Frogs face fatal fungal foes

Pathogens are organisms that cause disease, and like all organisms, they obey evolutionary principles. Pathogens that survive and reproduce successfully in a particular environment will have more offspring than those that are less successful, thereby passing on those traits that promote successful reproduction to future generations. The problem is that many pathogens change their environment in a way that makes their environment less hospitable for their own survival or reproduction. For example, the fungal pathogen Batrachochytrium dendrobatidis (Bd) causes chytridiomycosis in its amphibian host, which may severely reduce the host population size to the point where few individuals survive. If the host population goes extinct, then there are no hosts for the fungal offspring to infect.

Scheele fungal spore

Scanning electron micrograph of Batrachochytrium denbdrobatidis spore. Credit: Dr. Alex Hyatt, CSIRO Livestock Industries’ Australian Animal Health Laboratory.

Fortunately for Bd, but unfortunately for amphibians, there are several ways out of this conundrum. One approach is a reduction in pathogenicity so that a pathogen’s host species is able to tolerate the infection (and of course, natural selection will at the same time favor an increase in the host species’ tolerance for the pathogen). A second approach is to broadcast a wide net by infecting many different species. That way if one host species goes extinct, there are always many other species to infect. Bd infects over 500 species of amphibians, and has been implicated in the extinction of over 100 amphibian species, and the severe decline of an additional 100 species.

Ben Scheele and his colleagues wanted to know why the endangered northern corroboree frog, Pseudophryne pengilleyi, was declining in southeastern Australia. Several previous studies showed that many corroboree frog populations declined or went extinct in that region over the past 20 years, while the abundant common eastern froglet, Crinia signifera, showed no signs of decline over the same time period. Pilot studies showed that eastern froglets were heavily and commonly infected with Bd. The researchers reasoned that eastern froglets could be acting as a reservoir for Bd, so that corroboree frog populations are being decimated by association with Bd-infected eastern froglets.

Female Ppen copy Hunter

Female Pseudophryne pengilleyi. Credit: David Hunter.

Preliminary surveys indicated that the decline of corroboree frogs was not uniform across the study site; in fact there were some newly discovered populations that were doing very well. The researchers defined three types of sites in their research area. Absent sites (40 in total) had corroboree frogs in 1998, but the population went extinct by 2012. Declined sites (17 in total) had a greater than 80% decrease in abundance since 2000. New sites (25 in total) were newly discovered since 2012, and had much higher population densities than declined sites.


Study area in southeastern Australia, showing locations of Absent, Declined and New sites.

Unfortunately, it is impossible to visually distinguish an infected frog from an uninfected frog, at least until the few hours before death. But the researchers needed to be able to tell if a frog had chytridiomycosis. So they collected skin swabs from the frogs during the breeding season – only working at night to ensure cool humid conditions which minimized frog stress. They then did real time PCR on these samples to quantify the intensity of Bd infection.

Scheele and his colleagues had three important questions they were now prepared to answer. First, how prevalent is Bd in these two species? They found that infection rate was much higher in eastern froglets (79.4%) than in corroboree frogs (27.3%). The intensity of infection (measured by the number of fungal spores) was also much greater in eastern froglets than in corroboree frogs.

Second, do eastern froglets act as a reservoir for Bd, leading to infection and decline of corroboree frog populations? As we discussed earlier, the two species coexist at some sites, but not at others. If eastern froglets act as a reservoir for Bd, we would expect corroboree frogs to have higher infection rates at sites they share with eastern froglets, than they do at sites without eastern froglets. In support of this prediction, Bd prevalence in corroboree frogs was 41.4% at sites with eastern froglets, but only 2.6% at sites with no eastern froglets.

crinia and pengilleyi 3

C. signifera (left) and P. pengilleyi spending quality time together in a P. pengilleyi nest. Credit: David Hunter.

Finally, the researchers want to identify conditions that will promote corroboree frog recovery. They approached this quantitatively by modeling the probability of a site being classified as Absent, Declined or New, in relation to eastern froglet abundance. Based on their survey data of 81 sites, those sites with the highest eastern froglet abundance are most likely to be classified as Absent (corroboree frog extinction), while sites with very few eastern froglets are most likely to be classified as New (thriving corroboree frog populations).


