Eavesdropping on antshrikes

Growing up in the Spy vs. Spy era, and a bit later in the Watergate age, I developed a keen appreciation for clandestine operations, which I assumed at that time were unique to human culture.  As it turns out, eavesdropping is practiced by many different species for a variety of reasons. One important example occurs in bird flocks composed of several species of birds. Antshrikes (Thamnomanes ardesiacus) are sentinel species in multi-species flocks because they produce alarm calls when they spot a predacious raptor flying overhead, alerting other nearby birds of the threat. Ari Martinez and his colleagues wondered whether hanging out with antshrikes allowed these other bird species to expand their niches to forage in areas that might otherwise be too dangerous.

Alarm calling species Thamnomanes ardesiacus Photo cred E. Parra 600dpi (1)

An antshrike perched in the Amazonian rainforest. Credit: E. Parra.

This fear-based niche shift hypothesis makes two related predictions.  First, in the absence of antshrikes, the remainder of the flock should shift its range to areas with lower predation risk.  Second, without antshrikes some birds might leave the flock entirely, because without sentinel services they no longer benefit from hanging with other birds. To test these predictions, Martinez and his colleagues identified eight flocks of 5-8 species (including antshrikes) in a tropical lowland forest in southeastern Peru.  They established four removal flocks from which they removed all antshrikes after capturing them in mist nets. They left four control flocks, in which they captured all antshrikes, but then returned them to the flock (to control for the effects of handling).

Group banding and mist netting birds photo ced Micah Reigner

Research team mist-netting and measuring antshrikes.  Credit Micah Reigner

To determine where the flock was spending its time, researchers used a GPS device every 10 minutes to record the center of the flock. They also censused each flock for species composition from dawn to dusk for three days before removal and three days after removal. In control flocks, home range overlapped extensively (average of 69%) when comparing the first (pre-removal) and second (post-removal) three-day period. In removal flocks, there was only 8% overlap in home range, indicating that the remaining flock was shifting its range when antshrikes were gone.

MartinezFig1

Home ranges of a control flock (top) and a flock which had antshrikes removed (bottom). Red color indicates home range during the three day pre-removal period, while blue color indicates home range during the three day post-removal period.  Deeper colors indicate greater occupancy. 

But are the remaining species shifting their niches to safer locations when antshrikes are no longer available as sentinels? To answer this question the researchers measured the presence or absence of vegetation cover at different height intervals every 10 minutes at the center of the flock. Comparing the second (post-removal) to the first (pre-removal) period, the removal flocks (those without antshrikes) moved into understory vegetation (0-8 meters high) that was substantially denser than was the vegetation inhabited by the control flocks (those with antshrikes). Presumably, dense understory protects birds without sentinels from being spotted or captured by raptors flying overhead. These dense understory areas are usually associated with less tree cover at higher height intervals (above 16 meters), which allows more sunlight to reach the forest floor, resulting in lush vegetation growth.

MartinexFig3

Proportion change in vegetation cover occupied by flocks from pre-trial to post-trial period at different height intervals.  Positive numbers indicate an increase in vegetation density. Error bars are 95% confidence intervals. Data are based on the behavior of four control and four removal flocks.

Flocking occurrence is the proportion of time individuals of a particular species spend in flocks.  The fear-based niche shift hypothesis predicts that flocking occurrence should decrease when sentinel species are removed because the benefits of flocking are reduced for the remaining species. When the researchers compared post-removal to pre-removal time-periods, five species showed strong reductions in flocking occurrence for removal flocks in comparison to control flocks, two were unchanged, and one species showed an increase in flocking occurence.

MartinezFig2

Change in proportion flocking occurrence for eight different flocking species in control and removal flocks.  Error bars are 95% confidence intervals.  Chlorothraupis carmioli (CHCA), Epinecrophylla erythrura (EPER), Epinecrophylla leucophthalma (EPLE), Glyphorynchus sprirus (GLSP), Hylophilus ochraceiceps (HYOC), Myrmotherula longipennis (MYLO), Myrmotherula menetriesii (MYME), Xiphorhynchus elegans (XIEL).

