Too much of a good thing is killing Monarch butterflies

There was a time in the mid-Pleisticine when a photo of an ecological event was an awesome novelty, and a movie of an ecological event even more so.  Dodderers of an ecological bent (myself included), can vividly recall viewing a series of photos or a movie, either in a seminar or in an ancient ecology text, of a blue jay consuming a monarch butterfly, Danaus plexippus.  Consumption is immediately followed by explosive vomiting, as the cardenolides within the monarch butterfly claim another victim.  The monarch sequesters these cardenolide toxins from its larval food (milkweed), and incorporates them into its tissues as a means of protecting itself from predators – presumably blue jays learn from this very aversive experience.  I should point out that the individual sacrificial butterfly enjoys no fitness from this learning event – which raises some evolutionary questions we will not explore at the present.

Karen Oberhauser

Five instars (stages of development) of monarch caterpillars on a milkweed leaf. Credit: Karen Oberhauser

Rather we turn our attention to the relationship between milkweed, monarchs, and climate change. In several places in this blog we’ve talked about how climate change has influenced the behavior or physiology of a single species. For example, my first blog (Jan 31, 2017) discusses how increasing temperatures create more females in a loggerhead turtle population. But there are fewer studies that explore how climate change influences the ecological landscape, ultimately affecting interactions between species.  Along these lines, Matt Faldyn wondered if increased air temperature would change the chemical constitution of milkweed in a way that might influence monarch populations.  As he describes, “With milkweed toxicity, there is a ‘goldilocks’ zone where monarchs prefer to feed on milkweed that produce enough toxins in order to sequester these (cardenolide) chemicals as an antipredator/antiparasite defense, while also avoiding reaching a tipping point of toxicity where feeding on very toxic milkweeds negatively impacts monarch fitness.” He expected that at higher temperatures, milkweed would become stressed, and be physiologically unable to sustain normal levels of cardenolide production.

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Monarch butterfly feeds on a native milkweed, Asclepias incarnata. Credit: Teune at the English Language Wikipedia.

For their research, Faldyn and his colleagues worked with two milkweed species.  Asclepias incarnata is a common, native milkweed found throughout the monarch butterfly’s range in the eastern and southeastern United States.  Asclepias curassavica is an exotic species that has become established in the southern United States.  In contrast to A. incarnata, A. curassavica does not die back over the winter months; consequently some monarch populations are no longer migratory, relying on A. curassavicato provide them with a year round food supply.

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The exotic milkweed, Asclepias curassavica. Credit: 2016 Jee & Rani Nature Photography (License: CC BY-SA 4.0)

To protect against herbivory, milkweeds have two primary chemical deterrants: (1) the already-mentioned cardenolides, which are toxic steroids that disrupt cell membrane function, and (2) release of sticky latex, which can gum up caterpillar mouthparts and actually trap young caterpillars.

field_noborderii.jpgThe researchers wanted to simulate climate change under field conditions, so they created open-top chambers with plexiglass plates that functioned much like mini-greenhouses, into which they placed one milkweed plant that was covered with butterfly netting.  This setup raised ambient temperatures by about 3°C during the day and 0.2°C at nighttime.  Control plots were single milkweed plants with butterfly netting. Half of the plants were native milkweed, and the other half were the exotic species.

For their experiments, Faldyn and his colleagues introduced 80 monarch caterpillars (one per plant) and allowed them to feed normally until they pupated.  Pupae were brought into the lab and allowed to metamorphose into adults.

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Matt Faldyn holds two monarch butterflies in the laboratory. Credit Matt Faldyn.

At normal (ambient) temperatures, monarchs survived somewhat better on exotic milkweed.  But at warmer temperatures, there is a strikingly different picture. Monarch survival is unaffected by warmer temperatures on native milkweed, but is sharply reduced by warmer temperatures on exotic milkweed (top graph below). The few that managed to survive warm temperatures on exotic milkweed grew much smaller, based on their body mass and forewing length (middle and bottom graph below)

FaldynFig1

Survival (top), adult mass (middle) and forewing length (bottom) of monarch butterflies raised under normal (ambient) and warmed temperatures.  Error bars are 95% confidence intervals.