Probability of a site being classified as Absent, Declined or New, based on eastern froglet abundance. Data are log transformed. Dashed lines are 95% confidence intervals.

Scheele and his colleagues conclude that eastern froglets are a reservoir host for Bd, and have played a major role in the decline in corroboree frog populations. The researchers point out that, in general, areas lacking reservoir hosts may provide endangered species with refugia from infectious disease. For managing endangered species, conservation biologists should carefully monitor sites for the presence of reservoir hosts so they don’t reintroduce rare and endangered animals into locations where they will be attacked and killed by pathogens.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Scheele, Ben C., David A. Hunter, Laura A. Brannelly, Lee F. Skerratt, and Don A. Driscoll. “Reservoir‐host amplification of disease impact in an endangered amphibian.” Conservation Biology 31, no. 3 (2017): 592-600. 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.

Light levels limit lake phytoplankton response to fertilization

One might naively think that because we humans are land-dwelling creatures, our impact on aquatic ecosystems might be relatively minor. Unfortunately, this assumption is incorrect, as human activities are changing aquatic environments in profound ways that influence how aquatic species survive and interact. Global warming is increasing lake and river temperatures, uncontrolled development is causing some streams to run dry and others to flood, and agricultural practices are adding nutrients to many lakes and streams. Because these human impacts occur simultaneously, it is difficult to evaluate how each factor contributes to the observed changes in species relations.

In northern Sweden, lakes vary naturally in the amount of dissolved organic carbon (DOC) they contain. DOC comes from runoff of decaying plant matter, so lakes surrounded by substantial vegetation, or that experience a great deal of water input (runoff) from the surrounding area, would have higher DOC than other lakes. DOC is potentially very important to lakes, because DOC tends to discolor a lake, which reduces light penetration and slows down photosynthesis. On the positive side, carbon may bond to other molecules such as phosphorus and nitrogen, which are important nutrients that may be in short supply in these relatively infertile lakes.   Anne Deininger and her colleagues focused their studies on two factors: DOC and nitrogen. Most lakes have too much nitrogen, a result of excessive use of nitrogen fertilizers that run off into lakes, so these relatively low-nitrogen lakes provided the researchers with a unique opportunity to see how these two factors, DOC and nitrogen, interacted in a natural ecosystem.

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Low DOC control lake. Credit: M. Klaus

The researchers selected six lakes that varied naturally in DOC levels: two low (~7 mg DOC/liter), two medium (~11 mg DOC/liter), and two high (~20 mg DOC/liter). In 2011 they measured everything possible about each lake: abundance of all of the life forms, DOC, temperature, light levels, nutrients and photosynthetic rates. In 2012 and 2013, they supplemented one of each pair of lakes with nitrogen compounds every one to two weeks. The added nitrogen was equivalent to the higher nitrogen inputs that are experienced by lakes in southern Sweden. And, as you might expect, the researchers continued measuring all factors of interest in both the experimental (fertilized) and control (unfertilized) lakes throughout the year – at least until the lakes froze over.


Anne Deininger (in orange) and Sonja Prideaux collect samples from a lake. Credit: M. Deininger.

Deininger and her colleagues were most interested in differences in the abundance of phytoplankton – small free-floating photosynthetic organisms, because these are the primary producers – the organisms that produce the chemical energy (via photosynthesis) that enters food webs. There are many different types or groups of these phytoplankton; some are flagellated, with hair-like processes that allow them to navigate in the water column. Some are exclusively autotrophs, producing their own energy from photosynthesis, some are primarily hetrotrophic, eating other organisms or the remains of dead organisms, while others are mixotrophs, using both strategies to produce energy. Cyanobacteria are photosynthetic bacteria, while picophytoplankton are phytoplankton of unusually small size.

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Flagellated phytoplankton (Cryptomonas). Illustration by Anne Deininger.

