Posts Tagged ‘Birds’
Every thirteen years they come. After over a decade underground, they build burrows to the earth’s surface and emerge in synchrony, clawing and crawling up through the soil, rip their skins down the back and are reborn as adults. And after a month, they will be dead, whether consumed by the animals awaiting their arrival or as a part of their lifecycle, with the females having laid eggs in the soil to develop for another thirteen years.
Some cicadas emerge every single year — annual or “dog days” cicadas — but two broods are on much lengthier cycles. This year, 2011, Brood XIX cicadas have already begun emerging throughout the southern United States. In 2004, I was lucky enough to experience the emergence of Brood X and won’t have the honor again for yet another decade, after a total of 17 years in 2021.
Their peak in 2004 coincided with Princeton University’s alumni weekend — which I attended as a bored high schooler — and what poor timing for that event! The endless drone of the insects forced us to yell just to make conversation; the air was so dense with their swarms that they would fly into unsuspecting Princeton grads with a size and velocity that was actually painful; sidewalks and windshields were splotched with the pale green stains of the squished deceased.
Besides providing a weekend of entertainment for high school hooligans witnessing the torture of exasperated ivy-league graduates, the emergence of millions upon millions of cicadas for just a single month provides an ephemeral pulse of resources. Once dead, their decaying bodies add nutrients to the soil (1) and streams (2), increasing soil microbes (3) and detritivorous insects (4), while their predation on roots as nymphs and plants, young ones in particular, as adults can decrease tree (5, 6) and plant (7) growth in the cicadas’ emergence year.
This deluge of huge, nutritious bugs should be a boon for their predators as an undepletable food source. While one study (8) found no change in a population of white-footed mice after Brood X emerged, the same study saw the number of short-tailed shrews increase four-fold — now that’s a lot of shrews!
So you’d probably expect a similar reaction from insect-eating birds — that some would have no change, but some would benefit greatly from the cicada surge, especially since their migratory nature would allow them to gather by the cicadas during emergence years. But when ornithologist Walter Koenig and entomologist Andrew Liebhold compared populations of 24 bird populations over the course of 37 years from the Breeding Bird Survey data set with periodic cicada pulses (9), they found only two species that showed up just for the cicadas — both North American cuckoo species. Out of the other 22 species, only 6 populations increased; the remaining 16 declined, and 5 of them with statistical significance.
They had three hypotheses to explain why so many bird populations were decreasing, according to a large observation-based bird survey, even when the birds were practically drowning in ample food resources. The overwhelmingly loud noise of cicada calling could drown out bird calls for the birdwatchers, creating an observer bias artificially lowering the reported number of birds in the area — the detectability hypothesis. Alternatively, all the racket could keep the birds from hearing one another, disrupting their communication and driving them to quieter areas with fewer cicadas — the repel hypothesis. Or the birds populations could be declining for another reason, affecting them beyond the ranges of the cicadas — the true decline hypothesis.
Koenig and Liebhold just published a reanalysis (10) in March 2011 in Ecology to test their ideas about why these bird populations are dropping. Again, they used the Breeding Bird Survey data for the 12 species showing the greatest decline from their previous paper, but also compared populations to the counts from the previous winter (Christmas Bird Counts) and incorporated notes about cicada prevalence from the counts where they could.
Their results supported the true decline hypothesis — that the birds’ population declines are not related to the emergences at all. They suggest that the drop in population numbers could be an indirect effect of the cicada emergences, however. The voracious plant consumption of the cicadas could be negatively affecting other insect prey sources or otherwise adversely impacting the immediate habitat. Additionally, while North American cuckoos are not typically nest parasites, this behavior — laying their eggs in the nests of other birds — has been observed when cuckoos are under intense competition with one another, as in this situation.
Some scientists (11) suggest that cicadas emerge on such odd timescales — 13 and 17 years, I mean, c’mon! — specifically to mess with their predators. If they emerged too frequently, their tactic of completely overwhelming the area with their presence, basically guaranteeing that many of them will successfully reproduce no matter how many housecats and cuckoos are fed — predator satiation — wouldn’t work. If they emerged more frequently, the gains of their predators from the cicadas’ previous emergence may still be lingering, effectively increasing their predators’ numbers each year until the cicadas themselves were overrun. (A hard scenario to imagine, I know — that would take even more shrews!)