The authors emphasize that though flocking occurrence decreased for most species, the flocks did remain intact, which indicates that there are probably other benefits from flocking besides the opportunity to eavesdrop. There might be safety in numbers – a decrease in individual mortality as group size increases, or the possibility that the remaining flock members do provide some information about imminent predator attacks.

Martinez and his colleagues conclude that sentinels help other bird species succeed in tropical rainforests, thriving in dangerous habitats where they might otherwise fear to tread.  These species may provide important ecosystem services, such as dispersing seeds and eating herbivorous insects that threaten plants that are the foundation of these tropical ecosystems.

note: the paper that describes this research is from the journal Ecology. The reference is Martínez, A. E., Parra, E. , Muellerklein, O. and Vredenburg, V. T. (2018), Fear‐based niche shifts in neotropical birds. Ecology, 99: 1338-1346. doi:10.1002/ecy.2217. 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.

 

Parrotfish put on their big boy pants

While it would be awesome if parrotfish were named for their conversational abilities, it turns out that they earn their moniker for their specialized teeth that are fused together for scraping algae from coral, thus resembling a parrot’s beak. Despite lacking verbal skills these fish are incredible. Approximately 100 species occupy reefs, rocky coastlines and eelgrass meadows in tropical and subtropical waters. Many species are sequential hermaphrodites, beginning life as females and then changing into males after reaching a certain size. While female reproductive success is limited by the number of eggs she can produce, male reproductive success can be much higher if he can fertilize the eggs of many females.  So if a parrotfish transitions into a large male, and can control access to numerous females, he will enjoy greater reproductive success than if he had remained a female.

C. spilurusBrettTaylor

Two Chlorurus spilurus parrotfish show off their teeth and colors.  The large colorful fish on the right is a male, while the smaller darker fish to his left is a female. Credit: Brett Taylor.

Phenotypic plasticity describes the ability of an individual with a particular genetic makeup to vary in a variety of traits (such as what it looks like, or how it behaves) in response to different environmental conditions. About 15 years ago, Nick Gust’s PhD research on tropical reef fish revealed that tremendous variation in parrotfish traits existed over a distance of a few kilometers. But what causes this variation? When funding became available, Brett Taylor jumped at the opportunity to pinpoint the causes, focusing on the diverse parrotfish community in the Great Barrier Reef (GBR).

GBRChlorurus_microrhinos_AD_RR6_2

Eastern slope of the Great Barrier Reef hosts a diversity of fish and coral species. Credit: Brett Taylor.

Taylor and his colleagues surveyed 82 sites within 31 reefs across 6 degrees of latitude in the northern GBR. To standardize data collection, divers, armed with a multitude of cameras and GPS devices, swam at a standardized rate (about 20 meters/minute) for 40 minutes per survey, recording each parrotfish along a 5 m wide swath. They collected data about the habitat and the environment, about the physical traits of each individual parrotfish (such as size and sex), and about the type and abundance of parrotfish and their predators present at each site.

DiverKendraTaylot

Researcher takes notes while conducting a dive.  Credit Kendra Taylor.

The researchers wanted to identify what factors influenced growth rate, maximum body size, and the size at sex change, and how these factors related to the parrotfish mating system. Four species of parrotfish were sufficiently abundant across the GBR to allow researchers to do this type of analysis.

TaylorFig1

Four parrotfish species  abundant along exposed outer shelf (yellow sites) and protected inner shelf (blue) regions of the Great Barrier Reef. Males are larger and more colorful.

The GBR varies structurally across a relatively small spatial scale of 40 – 100 km, with outer shelf regions (eastern) exposed to wave action, and inner shelf regions (western) relatively protected. All four species tended to change sex at a larger size in protected sites than they did at exposed sites. However, the differences are only compelling for two of the species: C. spilurus and S. frenatus. There were fewer data points for the other two species, so it is possible (but unknown) that they too would show a more pronounced trend if more data were available.

TaylorFig1bottom

Proportion terminal phase (sex-changed males) in relation to body size (measured to the fork of the tail) in exposed (yellow) and sheltered (blue) sites.

