Frightened birds make bad parents

Song sparrow chicks. Photo by Tobyotter.

ResearchBlogging.orgPredators have an obvious impact on their prey: eating them. But if the threat of predators prompts prey species to change their behavior, those behavioral changes can also affect prey population dynamics [$a]—and thereby, potentially, the prey’s evolution—even if the predators never actually catch any prey.

This is the effect documented in a short, sharp study just published in Science, in which Liana Y. Zanette and her coauthors show that song sparrows raise fewer chicks if they simply think that there are predators nearby [$a].

The team’s experimental design was simple but probably pretty work-intensive. Over the course of one summer on several small islands off the coast of British Columbia, they watched song sparrows choose mates and build nests. Once nests were established, the team surrounded them with anti-predator defenses: netting and electrified fences. They confirmed that these measures kept predators out with regular video surveillance. And then they turned on the loudspeakers.

At some nests, the team broadcast looped recordings of calls made by song sparrow predators—raccoons, crows and ravens, hawks, owls, and cowbirds. At control nests, the broadcast was instead a playlist of similar-sounding calls made by non-predators, including seals, geese, hummingbirds, and loons. The team then monitored the nests, recording the behavior of the mated pair at each nest, and the ultimate success of the eggs they laid.

An adult song sparrow, looking watchful. Photo by kenschneiderusa.

The results are pretty unambiguous. Pairs of song sparrows that heard predator calls laid fewer eggs than pairs that heard non-predators. Of the eggs laid by pairs who heard predator calls, fewer hatched, and of those hatched chicks, fewer survived fledge. Just the continuous, threat of predators—predators that were never visible—reduced the number of chicks the sparrows fledged.

The reasons for the reduced offspring are apparent from other behavioral observations. Birds in the predator-call treatment were perpetually on high alert, as measured by “flight initiation distance,” the distance up to which a researcher could approach the nest before the birds took flight. Sparrows in the non-predator treatment let researchers get about 120 meters from the nest before taking off; sparrows in the predator treatment wouldn’t tolerate humans within twice that distance. In the predator treatment, sparrows spent less time sitting on their eggs, and visited to feed their chicks less frequently. Not surprisingly, chicks in the predator treatment also gained less weight than chicks in the non-predator treatment.

And, in what may be the most poignant data set I’ve ever seen in print, the team also measured the skin temperature of chicks in each nest 10 minutes after the parents had left. Chicks in the predator-call treatment were measurably, and significantly, colder.

So the simple fear of predators is enough to prompt free-living song sparrows to lay fewer eggs, and raise fewer of the eggs they do lay to fledging. However, the absolute difference in offspring between sparrow pairs in the predator and non-predator treatments—40%—probably reflects the maximum effect we might expect to see in natural populations.

That’s because left to themselves, sparrows probably seek nesting spots with less predator activity. Here, all the sparrows had established nests in what, presumably, were the best spots they could find—but for half of them, the new neighborhood suddenly seemed to become a lot less safe shortly after they settled in. What Zanette et al. document is very much a behavioral, short-term response, and it’s one that many prey animals may be able to mitigate, or avoid altogether, with other behavioral responses. It’s hard to say how exactly it reflects the impact that fear of predators might have in sparrow populations unmolested by ornithologists.

Nevertheless, this result does suggest that for many prey animals, the fear of predators can, itself, be something to fear. ◼


Creel, S., & Christianson, D. (2008). Relationships between direct predation and risk effects. Trends in Ecology & Evolution, 23 (4), 194-201 DOI: 10.1016/j.tree.2007.12.004

Martin, T. (2011). The cost of fear. Science, 334 (6061), 1353-4 DOI: 10.1126/science.1216109

Zanette, L., White, A., Allen, M., & Clinchy, M. (2011). Perceived predation risk reduces the number of offspring songbirds produce per year. Science, 334 (6061), 1398-1401 DOI: 10.1126/science.1210908

Nothing in Biology Makes Sense: Making sense of the latitudinal biodiversity gradient

Tropical forest along the Inca Trail in Peru. Photo by TheFutureIsUnwritten.