But could the cicadas have evolved to take advantage of such a long-term concept? That they would have to effectively “wait” for their predators to be on the decline before they emerge again? Some biologists have even hypothesized that the latency periods of 13 and 17 years are significant because they are prime numbers! Take it away, Dr. Nicolas Lehmann-Ziebart:
[A]ssume that cicada predators consist of species having cyclic or ‘‘quasi-cyclic’’ dynamics with either two- or three-year periods. This leads to high predator abundances, and high predation rates, in years divisible by either two or three. Because primes are the only numbers between 10 and 18 that are not divisible by 2 or 3, broods of prime-period cicadas frequently escape high predation levels and hence tend to dominate hypothetical cicadas with nonprime periods. This mechanism for generating prime numbers relies on either externally driven two- and three-year cycles of predators, or predators that have strict fecundity schedules creating dynamics that tend to show two- or three-year oscillations.
Lehmann-Ziebart and his undergrads suspect that the cicadas emerge in these odd patterns as a balance between predator satiation and competition within the cicadas themselves. They, unfortunately, couldn’t find an obvious explanation for the prime numbers, though suggest it could have to do with a genetic counting mechanism.
Another explanation for this odd pattern of bird decreases coinciding with great cicada food sources is shoddy data. The Bird Breeding Survey is performed by mere citizens after all — can’t trust them! JUST KIDDING! There have been criticisms of the survey, including new observer bias (a n00b bird counter gets better each year, so the early years are unreliable and this bias is not accounted for), its road-based sites and transects for the counter’s ease could cause bias due to car traffic, and variation in the number of counters year-to-year. Nonetheless, the survey covers an incredible amount of ground — with each route covering nearly 25 miles — and over 400 bird species and has been ongoing since 1966. Pretty good for any large-scale data set which will always have caveats.
It looks like the jury’s still out on why bird populations decline during cicada emergences, though I suspect it’s a combination of many factors — bird communication problems, detectability bias, ecosystem changes induced by the cicadas and the overall variability in bird populations and routes.
(1) Wheeler, G., Williams, K., & Smith, K. (1992). Role of periodical cicadas (Homoptera: Cicadidae: Magicicada) in forest nutrient cycles Forest Ecology and Management, 51 (4), 339-346 DOI: 10.1016/0378-1127(92)90333-5
(2) Pray, C., Nowlin, W., & Vanni, M. (2009). Deposition and decomposition of periodical cicadas (Homoptera: Cicadidae: Magicicada) in woodland aquatic ecosystems Journal of the North American Benthological Society, 28 (1), 181-195 DOI: 10.1899/08-038.1
(3) Yang, L. (2004). Periodical Cicadas as Resource Pulses in North American Forests Science, 306 (5701), 1565-1567 DOI: 10.1126/science.1103114
(4) Yang, L. (2005). Interactions between a detrital resource pulse and a detritivore community Oecologia, 147 (3), 522-532 DOI: 10.1007/s00442-005-0276-0
(5) Speer, J., Clay, K., Bishop, G., & Creech, M. (2010). The Effect of Periodical Cicadas on Growth of Five Tree Species in Midwestern Deciduous Forests The American Midland Naturalist, 164 (2), 173-186 DOI: 10.1674/0003-0031-164.2.173
(6) Koenig, W., & Liebhold, A. (2003). Regional impacts of periodical cicadas on oak radial increment Canadian Journal of Forest Research, 33 (6), 1084-1089 DOI: 10.1139/X03-037
(7) Yang, L. (2008). PULSES OF DEAD PERIODICAL CICADAS INCREASE HERBIVORY OF AMERICAN BELLFLOWERS Ecology, 89 (6), 1497-1502 DOI: 10.1890/07-1853.1
(8) Krohne, D., Couillard, T., & Riddle, J. (1991). Population Responses of Peromyscus leucopus and Blarina brevicauda to Emergence of Periodical Cicadas American Midland Naturalist, 126 (2) DOI: 10.2307/2426107
(9) Koenig, W., & Liebhold, A. (2005). EFFECTS OF PERIODICAL CICADA EMERGENCES ON ABUNDANCE AND SYNCHRONY OF AVIAN POPULATIONS Ecology, 86 (7), 1873-1882 DOI: 10.1890/04-1175
(10) Koenig, W., Ries, L., Olsen, V., & Liebhold, A. (2011). Avian predators are less abundant during periodical cicada emergences, but why? Ecology, 92 (3), 784-790 DOI: 10.1890/10-1583.1
(11) Lehmann-Ziebarth, N., Heideman, P., Shapiro, R., Stoddart, S., Hsiao, C., Stephenson, G., Milewski, P., & Ives, A. (2005). EVOLUTION OF PERIODICITY IN PERIODICAL CICADAS Ecology, 86 (12), 3200-3211 DOI: 10.1890/04-1615
“Overfishing” is a term associated with resource depletion, extinction, and human greed. While the definition of overfishing is technically a subjective measure (How much fishing is too much?), it has been widely accepted to mean catching more of an aquatic resource than can be replenished naturally by the system. The idea of depleting a marine resource is ubiquitous and familiar these days, with the bluefin tuna even featured as the cover article of the New York Times Magazine this past June.