Not surprisingly, parrotfish grew larger in protected areas. Presumably, less wave action provided a more benign environment for rapid growth, both of parrotfish and their preferred food items (algae growing on rocks and coral).

TaylorFig2I

Standardized maximum size (Lmax) attained by parrotfish in sheltered vs. exposed sites.

The researchers were somewhat surprised that most other factors, such as latitude, coral cover, sea surface temperature, and predator abundance, had very little effect on the size at sex change. Rather, the size at sex change appears to be strongly influenced by the local size distribution. In protected habitats, parrotfish grow large and change sex at a large size, while in exposed habitats, parrotfish are smaller, and change sex at a smaller size.

But sex is never simple. Nick Gust’s PhD research showed that C. spilurus had different patterns of sexual allocation in protected vs. exposed areas. In protected areas, the mating system is haremic, with a large male defending a territory and servicing a harem of females. In exposed areas, the mating system is mixed; there still are large territorial males with their harems, but they compete with many more small males, and group spawning is much more prevalent. Theoretically, the presence of these small males may make it less worthwhile for a female to transition into a male, and may influence the optimal size for transitioning in exposed reefs. Given that we still don’t know the mating system details of the other parrotfish in this study, it will be fascinating to see if they too show similar patterns of haremic vs. mixed mating systems in relation to habitat structure.

note: the paper that describes this research is from the journal Ecology. The reference is Taylor, B. M., Brandl, S. J., Kapur, M., Robbins, W. D., Johnson, G., Huveneers, C., Renaud, P. and Choat, J. H. (2018), Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes. Ecology 99(3): 642-651. doi:10.1002/ecy.2127. 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.

Prey populations: the only thing to fear is fear itself

In reference to the Great Depression, Franklin Delano Roosevelt is famously quoted as stating during his 1933 inaugural speech “the only thing we have to fear is fear itself.” Roosevelt was no biologist, but his words could equally apply to a different type of depression – the decline of animal populations that can be caused by fear.

FDR

Roosevelt’s inauguration in 1933. Credit: Architect of the Capitol.

Ecologists have long known that predators can depress prey populations by killing substantial numbers of their prey. But only in the past two decades or so have they realized that predators can, simply by their presence, cause prey populations to go into decline. There are many different ways this can happen, but, in general, a predation threat sensed by a prey organism can interfere with its feeding behavior, causing it to grow more slowly, or to starve to death. As one example, elk populations declined after wolves were introduced to Yellowstone National Park. There are many factors associated with this decline, but one factor is fear of predators causes elk to spend more time scanning and less time foraging. Also, elk tend to stay away from wolf hotspots, which are often places with good elk forage.

Liana Zanette recognized that ecologists had not considered whether predator presence can cause bird or mammal parents to reduce the amount of provisioning they provide to dependent offspring, thereby reducing offspring growth and survival, and slowing down population growth. For many years, she and her colleagues have studied the Song Sparrow, Melospiza melodia, on several small Gulf Islands in British Columbia, Canada. In an early study, she showed that playbacks of predator calls reduced parental provisioning by 26%, resulting in a 40% reduction in the estimated number of nestlings that fledged (left the nest). But, as she points out, Song Sparrow parents provision their offspring for many days after fledging; she wondered whether continued perception of a predation threat during this later time period further decreased offspring survival and ultimately population growth.

Song sparrow

The Song Sparrow, Melospiza melodia. Credit: Free Software Foundation.

Zanette’s student, Blair Dudeck, did much of the fieldwork for this study. The researchers captured nestlings six days after hatching , weighed and banded them, and fit them with tiny radio collars. They then recaptured and weighed the nestlings within a few hours of fledging (at about 12 days post-hatching) to assess nestling growth rates.

sparrowbaby

Banded sparrow nestling with radio antenna trailing from below its wing. Credit: Marek C. Allen.