This week at Nothing in Biology Makes Sense!, Noah Reid describes a new study that tries to explain the latitudinal biodiversity gradient—that is, the reason why a tropical rainforest has so many more species than, say, the mighty forests of British Columbia.

Almost invariably across taxonomic groups, hemispheres and continents, as one moves from polar regions towards the equator, species diversity increases (see the figure for a depiction of global bird diversity). The concept of diversity here can be broken down into three parts: “alpha diversity” or the diversity of species in a single location; “beta diversity”, or the turnover of species observed when moving among locations; and “gamma diversity” or the diversity of species found in an entire region. The latitudinal diversity gradient holds true for all three elements.

To find out what the new study reveals, go read the whole thing. ◼

Flowers stay open for pollinators, not daylight

A honeybee explores the depths of a dandelion, one of the species used in Fründ et al.‘s experiments. Photo by je-sa.

ResearchBlogging.orgIf you’ve ever stopped to admire morning glory flowers opening first thing in the morning, then noticed they’ve closed by evening, you’re at least dimly aware of one of the longest-established ideas in plant biology: that flowers open and close on a reliable daily schedule. Different species are open at different times of day, of course, but each flowering plant has its preferred open period, and it sticks to that schedule during its flowering season.

This idea led Carolus Linneaus, the father of modern biological taxonomy, to propose an Horologium florae, or “floral clock” using plantings of species with known flowering times to mark the hours. You can find his table of proposed species in the online version of Linneaus’ 1783 treatise Philosophia Botanica, if you’re not averse to Latin. Studies of flowers’ daily schedules go back to well before English was the language of international science, and continue to the present day [$a].

Yet no one seems to have spent much time considering how flowers’ schedules might respond to the activity of their very reason for being: pollinators. Flowers don’t open just to be open in a particular kind of sunlight—they’re open to attract animals that can carry pollen to another plant, and maybe leave some, too. If a flower receives enough pollen to make seeds by noon, why would it stay open until two o’clock?

According to some new experimental results, the answer to that question is that they don’t [$a].

Jochen Fründ, Carsten F. Dormann, and Teja Tscharntke set out to see whether a selection of European wildflowers adjusted their opening schedules in response to pollination, with two major experiments and a broader-scale observation project. The experiments address whether pollinator activity could change flowers’ schedules; the observations help determine how important those changes might be in studies of plant-pollinator interaction.

A floral clock in Geneva—not quite what Linneaus had in mind. Photo by aranmanoth.

In the first experiment, the team planted wildflowers—Crespis capillaris, a close relative of common dandelions—in experimental plots spaced across a field. Plots were either caged or left open to insect visitors, and Fründ et al introduced bees into some of the caged plots. So some plots had a controlled set of pollinators, some had none at all, and some had whatever pollinators were already active in the field.

The team then watched the flowers’ daily opening and closing in the experimental plots. (They had a lot of help—a long list of names in the paper’s Acknowledgements section ends with “and many others.”) Over the same period of time, flowers in the un-caged plots received more insect visitors than flowers in either other treatment, and had mostly closed by midafternoon; flowers in the caged plots with bees introduced received fewer visitors and closed hours later; and flowers in the plots with no pollinators at all stayed open till evening.

So flowers experiencing the same daylight pattern closed earlier if they received more pollinator visits. The team followed up this result by hand-pollinating flowers of C. capillaris and a handful of closely related species growing in the same field, including dandelions—and flowers of three out of four species closed more rapidly when hand pollinated. Dandelions didn’t respond to hand pollination, a result the authors explain by noting that dandelions often self-pollinate, and so don’t need to wait for animal pollinators.

Finally, the team compiled observations of plant-pollinator interactions from sites similar to their study field located across Germany, and divided them into observations taken before solar noon, when the focal flower species from the experiments above tend to be open, and after solar noon. Which pollinator species visited which flowering plants depended significantly on when the observations were made—to the extent that the apparent importance of C. capillaris and its relatives is entirely different before and after noon.