The idea may be commonplace now, but this was not always so. A 2003 paper by Nicholas Dulvy and others enumerates the reasons why it was long believed that marine populations were more resilient than terrestrial species, and less likely to go extinct due to overfishing, habitat loss, invasive species, disease, and other causes. Jean Baptiste de Lamark himself was a proponent of the “paradigm of ocean inexhaustibility” due to the high fecundity of fish. He (and others) argued that because fish lay so many eggs and have excessive offspring (with little care put into each), we could never actually catch enough of a population to cause any damage. One problem with this argument is that fecundity often increases with size of an individual. Since we selectively catch larger fish, we’re catching the most reproductively able of a population and causing a large impact per fish caught. Other arguments about the impossibility of aquatic extinction include broad geographic range and dispersal, and that economic extinction of a fishery would precede biological extinction of a species (all of which have counter-arguments).
In all the discussion of overfishing, it is always humans that are doing the fishing to the detriment of non-human species, either through depletion of a fished species itself, or by reducing resources for other species that rely on it for prey. It is we humans who must reduce our impacts and allot resources for other species on our fair planet.
Last month (August 2010), an article from ICES Journal of Marine Science asks whether humans are the only species capable of overfishing. More interesting than the research itself is the questions it raises about our own relationship with “nature.”
The story of cormorants in the Baltic Sea
The Great Cormorant (Phalacrocorax carbo) is a seabird that lives in the Baltic Sea, along with many other locales. According to the Helsinki Commission, in the 1950s and 1960s the bird was overhunted to near-extinction locally, at which point they were put under government protection. Over the rest of the 20th century, the bird population improved dramatically, recolonizing old haunts with great success. They were so successful that they began expanding their original range, initially colonizing Estonia in 1983. In 2005, there were 20 great cormorant colonies in Estonia with an estimated 10,000 nesting pairs.
Over the course of this period, fishing decreased in Estonia waters, in part to conserve the estuarine wetlands that are important for bird migration and fish spawning. Despite this, many commercially valuable fish stocks plummeted. Though working with a limited data set (fish were sampled only in 1995 and 2005), in the ICES paper, the scientists satisfactorily concluded that this loss of fish species was due to overexploitation, not by humans, but by these great cormorant colonies. The cormorants were fishing 10-20 times more than the commercial catch of fish species such as perch Perca fluviatilis and roach Rutilus rutilus, decreasing the fishes’ ability to recover year after year.
How this questions our typical relationship with “nature”
This is an interesting story for several reasons. The birds were able to spread their range as far as they did and, in the end, compete with humans for food resources because we were trying to protect them. Their near-extinction in the 1950s probably led the government to be hesitant to lift protection because the birds were no longer birds, but a symbol of species recovery. After such a great success, how could we take their resources away and potentially lead them to extinction once more?
The fact alone that they are seabirds also makes their presence hard to define. Some cases of “invasive species” are very clear cut. For example, brown tree snakes are not from Guam, but were brought there and are now wreaking havoc on native animal populations. But seabirds toe the line. They are able to fly anywhere, and simply live on colonies at sea. Who are we to determine where geographically those colonies exist? The authors of the paper do not even use the word “invasive” to describe the expansion of great cormorants into Estonia until the end of the paper.