Many important findings are summarized in the graph below. “B” represents the year before fertilization (2011), while “A1” is 2012 (after fertilization – 1st year) and “A2” is 2013 (after fertilization – 2nd year). Remember only the N-lakes were fertilized; the control lakes were simply monitored all three years. One finding is that in 2011, the high DOC lakes had the lowest phytoplankton abundance.  A second is that the low and medium DOC lakes had both flagellated and non-flagellated phytoplankton, while the high DOC lakes were dominated by flagellated phytoplankton.

Moving to the years after fertilization (A1 and A2), you can see that nitrogen fertilization increased phytoplankton abundance, but more so for the low-DOC lake. However, fertilization had little impact on the types of phytoplankton found in each lake; rather it simply increased the abundance of already existing groups.


Mean biomass of major phytoplankton groups in relation to DOC.  Recall that B refers to 2011 (the year before fertilization), while A1 and A2 refer to the two years after fertilization (2012, 2013).

The data can be organized so we can get a better view of what is happening quantitatively. Fertilization increases phytoplankton biomass, but much more for lakes with low DOC levels. In addition DOC appears to decrease phytoplankton abundance.


Deininger and her colleagues conclude that in these northern lakes, phytoplankton production is nutrient-limited at low DOC levels, but becomes limited by light availability in more murky waters. So adding nitrogen increases phytoplankton abundance to a greater extent in low DOC lakes. High DOC lakes have more flagellated autotrophs, as these species can swim to the top of the water column where there is more light for photosynthesis. As needed, flagellated phytoplankton can move lower in the water column where nutrients are more abundant.

The researchers emphasize that the nitrogen experiments were only conducted for two years. They don’t know if, for example, the types of species would change if fertilization continued for more than two years. They also don’t know if after 2013, the communities reverted to their pre-fertilization state, or if biomasses remained higher when nitrogen fertilization stopped. These types of questions are important to pursue because we humans are making drastic changes to most of our aquatic systems in a very uncontrolled manner. We need to understand the effects of these changes to the aquatic environment, and also how we can reverse the effects should they prove to be highly detrimental.

note: the paper that describes this research is from the journal Ecology. The reference is Deininger, A., Faithfull, C. L., & Bergström, A. K. (2017). Phytoplankton response to whole lake inorganic N fertilization along a gradient in dissolved organic carbon. Ecology98(4), 982-994. 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.

Urban frogs shed no blood

Life is a series of tradeoffs. As one example, we humans have the opportunity (if we are fortunate enough to be given choices) to opt for an urban or rural existence. The urban life is quicker-paced, offers more cultural opportunities, and can be annoyingly noisy and polluted. The rural existence is more laid-back, has fewer cultural opportunities, and may provide a peaceful and relatively unpolluted environment. These different environments can profoundly affect how we feel, with some people being stressed-out by cities and others by farms. On a personal level, I was born in New York City and now live in a very small town in Virginia – I was one of the fortunate ones who was given a choice.


Panama City skyline. Credit: Mariordo (Mario Roberto Duran Ortiz)

Heat, light and noise pollution are common in and near cities, and can influence the distribution and behavior of individuals of many different species. But these factors don’t only operate individually; they can work interactively. In other words, someone might not be annoyed by flashing light nor by loud noise, but might find the combination of the two very disturbing. In addition, these factors might not only operate on individuals; they can also affect relationships, or interactions. For example, loud noises generated by natural gas wells have been shown to influence the abundance of seed predators and seed dispersers, ultimately reducing the number of newly-established pine trees.

Armed with this understanding of interactions and relationships, Taegan McMahon and her colleagues wondered how the combination of heat, light and noise pollution might affect urban túngara frogs (Engystomops pustulosus) in comparison to their more rural counterparts. McMahon had observed that urban frogs were not being swarmed by small Corethrella midges that bite them and suck their blood in more rural and forested areas. These midges carry parasites, and if her observation was correct, urban frogs might have lower exposure to some diseases than do their rural counterparts.


Corethrella midge biting a túngara frog. Credit: Taegan McMahon.