Of course, these results apply directly to only a handful of species representing a particular group of flowering plants—but it’s a group with a lot of widespread and abundant members, and the result is straightforward and striking. Animal-pollinated plants may not behave much like clocks at all. Instead, they’re more like the patrons of a singles bar: they show up at about the same time and hang around until they find someone to buy them a drink. That’s a dynamic worth keeping in mind for studies of plant-pollinator interaction, since it suggests that the partners a pollinator chooses will depend, at least in part, on whether or not it’s out after closing time. ◼


Ewusie, J., & Quaye, E. (1977). Diurnal periodicity in some common flowers. New Phytologist, 78 (2), 479-485 DOI: 10.1111/j.1469-8137.1977.tb04854.x

Fründ, J., Dormann, C., & Tscharntke, T. (2011). Linné’s floral clock is slow without pollinators – flower closure and plant-pollinator interaction webs. Ecology Letters DOI: 10.1111/j.1461-0248.2011.01654.x

von Hase, A., Cowling, R., & Ellis, A. (2005). Petal movement in cape wildflowers protects pollen from exposure to moisture Plant Ecology, 184 (1), 75-87 DOI: 10.1007/s11258-005-9053-8

#ESA2011 #ESA11: Who to follow

Update, 9 August 2011: I seem to have picked the wrong hashtag–there’s more activity at #ESA11.

Western scrub jay. Photo by Minette Layne.

The annual meeting of the Ecological Society of America is underway in Austin, Texas, this week. If, like me, you’re not anywhere near Austin, do not despair. There are people who will use the Internet to tell you what is going on at the meetings anyway, out of sheer enthusiasm for ecology! Here are the ones I’m following:

Thanks in part to readers like you, Sarcozona will be covering the meeting at Gravity’s Rainbow. Zen Faulkes of NeuroDojo has apparently been there since Day 0. And Jeremy Fox has been anticipating the meeting for the last week over at the OIKOS blog. Finally, you can follow the official ESA twitter feed and the hashtag #ESA2011 #ESA11 for continuous updates. ◼

Queering ecology

Eastern bluebird, car. Photo by Automania.

Via Kate Clancy at Context and Variation: Alex Johnson takes a look at the way we think and write about the natural world, and finds it wanting.

Our culture sets Nature as the highest bar for decorum, while simultaneously giving Nature our lowest standard of respect. Nature is at our disposal, not only for our physical consumption, but also for our social construction. We call geese beautiful and elegant and faithful until they are shitting all over the lawn and terrorizing young children. Then we poison their eggs. Or shoot them.

Having popped the naturalistic fallacy with a few pokes, Johnson proposes queering ecology—a deliberate reference to the term’s usage in human sexuality—to better acknowledge the complications of the natural world and humans’ relationships to it. That summary doesn’t do the work justice, though—go read the whole thing.

(Kate linked to this more-or-less alongside my first volley in the old adaptive homophobia kerfuffle, but Johnson’s essay is another order of thought altogether. Also, how cool is it that I can just go to Flickr and find an illustration for Johnson’s point with a simple keyword search? Pretty cool, I think.)

Aphid-tending ants cull the sick from the herd

ResearchBlogging.orgJust released online at Biology Letters: aphid-tending ants have been observed to selectively remove sick members of their “herd” [$-a].

Most aphid species produce some sort of sweet honeydew as waste while feeding on their host plants; ant-attended aphid species use this honeydew to attract ants. In many cases, the ants “milk” the aphids by stroking them to prompt release of the honeydew. While exploiting a colony of aphids, ants defend it as a food resource, protecting the aphids from predators. Aphid species that commonly rely on ant protection often lack defensive adaptations [$-a] found on species that don’t interact with ants.

Ants tend aphids on a milkweed plant. Photo by dmills727.