Three days after the birds fledged, Dudeck radio-tracked them, and surrounded them with three speakers approximately 8 meters from where they perched. For one hour, each youngster listened to recordings of calls made by predators such as ravens or hawks, followed, after a brief rest period, by one hour of calls made by non-predators such as geese or woodpeckers (or vice-versa). During the playbacks, Dudeck observed the birds to record how often the parents visited and fed their offspring, and whether offspring behavior changed in association with predator calls. This included recording all of the offspring begging calls.

BlairRadio

Blair Dudeck simultaneously uses a tracking device to locate Song Sparrows and a recorder mounted to his head to record their begging calls. Credit: Marek C. Allen.

Fear had a major impact on parental behavior. Parents reduced food provisioning vists by 37% when predator calls were played in comparison to when non-predator calls were played. They also fed offspring fewer times per visit, which resulted in 44% fewer meals in association with predator calls.

DudeckFig1

Mean number of parental provisioning visits (in one hour) in relation to whether predator (red) or non-predator (blue) calls were played. Error bars are 1 SE.

Hearing predator calls had no effect on offspring behavior – they continued to beg for food at a high rate, and did not attempt to hide.

Some parents were much more scared than others – in fact, some parents were not scared at all. The researchers measured parental fearfulness by subtracting the number of provisioning visits by parents during predator calls from the number of visits during non-predator calls. A more positive number indicated a more fearful parent (a negative number represents a parent who fed more in the presence of predator calls). The researchers discovered that more fearful parents tended to have offspring that were in poorer condition at day 6 and at fledging.

DudeckFig2

Offspring weight on day 6 (open circles) and at fledging (solid circles) in relation to parental fearfulness.  Higher positive numbers on x-axis indicate increasingly fearful parents.

Importantly, more fearful parents tended to have offspring that died at an earlier age. Based on this finding, the researchers created a statistical model that compared survival of offspring that heard predator playbacks throughout late-development with survival of offspring that heard non-predator playbacks during the same time period. They estimated a 24% reduction in survival. Combined with their previous study on playbacks during early development, the researchers estimate that hearing predator playbacks throughout early and late development would reduce offspring survival by an amazing 53%.

This “fear itself” phenomenon can extend to other trophic levels in a food web. For example recent research by Zanette and a different group of researchers showed that playbacks of large carnivore vocalizations dramatically reduced foraging by raccoons on their major prey, red rock crabs. When these carnivore playbacks were continued for a month, red rock crab populations increased sharply. This increase in crab population size was followed by a decline of the crab’s major competitor – the staghorn sculpin, and the crab’s favorite food, a Littorina periwinkle. Thus “fear itself” can cascade through the food web, affecting multiple trophic levels in important ways that ecologists are now beginning to understand.

note: the paper that describes this research is from the journal Ecology. The reference is Dudeck, B. P., Clinchy, M., Allen, M. C. and Zanette, L. Y. (2018), Fear affects parental care, which predicts juvenile survival and exacerbates the total cost of fear on demography. Ecology, 99: 127–135. 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.

Limpet larvae and their fantastic voyage

As he began his PhD program, Takuya Yahagi was puzzled by some laboratory findings. Juvenile red blood limpets, Shinkailepas myojinensis, seemed to survive and grow extraordinarily well at temperatures between 15-25° C. Adult limpets live in deep sea vent communities, where temperatures generally range between 6-11° C.

limpet photo

Adult Shinkailepas myojinensis.  These are approximately 6 mm in length. Credit: Takuya Yahagi.

Yahagi and his colleagues wondered why limpets are making babies that survive and grow at much higher temperatures than they are likely to experience after hatching.

Screen Shot 2017-07-04 at 10.48.26 AM

Deep sea hydrothermal vent community at 795 meters depth at Myojinsho Caldera in the northwest Pacific. White patches on the rocks are vast communities of chemosynthetic bacteria which are being grazed by purple/pinkish limpets. You can also see the white feathery feeding legs of a barnacle population in the upper portion of the photo. Credit: JAMSTEC

Yahagi reasoned that perhaps, in the natural world, the limpet juveniles live in different (warmer) environments than do their parents. If they migrated closer to the sea surface, their world would be somewhat warmer. But limpet babies are microscopic, so capturing them near the sea surface (and knowing that you had captured them!) is very challenging. Working with three other researchers, Yahagi decided to collect indirect evidence to test the hypothesis that baby limpets migrate to the surface where they feed and grow before returning to the ocean depths.