The researchers surveyed 49 túngara frog calling sites in urban (Panama City) and rural (near the small town of Gamboa) areas. At each site they counted the number of frogs, number of midges on or above the frogs, the number of frog egg masses (in foam nests), and measured the air temperature, and the light and sound intensity. As expected, urban calling sites were lighter, noisier and warmer. There were slightly more (statistically insignificant) frogs at the urban sites and considerably more egg masses at rural sites. But the dramatic finding was that there were no midges to be seen on or near any urban frogs. So it might have been hot, bright and noisy, but at least those urban frogs were unbitten!

Factor Urban Rural
Light intensity 0.16 ± 0.02 lx 0.11 ± 0.02 lx
Noise intensity 69.0 ± 0.80 dB 59.2 ± 1.00 dB
Temperature 27.6° ± 0.09°C 25.9° ± 0.04°C
Túngara frog abundance 6.09 ± 2.63 frogs/site 4.05 ± 1.11 frogs/site
Foam nest abundance 0.24 ± 0.23 nests/site 2.06 ± 0.74 nests/site
Frog-biting midge abundance 0.00 ± 0.00 midges/site 67.75 ± 43.27 midges/site

Values are means ± standard error.

Analysis of the field survey data showed that temperature did not influence midge abundance but that light and noise were both important. Interestingly, light and noise interacted with each other in an interesting way. At low sound levels (below 65 db) light was important, in that midge abundance decreased at higher light intensity (Figure A). But at high sound levels, it could be pitch black and you would still have no midges (Figure B).


Log(number of midges) in relation to light levels, in field surveys in which noise levels were (A) below 65 db or (B) above 65 db.

Did light and noise somehow influence a midge’s ability to locate a frog? The researchers set up an experiment to see whether midges were attracted to frog calls at low, medium and high light intensities, and low, medium and high sound intensities. The sounds were recordings of Panama City traffic noise. At the same time, the researchers also broadcast the mating calls of túngara frogs at their normal calling intensity (which is remarkably loud for a small animal). They then counted the number of midges attracted to these traps, which were positioned in a rural setting.


Two calling túngara frogs competing for a female’s attention. Credit: Taegan McMahon.

At low light intensities, many midges were attracted to the recorded frog calls, but city noise (low or high) greatly reduced this attraction. At medium light intensity, fewer midges were attracted to frog calls, and again city noise reduced this attraction. Finally, at high light, even fewer midges were attracted to frog calls, regardless of noise.


Number of midges attracted to recordings of túngara frog calls in relation to light and sound intensity.

McMahon and her colleagues conclude that city noise and light pollution work together to disrupt the frog-biting midges host-parasite interaction. However, the overall impact of urbanization on túngara frogs is unclear at this point. Frogs can lose up to 10% of their blood volume to midges in a night of active calling. Frog-biting midges can transmit blood parasites such as Trypanosoma tungarae to túngara frogs, so urban frogs may be liberated from this scourge. A midge-free existence may allow urban male túngara frogs to call louder and for longer periods of time, which would make them more attractive to females. However, loud and long calling has also been shown to attract the túngara frogs’s mortal enemy, the voracious frog-eating bat. The researchers call for more research on how urbanization can affect species interactions, and for greater consideration of how different forms of pollution can interact to influence ecosystem dynamics.

note: the paper that describes this research is from the journal Ecology. The reference is McMahon, T. A., Rohr, J. R., & Bernal, X. E. (2017). Light and noise pollution interact to disrupt interspecific interactions. Ecology, 98(5), 1290-1299. 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.

Nitrogen nurses

Alfred Lord Tennyson puzzled over the conflict between love as a foundation of Christianity, and the apparent violence of the natural world.

Who trusted God was love indeed

And love Creation’s final law

Tho’ nature, red in tooth and claw

With ravine, shriek’d against his creed

The good poet would be relieved to learn that modern ecologists have uncovered a softer, gentler side of the natural world – facilitative interactions, in which one species (the facilitator) helps out a second species. In many, but not all, cases, the second species also helps out the first species. Ecologists describe these mutually-beneficial interactions as mutualisms. As an example, Mimosa luisana is a mutualist with Rhizobium bacteria, providing the bacteria with root nodules to live in and carbohydrates as an energy source, while receiving ammonia (NH3) that the bacteria fix (convert) from atmospheric N2. A second type of mutualism, a mycorrhizal association, is a very common facilitative interaction between plants and fungi, which grow alongside or within the plant roots. In many mycorrhizal associations, the plant provides carbohydrates to the fungi, which import and share nutrients and water.