Niesen et al. report the results of experiments performed ants attending colonies of milkweed aphids, Aphis asclepiadis, which are susceptible to a fungal pathogen that can wipe out aphid colonies in a matter of days. In two experiments, they introduced aphids into the ant-attended colonies, and tracked what the ants did to them. They found that

  • Ants were more likely to remove the corpses of fungus-killed aphids than either the corpses of aphids killed by freezing or introduced live aphids; and
  • Ants were more likely to remove live aphids contaminated with fungal spores (conidia) than live aphids without spores.

The authors speculate that this behavior is a re-application of ants’ treatment of their own sick and dead within the colony. It seems clear that it should have benefits to both ants and aphids in this new context, slowing or preventing the spread of the fungus within an aphid colony. This benefit isn’t directly tested by Nielsen et al., but such an experiment is a logical next step.


Nielsen, C., Agrawal, A., & Hajek, A. (2009). Ants defend aphids against lethal disease Biology Letters DOI: 10.1098/rsbl.2009.0743

Way, M. (1963). Mutualism between ants and honeydew-producing Homoptera. Ann. Rev. Entomology, 8 (1), 307-44 DOI: 10.1146/annurev.en.08.010163.001515

Invasive species not so bad?

Over on Slate, Rebecca Tuhus-Dubrow says some conservation biologists are starting to question the importance of preventing species invasions:

Certainly, they say, non-native plants and critters can be terribly destructive—the tree-killing gypsy moth comes to mind. Yet natives such as the Southern Pine Beetle can cause similar harm. The effects of exotics on biodiversity are mixed. Their entry into a region may reduce indigenous populations, but they’re not likely to cause any extinctions (at least on continents and in oceans—lakes and islands are more vulnerable). Since the arrival of Europeans in the New World, hundreds of imports have flourished in their new environments.

Tuhus-Dubrow cites the case of Tamarisk in the U.S. Southwest — an aggressive introduced shrub that has also ended up providing important nesting sites for the endangered southwestern willow flycatcher.

The fact of the matter is that human-introduced species can eventually integrate into an ecological community; once they do it’s hard to get them out, and problematic as to whether it’s a good idea. In Australia, dingoes helped extirpate many other large predators when they were introduced by the first humans to arrive on that continent — and now they’re critical to controlling other, later-introduced mammal species.

(Thanks to Ephraim Zimmerman for point this one out to me!)

Invasive pest, or critical flycatcher habitat? Maybe both. Photo by Anita363.

How to synchronize flowering without really trying

This post was chosen as an Editor's Selection for ResearchBlogging.orgOne way plants can gain an advantage in their dealings with pollinators, seed dispersers, or herbivores is to act collectively. For instance, when oak trees husband their resources for an extra-big crop of acorns every few years instead of spreading them out, acorn-eating rodents are overwhelmed by the bumper crop, and more likely to miss some, or even forget some of the nuts they cache. These benefits of synchronized mass seed production, or “masting,” are straightforward, but how it happens is less clear. A paper in the latest issue of Ecology Letters has an answer — synchronization happens accidentally [$-a].

Bumper acorn crops ensure that squirrels miss a few. Photo by douglas.earl.

When Dan Janzen first described masting as an adaptation in plants’ coevolution with seed predators, he proposed that “an internal physiological system” [$-a] acted as a timer between masting events, with masting ultimately triggered by weather conditions. However, mathematical models have suggested a different possibility, the “resource-budget hypothesis:” that masting synchronization arises through an interaction of resource and pollen limitation [$-a].

Resource limitation works in concert with pollen limitation by catching plants at two stages of the seed-production process. First, if the resources required for seed production are more than can be accumulated in a single year, or if the availability of resources varies from year to year, then some years will be spent building up reserves instead of producing flowers. When reserves are built up, seed production is limited by the availability of pollen to fertilize flowers. Plants that flower when most of the rest of the population doesn’t will fail to set much seed, so they’ll have reserves to make seeds in the next year. This doesn’t require Janzen’s “internal physiological system” for the plants to synchronize, although such a system might evolve to reduce the likelihood of wasting resources by flowering out of synch.