YahagiFig3

Larval S. myojinensis limpet 156 days after hatching. sh=shell, f =foot, e=eye, vl=velar lobe.

Initially, the researchers needed to determine what temperatures these growing limpets preferred. With the help of a remotely operated submarine, they collected adult limpets laden with egg capsules, and placed newly hatched larvae into separate containers under different conditions. Some larvae were fed and raised at one of six different temperatures: 5, 10, 15, 20, 25 and 30° C. Other larvae were starved at 5, 15 or 25° C to see how long they survived at different temperatures. If the larvae were migrating upwards to warmer waters, it was important to see how long they could survive until they arrived at the richer food sources near the surface.

Starved larvae survived up to 150 days at the lowest temperature, and for more than three weeks at 25° C, which provided ample time for upward migration (even at very mellow baby limpet swimming speeds). Fed larvae grew much more quickly at warmer temperatures, with best growth at 25° C, and no growth at 5-10° C, which is the approximate temperature at hydrothermal vents.. Larvae initially grew quickly at 30° C, but long term exposure to that temperature killed them.

YahagiFig4

Growth (shell length) of fed larvae at different temperatures.

These temperature profiles corresponded to temperatures at the sea surface down to about 100 meters, which ranged between 19-28° C. This correspondence supported the hypothesis that juveniles migrated upwards in the water column after hatching. But could Yahagi and his colleagues find any direct evidence for this vertical migration? To answer this question, they video-recorded new hatchlings in a clear plastic bath, and measured how fast these limpets swam, and what direction they preferred. They discovered that new hatchlings constantly swam upward in their test bath, and swimming speed was considerably faster at warmer temperatures.

The sea surface is a wonderful place to find food, because sunlight is abundant, so there are abundant phytoplankton to satisfy even the most voracious juvenile limpets. But sea surfaces also have very strong currents which can whisk juvenile limpets hundreds or thousands of kilometers away. The upshot is that vertical migration and wide dispersal of juveniles by ocean currents can introduce new genes into far-away limpet populations.

Screen Shot 2017-07-04 at 10.48.05 AM

A hot vent animal community at 700 meters depth at Minami-Ensei Knoll in the northwest Pacific. Prevalent groups include lobsters (white), two species of shrimp, mussels and two different limpet species. Credit: JAMSTEC.

Gene flow – the movement of genes from one population to another – has some important genetic impacts. Without gene flow, two populations that are separated from each other can become genetically distinct. But the mixing of genes from long-distance dispersal can prevent this from occurring. The researchers compared 1218 base pairs of the COI gene from 77 adult limpets that were collected from four different sites which were separated, in some cases, by more than 1000 kilometers. In support of the gene flow hypothesis they found no evidence of any genetic differentiation among the four populations.

Yahagi Fig1

Hydrothermal vent fields in the northwest Pacific Ocean.  Black squares are limpet collection sites for this study.  Notice the vast distances separating these populations.

Gene flow requires long distance dispersal, and the adult limpets travel very little along the sea floor. This finding of no genetic differentiation among the geographically separated populations supports the hypothesis that the juveniles migrate upwards, feed on abundant phytoplankton, and are carried to new distant environments. There, they mature and settle into new ocean vent communities where they can feed on the superabundant chemosynthetic bacteria associated with the ocean vents. But we still don’t know how limpets find a new ocean vent community – do they migrate, checking out possible vent habitats, while they are still juveniles and still capable of swimming? Do they have sense organs that pick up environmental cues such as hydrogen sulfide content, water temperature, turbulence or noise from vent emissions, to help them complete their fantastic ocean voyage?

note: the paper that describes this research is from the journal Ecology. The reference is Yahagi, Takuya, Hiromi Kayama Watanabe, Shigeaki Kojima, and Yasunori Kano. 2017. Do larvae from deep‐sea hydrothermal vents disperse in surface waters? Ecology 98: 1524-1534Thanks 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.