Are these birds invasive? It depends on your definition of the term. Some would argue that, yes, they did not live there before but do now, and are affecting the ecosystem to the detriment of other species. But it’s all relative: invasive species are defined by an anthropocentric view of the world, in which what is “natural” is the distribution of organisms we initially encountered and recorded. But who are we to decide that a species belongs or does not belong in a certain place? Who are we to tell the cormorants that they cannot live on that rock near an ample food supply? We’re the only species that sets these sorts of boundaries; all the other species are just trying to utilize resources and survive.
The idea that humans are the only species able to overexploit a resource is also anthropocentric. It makes Homo sapiens the center of the world, the ones who determine the fate of all other organisms, who can harvest them for ourselves or choose to spare them. This case of the cormorants places us back in our role as a competitive species: we have to decide whether or not we are willing to take back our resource, even if it means losing some of these big, aesthetically-valuable cormorants. We are no longer the masters of nature, but rather are inserted back into it.
I hope I manage to keep up with this case and find out what happens in Estonia. At this point, “taking back our resource” would not mean going in and competing by fishing; there are too many cormorants, so we would simply deplete the resources further. Instead, the Estonian government would have to enter the colonies and manage the population through oiling or pricking eggs to kill the developing birds (the Helsinki Commission estimates that this is done to 18% of nests in Denmark). Already 10,000-20,000 birds are shot in the Baltic Sea area each year, but public protests limit the amount of population control that is performed.
We may have simply lost control of the situation at this point. There may just be too many cormorants to keep them from overfishing, for our own sake or to preserve the fish as an ecosystem resource.
Dulvy, N., Sadovy, Y., & Reynolds, J. (2003). Extinction vulnerability in marine populations Fish and Fisheries, 4 (1), 25-64 DOI: 10.1046/j.1467-2979.2003.00105.x
Vetemaa, M., Eschbaum, R., Albert, A., Saks, L., Verliin, A., Jurgens, K., Kesler, M., Hubel, K., Hannesson, R., & Saat, T. (2010). Changes in fish stocks in an Estonian estuary: overfishing by cormorants? ICES Journal of Marine Science DOI: 10.1093/icesjms/fsq113
Dimethylsulfide. Does that word mean anything to you? “Why yes,” you organic chemistry nerds may say, “It clearly is a molecule of sulfur with two methyl groups attached.” That’s as far as I could have gotten – until this past week, when I inundated myself with information on dimethylsulfide (DMS) due to a paper published in Science. Now I’m enlightened – what a wonderful molecule! Let me spoil it for you: it is simultaneously a defense mechanism, a chemical cue pervasive throughout the marine food web, and an effector on the earth’s climate. (See illustration at bottom of post for summary.) That’s right. Just a sulfur molecule with two methyl groups attached. Now let’s back up a bit.
DMS is a sulfur compound that accounts for 50-60% of the total natural reduced sulfur flux to the atmosphere (even more than either volcanoes or vegetation). While sulfur in the atmosphere can cause acid rain, it is also very important, as it helps form clouds. In order for water to transition from a gas to liquid in the atmosphere, it needs a small particle in the air to adhere onto, known as a cloud condensation nucleus. Sulfur oxide, which can be derived from DMS, is one of these particles. Clouds not only carry our precipitation, but help to reflect sunlight (and thus heat) back into space, affecting our planet’s climate.
After the realization of its importance as a cloud condensation nucleus, scientists began to look for DMS’s planetary source and found that 95% of the atmospheric DMS originates in the oceans – but from where? As illustrated in my figure, it is actually formed in certain species of phytoplankton and released when cells leak, most often due to herbivory by other organisms. The phytoplankton itself actually makes a molecule called DMSP (dimethylsuphoniopropionate, if you must know). When its cell wall begins to break down, stores of DMSP (from an unknown location within the cell) and an enzyme, DMSP-lyase, are released into the surrounding water. This DMSP-lyase removes the P-group, leaving us with our favorite molecule of the day, DMS.