The new paper tests this model in populations of a western U.S. wildflower, Astralagus scaphoides, which flowers at high frequency every alternate year. The authors prevented seed production in the plants by removing their flowers, either in a “press” of three years in a row or in a single “pulse” during one high-flowering year. The plants’ response to these treatments would reveal the role of resource and pollen limitation in synchronizing seed production.

If resource depletion after fruit set prevents reproduction in successive years, we predicted that ‘press’ plants would flower more than control plants every year, as they were never allowed to set fruit. We predicted that ‘pulse’ plants would flower again in 2006, but not set fruit due to density-dependent pollen limitation in a low-flowering year.

The authors also measured the sugars stored in the roots of plants collected before and after flowering in a high-flowering year.

Seed predator in action. Photo by tombream07.

The resource-budget hypothesis worked. Plants prevented from setting seed were forced out of synch with the rest of the population. “Pulse” plants flowered the year after treatment, but because few other plants did, they received little pollen and set little seed. They then had resources to flower yet another year, with the rest of the population this time, and set much more seed, depleting their reserves and bringing them back into synch. “Press” plants continued to flower at high rates each year, as long as they were prevented from setting any seed. Sugar levels built up in the tested roots during non-flowering years, and dropped after high-flowering years.

So masting arises as an emergent result of two limitations acting on plants — the resources needed to make seed, and good access to pollen. A couple of simple rules lead, undirected, to an ordered system that affects entire natural communities.


Crone, E., Miller, E., & Sala, A. (2009). How do plants know when other plants are flowering? Resource depletion, pollen limitation and mast-seeding in a perennial wildflower. Ecology Letters, 12 (11), 1119-26 DOI: 10.1111/j.1461-0248.2009.01365.x

Janzen, D. (1971). Seed predation by animals Ann. Rev. Ecol. Syst., 2 (1), 465-92 DOI: 10.1146/

Janzen, D. (1976). Why bamboos wait so long to flower Ann. Rev. Ecol. Syst., 7 (1), 347-91 DOI: 10.1146/

Satake, A., & Iwasa, Y. (2000). Pollen coupling of forest trees: Forming synchronized and periodic reproduction out of chaos. J. Theoretical Biol., 203 (2), 63-84 DOI: 10.1006/jtbi.1999.1066

With or without you? Species interactions and responses to climate change

ResearchBlogging.orgReading a pair of papers recently published in PLoS ONE, you might be forgiven for thinking that ecologists don’t know whether or not interactions between species matter. Both examine the effects of climate change on ecological communities — but where one assumes that species in a community are as interchangeable as bricks in a wall, the other concludes that the presence of competitors is pretty important.

First, Stralberg et al. attempt to predict what will happen to the birds of California under projected climate change. They constructed individual models of each bird species’ environmental requirements, and then figured out where those requirements would be met under a range of possible climate change scenarios. They find, not surprisingly, that this produces a lot of never-before-seen bird communities:

Our analysis suggests that, by 2070, individualistic shifts in species’ distributions may lead to dramatic changes in the composition of California’s avian communities, such that as much as 57% of the state … may be occupied by novel species assemblages.

But do species really move across the landscape as independent agents? It’s hard to believe that the do. Every species interacts with others — competitors, predators, prey, parasites — and presumably these interactions have some impact on where that species can survive.

How far can this common crossbill move its range if its favorite food tree doesn’t come along? Photo by omarrun.

That’s certainly what the other paper suggests. Adler et al. tested the effects of altered water availability (as a proxy for climate change: normal, supplemental, or drought conditions) and competition (normal or with competitors removed) on experimental plantings of three different prairie grass species. They found significant effects of both competition and rainfall on the plantings’ growth — although there wasn’t a meaningful interaction between the two factors. (That is, competition conditions didn’t alter the effect of water availability.)