Mimosa plant

Mimosa luisana. Credit: Leticia Soriano Flores, algunos derechos reservados (CC BY-NC)

Alicia Montesinos-Navarro and her colleagues, and researchers before them, noticed that in arid and semi-arid environments, plant-plant facilitation was most common between two plant species that were structurally and functionally very distinct, and that tended to be very distantly related to each other. In particular, M. luisana tends to associate with many different species of plants, including many cacti that look nothing like it, and are very distantly related. M. luisana is called a nurse plant, because other species tend to grow under its branches, which shade the soil and reduce water loss from evaporation. Recent work by Montesinos-Navarro and her colleagues showed another benefit of nursing – some plants receive nitrogen from these nurse plants via the network of mycorrhizal fungi.

Traditionally, ecologists have argued that associations between distantly-related plants occur because the plants have very different ecological niches, using different resources in different ways, so they are not competing with each other. Montesinos-Navarro and her colleagues argue that a second process might be important in this and other systems. Close relatives of M. luisana might tend to have high nitrogen levels and thus not benefit from nitrogen transfer from the nurse plant, while more distantly-related plants might tend to have lower nitrogen levels and thus benefit from any nitrogen arriving from M. luisana. They explored this hypothesis in the semi-arid Valley of Zapotitlan in the state of Puebla, Mexico.


Study site dominated by the columnar cactus Neobuxbaimia tetezo, Credit: Alicia Montesinos-Navarro.

Measuring nitrogen transfer from the nurse plant to the recipient is not the world’s easiest task. Fortunately there is a rare form or isotope of nitrogen, 15N, which can be distinguished from the more common 14N. The researchers soaked M. luisana leaves in urea that was made up of primarily 15N, and the leaves took up the urea. Consequently, any exported nitrogen would contain a disproportionately high concentration of 15N, resulting in high 15N levels in the recipient plant. They then measured 15N levels in 14 different species of plants that used M. luisana as their nurse. The researchers were able to test two hypotheses. First, they could see whether close relatives to M. luisana tended to have higher N-levels than more distantly related species. Second they could see whether distant relatives tended to receive more nitrogen from nurse plants than did close relatives.


Mimosa luisana branch taking up 15N-labeled urea. Credit: Alicia Montesinos-Navarro.

The graph below summarizes the results. The y-axis measures how much the 15N level in the facilitated species increased by the end of the experiment (15 days). The x-axis measures the evolutionary relationship between M. luisana and the facilitated species – more precisely how long ago the two species shared a common ancestor. Lastly, the size of the dot measures the initial difference in leaf N-levels between M. luisana and the facilitated plant.

Ecology Fig 2

Influence of evolutionary relationship between M. luisana and the facilitated species (x- axis) and nitrogen gradient – the initial difference in nitrogen levels between the two species (size of dots) on the amount of nitrogen imported by the facilitated species.

Several trends are evident. First, close relatives of M. luisana tended to have similar leaf nitrogen values to M. luisana (medium sized dots), while distant relatives tended to have much less nitrogen than M. luisana (largest dots). Second, the most distant relatives tended to have the greatest increase in their 15N levels, which indicates that they received the greatest nitrogen export from their nurses.

One question is how the nitrogen is transported. Montesinos-Navarro and her colleagues describe how they treated soil with a fungicide, presumably killing the mycorrhizae, which resulted in a substantial reduction in nitrogen transport. This suggests that the mycorrhizal network is important for nitrogen transport. But more pressing is what do the nurse plants get out of the relationship. The researchers suggest that the recipient plants may provide M. luisana with either water or phosphorus, both of which may be in short supply in arid environments.

This study indicates that we need to look beyond traditional niche theory, and may need to  dig deeper to understand the structure of plant communities, and how facilitative interactions can explain the coexistence of very distantly related plants.

note: the paper that describes this research is from the journal Ecology. The reference is MontesinosNavarro, A., Verdú, M., Querejeta, J. I., & ValienteBanuet, A. (2017). Nurse plants transfer more nitrogen to distantly related species. Ecology, 98(5), 1300-1310. 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.