In 1987, the CLAW hypothesis (named for its authors) was put forward by James Lovelock and a handful of his lackeys to support his infamous Gaia hypothesis which suggests that microorganisms regulate the Earth’s climate to maintain conditions suitable for life. CLAW hypothesized that levels of DMSP and its P-cleaving enzyme in phytoplankton are regulated by light and temperature, with greater amounts of DMSP produced when it gets warm in order to send more DMS into the atmosphere, deflecting sunlight and reducing global temperatures. However, like most support for the Gaia hypothesis, this idea requires that phytoplankton act altruistically, releasing the DMS for the good of the planet, which does not make much sense in light of natural selection. (A good review of this and the above sections can be found in this paper by Rafel Simo.)
A 2001 MEPS paper by Kathryn Van Alstyne and others provides evidence that the release of DMSP and DMSP-lyase by phytoplankton is actually a chemical defense mechanism. After DMSP-lyase activity, the resulting products are DMS and acrylase or acrylic acid. The authors found that acrylic acid deterred grazing by two species of sea urchins on algae, and they suggest that this is due to an aversion to acidity by the urchin itself or that the acid irritates its gut microbes. While the evidence is not directly causative, as the authors showed a reaction to acrylic acid and not to DMSP-produced acrylic acid in vivo, it does suggest (with other evidence) that the important part of this reaction to the phytoplankton is not DMS, but rather its byproduct.
Smaller grazers, such as isopods, had no reaction to the acrylic acid in that paper. But a paper published in Science this week (July 16 2010) by Justin Seymour, Rafel Simo, and others looks into the effects of DMSP on the smallest grazers: microbes. Using “microfluid technology” (see details at end of post), the researchers measured the strength of attraction of 4 different types of microbes (7 species) to varying concentrations of DMSP, DMS, DMSO (dimethylsulfoxide, a DMS and DMSP degradation product), GBT (glycine betaine, a molecule analogous to DMSP in structure and function), and artificial seawater (as a control).
- Each of the 3 species of autotrophic plankton reacted differently to DMSP in the water. The algae Micromonas pusilla showed strong attraction to DMSP, taking it up presumably as a carbon and sulfur source. The cyanobacterium Synechococcus sp. showed no reaction. Most strangely, the algae Dunaliella tertiolecta moved very strongly toward DMSP, but not to assimilate it directly; rather, it cleaved the molecule into DMS extracellularly and potentially assimilated that molecule instead. The authors do not know why this action occurs.
- Two species of bacteria, Pseudoalteromonas haloplanktis and Silicibacter sp., each moved toward the DMSP for assimilation as part of their carbon and sulfur requirements.
- Two consumers, one a herbivore to eat the algae itself (Oxyrrhis marina) and the other a bacteriovore which strove to eat the bacteria consuming the DMSP, each showed positive chemotaxis and moved toward the DMSP source.
This last part is the most interesting: these two microbe species use the DMSP as a chemical signal that there is food around. Out of all the molecules that could leak from the burst cell and indicate prey, it is this very molecule, DMSP, that does the trick.
But wait: didn’t the 2001 paper I just wrote about suggest that DMSP is a chemical defense of phytoplankton? What is it doing drawing in its own predators? The authors suggest that previous studies have flawed experimental design, releasing far too much bulk DMSP into the environment in contrast to their own “microfluid technology.” Previous studies, such as a 1997 Nature paper by Gordon Wolfe and a 2003 paper by Suzanne Strom, found that O. marina has a higher tolerance to digesting DMSP and is less repelled than other species. More work should be done in order to get to the root of this contradiction.
Thus far, we have DMSP attracting bacteria to consume the DMSP itself, drawing in an herbivore to consume the DMSP-producer, and a bacteriovore attracted to the DMSP in order to find its own bacterial prey. This is not the end of the story, as DMSP is a prey indicator at higher trophic levels as well. A 2008 Science paper out of UC-Davis and UNC found that planktivorous fish use DMSP as a foraging cue, aggregating near DMSP hotspots. Furthermore, Gabrielle Nevitt reviewed literature in 2008 on seabirds (Order: Procellariiformes) using DMS as an olfactory cue to identify patches of its own prey, fish and squid, feeding on the zooplankton and its phytoplankton prey. A similar pattern has also been found in seals and whale sharks.
