Biological control: birds vs. (insects vs. insects)

We all know that birds eat crop-destroying bugs, so we might think that farmers would welcome insectivorous birds to their fields with radiant rakes or happy hoes. But not so fast! Research by Ingo Grass and his colleagues alerts us to the reality that not all insects are created equal. Some insects eat crops, but some insects eat insects that eat crops.

Aphids are one of the worst scourges of the agricultural world. They suck the phloem sap from many plant species; this action can kill the plant directly, and also cause infections by plant pathogens and viruses. Fortunately for farmers, many animals enjoy eating aphids, including birds such as the Eurasian Tree Sparrow, Passer montanus, and insects such as ladybird beetles and hoverfly larvae.


Hoverfly larva consumes an aphid while a second aphid looks on. Credit: Beatriz Moisset.

Grass and his colleagues knew that sparrows eat both aphids and hoverflies, but they did not know how the effects of bird predation on these insects cascaded down to the oats and wheat crops grown near Gottingen, Germany. Their research tested the hypothesis that sparrows eat so many hoverflies that aphid abundance actually increases (despite also being eaten by sparrows), and oat and wheat abundance decreases (top food web in the diagram below). If so, they reasoned that removing the birds would increase hoverfly abundance, thereby decreasing aphids and increasing grain abundance (bottom food web).


Agricultural food web with (top) and without (bottom) sparrows. Arrows show consumption, with dashed arrows indicating weak effects, and solid arrows and doubled organisms indicating strong effects.

The researchers set up an experiment with 11 nest boxes strategically placed between an oat field and a wheat field. Each box was equipped with a camera, so the researchers could see what the parents fed to their nestlings. In addition, Grass and his colleagues set up eight 4 X 5 meter plastic mesh exclosures which excluded birds, but allowed insects free access. They periodically surveyed 50 plants in each exclosure and in equal-sized control plots for hoverflies and aphids over the course of the sparrow breeding season. Because these birds can have three broods, this project kept them (the sparrows and the researchers) busy from early May to late July.


The birds fed very little on the two grain fields during the first brood, but towards the end of their second brood, they turned their attention to feeding on insects from the two grain fields, and later to eating the ripening grain. One important finding is that bird predation severely reduced hoverfly abundance. By early July hoverfly abundance was about 1 per 50 shoots when birds were present, and more than 3 per 50 shoots when birds were excluded (top graph below).



How did hoverfly consumption translate to aphid abundance? As you can see from the bottom graph, by early July, aphid abundance without birds was considerably lower than aphid abundance in the presence of birds. Taken together, these findings indicate that European Tree Sparrows consume hoverflies, which ultimately leads to an increase in aphid abundance.

Grass and his colleagues conclude that insectivorous birds can interfere with natural pest control of cereal production in central Europe. When birds were experimentally excluded, aphid densities declined 24% in wheat and 26% in oat crops. European Tree Sparrows were doubly bad for the crops, as they also harvested substantial quantities of grain from these fields to feed their third brood. The researchers argue that management of biological control systems for agriculture requires a broad food-web perspective that accounts for trophic cascades, such as the interactions that occur among sparrows, hoverflies, aphids and various types of economically important grain crops.

note: the paper that describes this research is from the journal Ecology. The reference is Grass, Ingo, Katrin Lehmann, Carsten Thies, and Teja Tscharntke. 2017. Insectivorous birds disrupt biological control of cereal aphids. Ecology 98 (6): 1583-1590Thanks 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.


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.

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.

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.