Both milkweed species increased production of both types of chemicals over the course of the experiment. But by the end of the experiment, the exotic species released 3-times the quantity of latex and 13-times the quantity of cardenolides than did the native milkweed species.

FaldynFig2

Average amount of latex released at the beginning and end of the experiment.  Error bars are 95% confidence intervals.

FaldynFig2

Average cardenolide concentration at the beginning and end of the experiment.

The researchers argue that the exotic milkweed, Asclepias curassavica, may become an ecological trap for monarch butterflies, in that it attracts monarchs to feed on it, but will, under future warmer conditions, result in dramatically reduced monarch survival. Interestingly, these results are not what Faldyn originally expected; recall that he anticipated that temperature-stressed plants would reduce cardenolide production. The tremendous increase in cardenolide production in exotic milkweed at warmer temperatures may simply be too much toxin for the monarchs to process. The researchers predict that as climate warms, milkweed ranges will expand further north into Canada, and lead to northward shifts of monarch populations as well.  They urge nurseries to emphasize the distribution of native rather than exotic milkweed, so that monarchs will be less likely to become victims of this ecological trap.

note: the paper that describes this research is from the journal Ecology. The reference is Faldyn, M. J., Hunter, M. D. and Elderd, B. D. (2018), Climate change and an invasive, tropical milkweed: an ecological trap for monarch butterflies. Ecology. doi:10.1002/ecy.2198. 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.

Saguaro survival: establishing an icon

Having grown up in the New York metropolitan area, my only contact with the saguaro cactus, Carnegiea gigantea, was from several TV westerns, which dubiously placed these mammoth cacti in New Mexico, Texas and Colorado.  In fact, the saguaro is limited to the Sonoran Desert of northwestern Mexico, extreme southeast California and southern and central Arizona. You won’t find these cacti further north, because a freeze lasting more than 24 hours kills them.  I still remember my first real sighting of these cacti; I was amazed at how distinct they seemed in comparison to the other vegetation, and I delighted in their abundance.

Daniel Winkler - Saguaro Photo 1

Dense patch of saguaros. Credit: Daniel Winkler

Many others delight in their abundance as well.  The flowers, fruits and seeds feed many animals (including humans).  They were an important food for the Tohono O’odham and Pima Indians – eaten fresh or converted into numerous products including wine, juice, jam and syrup.

Daniel Winkler - Saguaro Photo 2

Large saguaro with many fruits emanating from the apex of its branches. Credit: Daniel Winkler

Woodpeckers and flickers excavate nests in the saguaro’s trunk, which are subsequently occupied by other animals such as snakes, arthropods and small mammals.

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Saguaro with nest cavity excavated near the top of its trunk. Credit: Daniel Winkler

Daniel Winkler also delighted in the saguaro’s awesomeness. As he describes “I fell in love with answering some basic ecology questions about the saguaro. I was surprised that scientists had been studying this wonderful plant for almost 100 years and there were still many basic questions about the species general biology and ecology that remained unanswered. Thus, I was hooked immediately and became obsessed with saguaro.”

Don Swann - Photo of D. Winkler with young saguaros

Daniel Winkler with young saguaros. Credit: Don Swann

Winkler and his colleagues wanted to know how moisture, temperature and habitat influence the establishment or survival of juvenile saguaro seedlings. Previous research had shown that saguaro height can be used to estimate saguaro age, given knowledge of previous rainfall in a particular area. So buoyed by an army of citizen scientists whom they recruited with the help of social media, student groups from schools and volunteers working at the Saguaro National Park, the research team estimated the age of every saguaro on 36 4-ha plots (1 ha = 10,000 m2).

