either none or only two crabs present in the reef. Four or more crabs in the reef reduced the deposition of sediment organic matter. These findings were not influenced by the presence or absence of toadfish.

This is a complicated system, but we (and toadfish, crabs and oysters) live in a complicated world. And there are several other complications that I have not even mentioned! We might argue that the crabs may habituate (get accustomed) to these toadfish, so that by the middle of the experiment, the toadfish NCE had worn off. That begs the question of why the NCE returned towards the end of the experiment. Kimbro suggests that at the beginning of the experiment, the novelty of the predator cue probably caused strong NCEs. But by the middle of the experiment, the crabs became hungry and chose to forage regardless of predator cue. Finally, towards the end of the experiment, the crabs, having filled up on juvenile oysters, opted to hide rather than forage when toadfish were present. Whatever the reason, these findings caution us that if we want to understand trophic cascades, we need to consider the dimensions of both space and time.

note: the paper that describes this research is from the journal Ecology. The reference is Kimbro, D. L., Grabowski, J. H., Hughes, A. R., Piehler, M. F., & White, J. W. (2017). Nonconsumptive effects of a predator weaken then rebound over time. Ecology 98(3): 656-667. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

Chironomids: the great Icelandic farmers

Ecologists describe plants and algae as producers because, with the help of solar energy, they produce sugar and other complex carbohydrates from carbon dioxide in the process we call photosynthesis. Consumers, such as horses, chironomids and lions, eat producers or other consumers, using the chemical energy in their food’s complex molecules to fuel their own metabolic processes. Without photosynthesis there would be almost no life, as consumers would need to scavenge the organic molecules that happened to be lurking about in the environment.

You’ll notice I slipped in chironomids as consumers, because they are the diminutive heroes of this tale. There are actually more than 10,000 chironomid species, but the ones we are discussing lay their fertilized eggs into lake water where they sink into the sediment and hatch out as larvae. These larvae go through several growth stages, building tubes which serve as their houses during growth and development. Larvae then transform into pupae, which after a few days swim to the surface and metamorphose into winged adults, which mate and produce more fertilized eggs.


Chironomid Larvae. Credit Michael Drake


Larval tubes in sediment. Credit Cristina Herren








We usually think about consumers as having a negative effect on their food and/or prey. If we introduce a herd of sheep into a small pasture, we are confident that the grass will quickly disappear inside of sheep bellies. Similarly, if we introduce a few lions into a pen of sheep, we can be fairly confident that the sheep population will decline. But consumer effects on populations can act in strange and wonderful ways.

The subarctic Lake Mývatn in Iceland is host to an amazingly huge number of chironomid larvae; over 100,000 of these insects can squeeze into 1 m2 of lake bottom!


Lake Myvatn. Credit Michael Drake


Swarming adult chironomids. Credit Michael Drake






As Cristina Herren describes, Lake Mývatn has long been studied because of the dramatic changes in chironomid densities. Chironomid populations can increase 10-fold in each of four or five consecutive generations during the subarctic spring and summer. So if you began with a density of 10 chironomids/m2 in April, you might find 100/m2 in May, 1000/m2 in June, 10,000/m2 in July and 100,000/m2 in August. Herren was intrigued by this exponential growth, as it suggested that somehow chironomid food resources (primarily algae) were keeping pace with the exploding chironomid population, despite being eaten by this ever-expanding population. How could the algae keep pace with the furious chironomid growth rate? Herren wondered whether the chironomids were acting as farmers and somehow stimulating algal production.

Herren worked with several other researchers to figure out the answer to this puzzle. First, they wondered whether the larval tubes provided an awesome place for algae to live. Second, perhaps chironomids were pooping-out vast quantities of nutrient-rich waste products, which algae used to build their bodies. Either or both of these positive effects could more than compensate for the direct negative effect from chironomids eating the algae.

To investigate both hypotheses, the researchers set up 1-liter clear plastic containers with lake sediment and either 0, 50, 100, 200, 400, 600, 800 or 1200 chironomids (that must have been fun to count!). They placed six or seven containers with each population size into racks at the bottom of the lake.

The first task was to discover whether production actually increased with chironomid abundance. Oxygen is a waste product of photosynthesis, so scientists use oxygen production to measure photosynthetic rate, and also to infer algal abundance. They found that oxygen production actually increased with chironomid abundance. Note that chironomids (and the algae too) actually consume oxygen (just like you and I do) in the process of respiration, so this is a truly remarkable result. It indicates that production increased so much that it more than compensated for the oxygen used up by the chironomids and algae from respiration.


The algae use chlorophyll a in their cells as the molecule for photosynthesis, so algal abundance can be estimated by measuring how much chlorophyll a is present in each bottle. Again, they found more chlorophyll a in the bottles with more chironomids, despite the fact that chironomids were eating all the algae they could find.


In addition, the chironomids from more crowded conditions weighed more than those from sparsely-populated bottles. The researchers concluded that by eating algae, the chironomids were actually increasing algal abundance, thereby creating more food for themselves.

These findings fly in the face of our usual assumptions about consumers reducing the population size of the species they are consuming. The researchers confirmed two important indirect effects of chironomids on algae. First, the chironomid larvae do excrete vast quantities of concentrated nutrients (nitrogen and phosphorus) that are consumed by the algae. In addition, the chironomids tubes are indeed ideal surfaces for algae to hang-out on, as evidenced by finding much more chlorophyll a on the tubes than in the nearby sediment.

We citizens need to recognize that both direct and indirect effects operate within ecosystems. In this case, algae are clearly directly benefitting chironomids by providing them with food. Less obvious, the chironomid effects on algae are in two directions. Chironomids have a direct negative effect on algal populations by consuming vast quantities of algae. However, they have a stronger indirect positive effect on algal populations, by providing algae with high quality housing and abundant resources, so that the algal population grows dramatically over the year. The net effect of chironomids on algal populations (dashed arrow) is positive.


Most ecosystems have many different direct and indirect effects operating between a large number of species. It’s a real challenge to identify and understand these diverse interactions, which is why we need to be cautious about changing ecosystems in significant ways. For example, when we dump our waste products into waterways or soils, the added nutrients can have pronounced direct and indirect effects on the species that live there. In many cases, we won’t be able to identify the unintended consequences of our actions on an ecosystem until the native species have gone extinct.

note: the paper that describes this research is from the journal Ecology. The reference is Herren, Cristina M., et al. “Positive feedback between chironomids and algae creates net mutualism between benthic primary consumers and producers.” Ecology 98.2 (2017): 447-455. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.