There are actually a lot of studies suggesting that species interactions will be important in determining how communities cope with changing climates:

All of which is to say, we may not know how the species interactions within a particular community will shape its response to climate change, but there’s good reason to think that they will.


Adler, P., Leiker, J., & Levine, J. (2009). Direct and indirect effects of climate change on a prairie plant community PLoS ONE, 4 (9) DOI: 10.1371/journal.pone.0006887

Pelini, S., Dzurisin, J., Prior, K., Williams, C., Marsico, T., Sinclair, B., & Hellmann, J. (2009). Translocation experiments with butterflies reveal limits to enhancement of poleward populations under climate change Proc. Nat. Acad. Sci. USA, 106 (27), 11160-5 DOI: 10.1073/pnas.0900284106

Post, E., & Pedersen, C. (2008). Opposing plant community responses to warming with and without herbivores Proc. Nat. Acad. Sci. USA, 105 (34), 12353-8 DOI: 10.1073/pnas.0802421105

Stralberg, D., Jongsomjit, D., Howell, C., Snyder, M., Alexander, J., Wiens, J., & Root, T. (2009). Re-shuffling of species with climate disruption: A no-analog future for California birds? PLoS ONE, 4 (9) DOI: 10.1371/journal.pone.0006825

Visser, M., Holleman, L., & Gienapp, P. (2005). Shifts in caterpillar biomass phenology due to climate change and its impact on the breeding biology of an insectivorous bird Oecologia, 147 (1), 164-72 DOI: 10.1007/s00442-005-0299-6

A helpful invasive species?

This post was chosen as an Editor's Selection for ResearchBlogging.orgIntroduced species can wreak havoc on the ecosystems they invade. But what happens after they’ve been established for centuries? A new study in the latest Proceedings of the Royal Society suggests that, in one case, an introduced species has actually become an important part of the native ecosystem — and helps protect native species from another invader [$-a].

Dingoes (above) control red
foxes, which is good for native
Photos by ogwen and

The introduced species in question is the Australian dingo, the wild descendant of domestic dogs [$-a] that moved Down Under with the first humans to settle the continent. Today, 5,000 years after their introduction, dingoes are the largest predator in much of Australia, and they were a prominent part of the ecosystem encountered by European settlers. Europeans, like previous waves of human arrivals, brought their own domestic and semi-domestic animals — including red foxes, which prey on small native mammals.

The new study’s authors hypothesized that because dingoes reduce red fox activity both through direct predation and through competition for larger prey species, dingoes should reduce fox predation on the smallest native mammals. At the same time, dingoes prey on kangaroos, the largest herbivore in the Australian bush — and reducing kangaroo populations should increase grass cover, providing more habitat for small native mammals. When the authors compared study sites with dingoes present to sites where dingoes had been excluded to protect livestock, this is what they found: increased grass cover, and greater diversity of small native mammals where dingoes were present.

Recently a news article in Nature discussed ragamuffin earth [$-a] — the idea that human interference in nature has so dramatically changed natural systems that it may often be impossible to restore “pristine” ecological communities. In these cases, some ecologists say, conservation efforts might be better focused on how to maintain and improve the diversity and productivity of the novel ecosystems we’ve inadvertently created. It looks as though the dingo could be a poster child for exactly this approach.


Letnic, M., Koch, F., Gordon, C., Crowther, M., & Dickman, C. (2009). Keystone effects of an alien top-predator stem extinctions of native mammals Proc. R. Soc. B, 276 (1671), 3249-3256 DOI: 10.1098/rspb.2009.0574

Marris, E. (2009). Ecology: Ragamuffin Earth Nature, 460 (7254), 450-3 DOI: 10.1038/460450a

Savolainen, P. (2004). A detailed picture of the origin of the Australian dingo, obtained from the study of mitochondrial DNA Proc. Nat. Acad. Sci. USA, 101 (33), 12387-90 DOI: 10.1073/pnas.0401814101