Golden Eagles: no tilting at windmills

Todd Katzner and several other scientists were puzzled by a vexing problem. They knew that the wind turbines at Altamont Pass Wind Resource Area (APWRA) were killing large numbers of Golden Eagles that flew into their spinning blades. Yet the population of Golden Eagles in the area had stayed relatively stable over the years despite this unnatural source of mortality. The researchers considered two possibilities. First, this population of eagles may have had unusually high birth rates or unusually low death rates from other sources to compensate for the high windmill-induced mortality. Alternatively, immigrant Golden Eagles might be replacing those killed by turbines.

Altamont Pass Wind Farm

Altamont Pass Wind Farm, California. Credit: Todd Katzner.

This question has important implications for conservation biologists. If immigrant Golden Eagles are replacing those killed by windmills at APWRA, then the apparent stability of the local Golden Eagle population may be at the expense of other populations that are providing APWRA with these immigrants. So, even though APWRA’s windmills are not directly causing local eagle populations to decline, windmills at APWRA (and other windmill sites) may be indirectly leading to a decline in other populations. So Katzner and his colleagues did genetic and molecular analyses of tissues remaining from these killed eagles to learn as much as they could about these eagles and where they came from.

Golden Eagle in flight

Golden Eagle in flight. Credit: Michael J. Lanzone.

The researchers used tissue samples from 67 eagles that were killed at APWRA between 2012-2014. They subjected these tissues to a variety of genetic tests to determine the sex and age of each individual, and to evaluate the genetic differences between individuals killed by the windmills.

In addition, Katzner and his colleagues used stable isotope analysis to evaluate whether the killed individuals were local birds, or immigrants from afar. For this analysis the stable isotope ratio is the ratio of a rare and nonradioactive isotope of hydrogen (2H) found in the sample (feathers of killed birds) in relation to the common isotope (1H). A feather’s stable isotope ratio is very tightly correlated to the stable isotope ratio of the water the bird drinks. The last important point is that different regions of the world have different characteristic stable isotope ratios in rainwater. So if you can determine the stable isotope ratio of a bird’s feather, you can compare it to the world stable isotope ratio map, and determine where the bird most likely spent the previous year (once birds molt, their new feathers assume the stable isotope ratio of their new location). This approach will underestimate the number of immigrants, because some distant locales have a similar stable isotope ratio as APWRA, and birds from those regions will be incorrectly scored as being local.

Stable isotope map

Map of May-August stable isotope ratios (of 2H in rainwater).  Same colors represent similar stable isotope ratios, ranging from relatively high ratios (deep orange), to relatively low ratios (dark blue). I don’t discuss the meaning of the circles and triangles in this blog post.

Based on this analysis, more than 25% of the dead eagles were immigrants to the area, with some birds originating from more than 800 km away. The researchers point out that APWRA might be particularly attractive to eagles looking for a home because it provides two types of resources that are important to these birds – visually open feeding grounds with easily-located prey, and a consistent updraft to facilitate relatively effortless flight.

Fig 3a

Probability that an eagle killed at APWRA was local.  If the probability was less than 0.5 the researchers scored it as immigrant; if greater than 0.5 the researchers scored it as local.

About half of the immigrants that could be sexed were juveniles or subadults. The researchers argue that the apparent stability of the population in the APWRA region is achieved by young immigrants replacing those birds that are killed by windmills.

Fig3b

Percentage of local vs. immigrant (nonlocal) Golden Eagles by age.

