Highly disturbed birds

About 50 million years ago, the fast-moving Indo-Australian plate crashed into the Eurasian plate, giving rise to the Indian peninsula, and beginning a process of faulting and folding that ultimately formed our present day Himalaya Mountains. This process continues today, with the Himalayas still rising about 5 mm per year. The region is very variable, with tremendous glaciers and snowfields at high elevations, and forests and grasslands at lower elevations.


The lead Author, Paul Elsen, stands in front of the Tirthan Valley.  The highest peaks range up to 4900 meters.

The variation in elevation, climate and soils make the Himalyan region in northern India a mecca of biological diversity, hosting over 10,000 identified plant species and about 1000 bird species. As in most of India, human population growth is putting enormous pressure on the forested regions, partly as a source of wood for heating and cooking, which has led to extensive deforestation. In concert, substantial forested areas are being converted to farms or pastures to feed the growing population. Paul Elsen and his colleagues wanted to know how these transformations of forests to cropland and pastures were affecting bird population across the region. They were particularly interested in how birds survived the winter, a period of climatic stress and food scarcity, when many of the birds descend from their high elevation breeding grounds to lower elevations that are nearer to human populations.


Chestnut-headed Tesia, an altitudinal migrant found in high elevation forests in summer, and in forests and agricultural lands in winter. Credit: Prashant Negi.

The researchers set up three transects across four different landscapes (total of 12 transects), representing four levels of disturbance. The undisturbed landscape was primary forest in the Great Himalayan National Park. A second disturbance type – low intensity – retained a mixture of community forest used for timber and fuel, and also included some small agricultural plots. A third disturbance type – medium intensity – had small wooded areas, but was dominated by mixed agriculture including orchards and a variety of crops such as grains, beans and garlic. The final disturbance type – high intensity – was used as pasture, had mostly grasses and very few trees or crops.


Four land-use types. Credit Paul Elsen

The basic research protocol was literally a walk in the woods. Elsen walked (slowly) along the same trail in each transect three times during the winter season, and identified and counted all of the birds. Other researchers identified, measured and counted the plants growing along the transects.


Lead field assistant, Lal Chand (left), and co-author Kalyanaraman Ramnarayan (right) conduct plant surveys near the top of the world.


Elsen was stunned by what his team discovered. Before beginning this study, he had spent about a year in the Himalayas within intact forests doing other PhD-related research. His travels into surrounding villages showed significant bird activity, but he assumed these birds were primarily species associated with humans or more open habitats. He expected decreasing bird diversity and abundance with increasing agricultural intensification, where the bird communities in intact primary forest would be teeming with species in high densities, and the areas with mixed agriculture and intensively grazed pastures would have just a few species. The data below paint a contrasting picture.


Mean and standard error of (a) bird abundance and (b) number of bird species per site across the four land-use types.

Primary forest hosted the fewest number of birds and the fewest species of birds. Among the three disturbance levels, low- and medium-intensity had greater abundance and diversity than did the high-intensity disturbed sites. At least in the winter, low- and medium-intensity disturbed landscapes can be beneficial to bird populations. Elsen suggests that birds are attracted to the tremendous amount of food available in the agricultural lands, such as fruiting trees and shrubs, even in winter. Some birds can consume these fruits, while other birds consume the yummy energy-rich insects that are attracted to the fruit. There are also plenty of seeds available for granivorous birds. But high-intensity disturbed landscapes lack these benefits, leading to fewer forest-adapted bird species, which are replaced by open-country or generalist bird species.


Pastoralist and his goats in a high-intensity disturbed site. Credit: Prashant Nagi.


The researchers caution that we still don’t know have a clear picture of how birds use different landscapes during the breeding season, although preliminary data indicate that more species are unique to primary forests during breeding season than in winter, and that fewer species inhabit intensively grazed pastures during breeding season than in winter. Consequently, Elsen and his colleagues recommend a holistic conservation approach, which recognizes the importance of conserving large portions of intact primary forest, while at the same time preserving landscapes with low- and medium-intensity agriculture.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Elsen, P. R., Kalyanaraman, R., Ramesh, K., & Wilcove, D. S. (2016). The importance of agricultural lands for Himalayan birds in winter. Conservation Biology 31 (2): 416-426. 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.