Mustard musters its troops

North American forests are being invaded. The invading forces use chemical warfare to attack the native inhabitants and to repel counterattacks by hostile enemies. As it turns out, the invader is the humble garlic mustard, Alliaria petiolata, which releases toxic chemical compounds into the soil that reduce the growth rate of many native plant species, and has strong chemical defenses that makes it unpalatable to most herbivores.

garlic mustard field

Garlic mustard invasion. Credit Pam Henderson

Lauren Smith-Ramesh wondered why garlic mustard was not even more successful as an invader. Its chemical arsenal should allow it to overrun an area, but she (and many other researchers before her) observed that garlic mustard invasions often decline after a while. As part of her investigations into garlic mustard’s use of chemicals to inhibit native plants, Smith-Ramesh collected seeds from plants from different populations. While shaking these seeds into bags, she noticed that web-building spiders often colonized the garlic mustard’s seed-bearing structure (silique). Were these spiders somehow behind the garlic mustard’s surprising lack-of-success?


Garlic musard silique with web. Credit Lauren Smith-Ramesh

Spiders can benefit plants in several ways. As important predators in food webs, spiders can kill large numbers of herbivorous insects that might otherwise attack a plant. In addition the decaying corpses of their insect prey can add vital nutrients to soils. Garlic mustard does not enjoy these potential spider-associated benefits, because spiders colonize the garlic mustard after it has already gone into decline, and also because garlic mustard is already well-protected (chemically) against herbivorous insects.


About 60% of the spiders were this species – Theriodiosoma gemmosum. Credit Tom Murray.

Smith-Ramesh first wanted to understand the relationship between seed structures (siliques) and spider abundance. She established three different types of plots that measured 2 X 2 meters: (1) S+, which had mustards with intact siliques, (2) S-, which had mustards with siliques removed, and (3) N, which had no garlic mustard plants at all in 2015. After several months, she collected all spiders from the middle square meter of each plot. Plots with garlic mustard with intact siliques (S+) had, by far, the highest spider density. S- plots had a somewhat higher spider density than N plots, which Smith-Ramesh attributes to spiders wandering in from just outside the S- plots (which tended to have more silique-bearing garlic mustard plants nearby than did the N plots). Based on this experiment Smith-Ramesh concluded that garlic mustard siliques were dramatically increasing spider density.

SR2b use

But did increased spider density in S+ plots reduce the number of herbivorous insects, thereby benefiting nearby native plants? Smith-Ramesh set up insect traps that collected insects over two 48 hour time periods – once in August and again in September – in each of the S+, S- and N plots. Both surveys showed fewest herbivorous insects in the S+ plots. This supports Smith-Ramesh’s hypothesis that native plants are benefitting from higher spider density associated with garlic mustard siliques.

SR 2c use

Next, Smith-Ramesh wanted to know whether the decrease in herbivorous insects benefitted native plant growth. To test this directly, she transplanted three types of native plants into her S+, S- and N plots. One of the species, the Hairy Wood Mint Blephilia hirsuta, enjoyed a 50% biomass boost in S+ plots compared to S- plots. The other two native plants species showed very little effect.


Smith-Ramesh collecting data with three siliques in the foreground. Credit: Lauren Smith-Ramesh.

Garlic mustard plants with intact siliques also benefitted the soils by increasing the amount of available phosphorus by approximately 60%. This phosphorus may have originated with insect carcasses that made their way into the soil and released their nutrients. In theory, soils with higher phosphorus availability could help support the growth of native plants. Smith-Ramesh plans to explore other plant communities that are suffering from different invasive plants, to see whether these invaders are also inadvertently providing resources or conditions that may undermine the success of their invasion.

note: the paper that describes this research is from the journal Ecology. The reference is Smith‐Ramesh, L. M. (2017). Invasive plant alters community and ecosystem dynamics by promoting native predators. Ecology98(3), 751-761. 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.

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.