Katzner and his colleagues are concerned that APWRA functions as an ecological sink that attracts eagles, primarily from nearby western states, to replace those killed by windmills. High death rates are particularly problematic to slow-growing populations, such as Golden Eagles, which usually lay only two eggs, with generally only one surviving chick per breeding season (the larger chick often kills its sibling). The researchers also point out that windmills also kill many other animals, including numerous bat species, which also have slow-growing populations. They encourage the renewable-energy industry to develop technology that will reduce windmill-induced death. Such efforts are already underway, and there is preliminary evidence that newer generation turbines are reducing Golden Eagle mortality rates.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Katzner, T.E., Nelson, D.M., Braham, M.A., Doyle, J.M., Fernandez, N.B., Duerr, A.E., Bloom, P.H., Fitzpatrick, M.C., Miller, T.A., Culver, R.C. and Braswell, L., 2017. Golden Eagle fatalities and the continental‐scale consequences of local wind‐energy generation. Conservation Biology31(2): 406-415.Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2017 by the Society for Conservation Biology. 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.

Kimbroreef4

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.

mudcrabhiding

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.

Kimbrofig1

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.

kimbrosetup

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.

Kimbrograph

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.

E-lek-trical death to migrants

Leks have been described as singles bars for birds, though with all the singing and dancing that can go on there, a Karaoke bar might be the closest human analog. Male birds, such as the Great Bustard, Otis tarda, get together at traditional display grounds (leks) and strut their stuff, providing no material resources for females, and being visited by females solely for the purpose of mating.

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Three male Great Bustards on a lek in Central Spain. Credit: Carlos Palacin.

After the mating season concludes, some male great bustards in central Spain fly further north while others remain near the lek area. Migrants benefit from cooler and moister environmental conditions, and, in some cases, greater food availability. But migrants flying to a new area consume calories, and more recently, run the risk of flying into power lines, thereby injuring or killing themselves.

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Newly erected power lines in central Spain. Credit: Carlos Palacin.

 

Carlos Palacín and three other researchers used radio-tracking technology to follow the behavior of 180 male bustards over the course of 16 years. They knew that some bustards died from collision with power lines, but they didn’t know whether these collisions were affecting migrants and non-migrants (sedentary birds) differently, nor if these collisions were changing the migratory behavior of bustards in the 29 breeding groups they studied. So they tracked their birds by ground and by air and determined whether each bird was migrant or sedentary, how long each bird survived, and when possible, the cause of death. For migrant bustards, the researchers measured when and where they migrated, and whether they remained migrants their entire lives.

Palacín and his colleagues discovered that birds migrated away from the lek primarily in May and June, and returned to the breeding grounds over a much more prolonged time period during the autumn and winter.

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About 35% of the birds were sedentary, while 65% migrated an average of 89.9 km, with the longest migration of 261 km. Migrants had much higher mortality rates; for example among 73 birds captured and marked as juveniles, migrants survived an average of 90.6 months (post marking), while sedentary males survived an average of 134.7 months, almost 50% longer! The same pattern follows for 107 birds that were captured and marked as adults. The lesson here is that migration kills.

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So why migrate? Well it appears that before humans (and in particular, before power lines), migration was a much more beneficial strategy. The researchers identified three causes of bustard mortality: collision with power lines in 37.6% of the cases, poaching (9.1%) and collision with fences (2.6%). The bustard forensic team was unable to determine mortality in the remaining cases, so these percentages may underestimate human impact. Importantly, the researchers discovered that death from power lines was more than three times greater in migrants than in sedentary birds.

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This study clearly demonstrates that human infrastructure can shape the migratory behavior of a population. Over the time period of the study, the percentage of sedentary birds has increased sharply even though food availability actually decreased near the breeding grounds as a result of urbanization.

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The decrease in migration may be compounded by a finding that juveniles learn to migrate (or not) from adults during their first three years of life. So if there are more sedentary adults to serve as role models for juvenile behavior, more juveniles will develop into sedentary adults. But sedentary behavior can have several drawbacks. A greater number of sedentary males will increase competition for food and other resources. Also, birds may overheat during particularly hot summers near the breeding grounds. In addition, sedentary birds may have higher inbreeding rates and lower genetic diversity, which in turn can make a local population more susceptible to disease and other environmental changes, ultimately making it more prone to extinction.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Palacín, C., Alonso, J. C., Martín, C. A., & Alonso, J. A. (2017). Changes in bird‐migration patterns associated with human‐induced mortality. Conservation Biology 31: 106-115Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2017 by the Society for Conservation Biology. All rights reserved.