Cottonwood genes and spider hostels

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


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

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

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

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


Black Cottonwood garden. Credit Matt Barbour

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

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


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

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


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

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

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

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

Fungal fiasco for furry flying friends

Because they are nocturnal, relatively quiet (to our ears), and in general, not very large, most people don’t realize how abundant and diverse bats are. Bats make up about 20% of all mammal species. They are ecologically critical in their roles as insect predators, pollinators and seed dispersers. Unfortunately, bats in the eastern United States and Canada are under siege by the fungus Pseudogymnoascus destructans (Pd), which has killed several million bats in the eastern United States and Canada since its emergence in 2006.


Bats hibernating in Aeolus Cave (Vermont) in 2009, prior to fungal induced die-off. Credit: Joel Flewelling.


The same location one year later. Credit: Joel Flewelling.

Bats are infected when they return to their caves and mines to hibernate. The fungus invades their skin, creating white fungal patches on the muzzle and ears, and disrupting hibernation patterns with consequent high overwintering mortality for several species. The disease is called white-nose syndrome (WNS)


Two little brown bats (Myotis lucifugous) with white-nose syndrome. Credit: Alan C. Hicks.

Winifred Frick has been studying bats for 17 years. She and her colleagues are trying to determine the long-term prognosis for WNS in North American bat populations. They are interested in several related questions. First, how is WNS spreading in North America? Second, are some individuals, or species, tolerant of the fungus, and thus able to sustain infections without dying? Third, is there any evidence for the evolution of resistance, in which some individuals can fight off the infection, and thus carry reduced fungal loads?

Thirty ecologists and even more research assistants throughout the United States and Canada collaborated in this study, collecting tissue from many thousands of bats, and suspected fungal samples from 79 cave walls. This team of researchers used molecular biology techniques (quantitative PCR) to estimate fungal loads. The map and data below summarize some of the findings.


The map on the left shows the spread of WNS over the past 9 years (see key below map). The eight graphs show colony size in red, using the left y-axis, and Pd load in log10 attograms (1 attogram (ag) = 10-18grams), using the right y-axis. Thus, for example, a Pd load value of 5 = 100,000 ag, while a Pd load value of 4 = 10,000 ag.

The first point is that WNS was first detected in New York (black patch with arrow # 1), and quickly spread throughout the Appalachian Mountains in New England, north into Canada, and south into Virginia and West Virginia. More recently WNS has spread further west, and most disturbingly (not pictured) it was also found in the state of Washington in 2016.

On a slightly brighter note, populations of two species, Myotis lucifugus and Perimyotis subflavus, are showing evidence of resistance. For example, two Myotis lucifugus populations (1 and 2 on the map and graph) have reversed their initial sharp declines and are showing significant recovery (red dots). While all sampled individuals still have numerous Pd parasites (open circles on the graphs), the average fungal load has dropped sharply in several populations in recent years (blue dots), indicating the development of resistance.

But there is still a huge reason for concern. For example, consider the northern long-eared bat, Myotis septentrionalis.  WNS spreads very rapidly and fungal loads climb to unsustainable levels among individuals of this species, usually leading to complete extirpation within three years of the first Pd infection at any site. This bat has disappeared from 69% of its caves, and is now endangered in Canada, and is being considered for protection under the United States endangered species act.


Lone Myotis septentrionalis with WNS. Credit: Alan C. Hicks.

The question becomes, what can we do about white-nose syndrome? This disease is particularly pernicious, because samples from cave walls indicate that the fungus can persist outside the host for extended periods of time. So even if populations crash, there is still a reservoir of infection waiting to attack any bats that might move into a cave. Frick suggests that we need to think broadly about conservation efforts that might help the bats, particularly in areas where they are developing tolerance or resistance. She recommends identifying and protecting habitat that contains suitable hibernacula during the winter, and rich foraging sites and appropriate roosts for the rest of the year.

note: the paper that describes this research is from the journal Ecology. The reference is Frick, Winifred F., Tina L. Cheng, Kate E. Langwig, Joseph R. Hoyt, Amanda F. Janicki, Katy L. Parise, Jeffrey T. Foster, and A. Marm Kilpatrick (2017). Pathogen dynamics during invasion and establishment of white‐nose syndrome explain mechanisms of host persistence. Ecology 98(3): 624-631.Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2017 by the Ecological Society of America. All rights reserved.

Timely trophic cascades

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


Oyster reef. Credit: WFSU, Public Media

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


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

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


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

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


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

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


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

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

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

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.


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.


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.


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.


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.


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.


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.