The evolutionary implications of this are astounding. It seems as though many molecules released from a leaky phytoplankton cell could be used as indicators of these clusters of consumption. However, DMSP has something special: sulfur. We all know that smell, and perhaps it is this stinkiness that has allowed it to become such a pervasive indicator throughout the marine food web. In her review, Nevitt discusses the evolution of DMS-sensitivity in seabirds, and using phylogenetic trees, shows that only the species that are reared in dark burrows, relying on smell alone to identify food, currently have DMS-sensitivity. How did this apparent convergent evolution occur? Is it convergent? (I have no answers to these questions.)
Are there any implications for climate in these findings, as DMSP is indirectly responsible for increased albedo (sunlight reflection) in our atmosphere? I doubt that there are any direct consequences that we can enumerate. As all biogeochemists know, the stuff of the air frequently comes from the stuff we live on and in: soil and water. This is simply another tie to the way microbes and abiotic stuffs relate to climate-regulating molecules. The authors of this week’s Science paper note that “microbial behaviors, played out over microscale chemical landscapes, shape planktonic food webs while potentially influencing climate at global scales.” DMS as a prey cue should create a positive feedback loop, drawing more herbivores to open more cells and leak increasing DMSP, which in turn draws more herbivores. Some studies show varying ties of DMSP production to species, light, temperature and salinity (review by Stefels et al. here), but it seems to me that the DMS-as-prey-cue and DMS-as-climate-regulator processes are unlinked, so would not work together in any predictable way.
If you take nothing away, take this: sometimes the universe is more connected than we can imagine.
(Sidenote: should I give up strict science and become a science illustrator?)
NOTES ON MICROFLUID TECHNOLOGY:
The idea behind this technique is that microbes inhabit a “dynamic and patchy nutrient landscape” in which nutrient levels vary over micrometer scales. The microfluidic device is a chamber designed with the “objective of creating a diffusing band of chemoattractant, to simulate an ephemeral, microscale nutrient patch.” There is a chamber in the center into which fluorescence-labeled chemoattractant is added to the desired concentration, and then input is cut off. Thus the chemical will dissipate slowly through the closed chamber, trying to imitate the open ocean. The researchers then add their microorganisms, and measure their distribution and the distribution of the fluorescent chemical. This allows the researchers to track the intensity and location of the chemical, as well as the behavior of single organisms.
This information is from a paper in Limnology and Oceanography: Methods by J.R. Seymour, T. Ahmed, and R. Stocker entitled “A microfluidic chemotaxis assay to study microbial behavior in diffusing nutrient patches” (2008: 6 (477-488)). A pdf copy of this paper is available on Roman Stocker’s webpage, here (pdf warning!).
Here’s a picture of the device, thanks to Roman Stocker. The blue tube is the microbe input, the green tube is chemical input, and the red tube is for drawing out waste. It sits on top of a microscope.
DeBose, J., Lema, S., & Nevitt, G. (2008). Dimethylsulfoniopropionate as a Foraging Cue for Reef Fishes Science, 319 (5868), 1356-1356 DOI: 10.1126/science.1151109
Nevitt, G. (2008). Sensory ecology on the high seas: the odor world of the procellariiform seabirds Journal of Experimental Biology, 211 (11), 1706-1713 DOI: 10.1242/jeb.015412
Seymour, J., Simo, R., Ahmed, T., & Stocker, R. (2010). Chemoattraction to Dimethylsulfoniopropionate Throughout the Marine Microbial Food Web Science, 329 (5989), 342-345 DOI: 10.1126/science.1188418
Simó, R. (2001). Production of atmospheric sulfur by oceanic plankton: biogeochemical, ecological and evolutionary links Trends in Ecology & Evolution, 16 (6), 287-294 DOI: 10.1016/S0169-5347(01)02152-8
Stefels, J., Steinke, M., Turner, S., Malin, G., & Belviso, S. (2007). Environmental constraints on the production and removal of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling Biogeochemistry, 83 (1-3), 245-275 DOI: 10.1007/s10533-007-9091-5
Van Alstyne, K., Wolfe, G., Freidenburg, T., Neill, A., & Hicken, C. (2001). Activated defense systems in marine macroalgae: evidence for an ecological role for DMSP cleavage Marine Ecology Progress Series, 213, 53-65 DOI: 10.3354/meps213053
G. V. Wolfe, M. Steinke, & G. O. Kirst (1997). Grazing-activated chemical defence in a unicellular marine alga Nature, 387, 894-897