Going into the study, the researchers knew that rainfall was a very important factor, with saguaros surviving better during wet periods.  But they also knew that historically, some areas located near each other showed different establishment trends, thus they suspected that other variables, particularly land use and other landscape factors, might be important.  They did their research in two different districts within the park: 21 plots in the Rincon Mountain District (RMD) on the east side of the park, and 15 plots in the Tucson Mountain District (TMD) to the west. They classified each plot as a particular habitat type based on slope, elevation and soil-type. Bajada was low elevation, flat and had gravelly porous soils.  Foothills were intermediate elevation and intermediate slope, while sloped habitats had highest elevation, steepest slope, and the coarsest rockiest soils.

Daniel Winkler - Saguaro Photo 4

Panoramic view of Saguaro National Park showing diversity of habitats. Credit: Daniel Winkler.

Winkler and his colleagues calculated the Palmer Drought Severity Index (PDSI) for the years 1950-2003. The PDSI quantifies the water balance between precipitation and evapotranspiration, taking into account not only rainfall but also other factors such as temperature and cloud cover.  The PDSI was estimated by assessing tree ring width for each year in nearby woodlands; wet conditions have wide tree rings (maximum PDSI value = +6), while dry years have narrow tree rings (minimum PDSI value = -6).

The researchers discovered a very strong association between the PDSI and seedling establishment. Low PDSI at the beginning and especially the end of the time frame was associated with low seedling establishment, while high PDSI (particularly in the 1980s was associated with high rates of seedling establishment (top graph below).  But other patterns emerged as well.  For example, establishment was higher in the TMD during the wettest years, but higher in the RMD during the most recent drought (bottom graph below).

WinklerFig1

Top. Total number of saguaros (left Y-axis) established per hectare from 1950-2003 in relation to PDSI (dashed line, right Y-axis). Bottom. Total number of saguaros established per hectare in the Tucson Mountain District (TMD – filled bars) and the Rincon Mountain District (RMD – open bars)  from 1950-2003 in relation to PDSI (dashed line, right Y-axis).

Saguaro establishment increased in all habitats when conditions were relatively wet (more positive PDSI values).  Under drought conditions, slopes had greatest saguaro establishment, while establishment increased more rapidly in foothills (and to a lesser extent in Bajadas) as moisture levels increased.

WinklerFig2

Model projecting number of saguaros established in the three major habitats in relation to PDSI.  Shaded regions are 95% confidence intervals.

The researchers were surprised at how tight the connection was between drought and saguaro establishment. But landscape features are also important.  The TMD is warmer and dryer than the nearby RMD, and had substantially lower establishment during the recent drought. The slopes in the RMD are steeper and rockier than sloped areas of the TMD, and may buffer saguaros from drought by capturing water in rock crevices and holding it for longer periods of time so it can be absorbed by saguaro roots. Nurse trees that provide shade to young saguaros may also be more common on the RMD slopes.

Winkler and his colleagues are concerned about the long-term impacts of climate change on saguaro populations, particularly in the drier areas of the TMD. They urge researchers to explore how long-term management of grazing and invasive species influences saguaro establishment across the landscape.  They also encourage researchers to gather some very basic data about saguaros, such as how they access water and how human water use patterns influence the water’s availability to this iconic species.

note: the paper that describes this research is from the journal Ecology. The reference is Winkler, D. E., Conver, J. L., Huxman, T. E. and Swann, D. E. (2018), The interaction of drought and habitat explain space–time patterns of establishment in saguaro (Carnegiea gigantea). Ecology 99: 621-631. doi:10.1002/ecy.2124. 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.

Predators and livestock – “stayin’ alive.”

President Donald Trump was elected on a platform that included building a great wall whose purpose was to keep out unwanted intruders from the south, and that would be paid for (apparently magically) by these same intruders.  The idea of building a great wall has been around for a long time; the Great Wall of China was constructed over a time period of almost two thousand years to keep out unwanted intruders (this time from the north). Not surprisingly, the cost of that Great Wall was not borne by the unwanted intruders. More recently, in the 1880s, the government of Australia constructed a 5500 km fence designed to keep unwanted dingoes away from sheep that pasture in southeastern Australia. As Lily van Eeden describes, the Australian government spends about $10 million dollars per year to maintain the fence but there are almost no data to compare livestock losses on either side of the fence. Thus she and her colleagues decided to look at what was being done globally to evaluate the effectiveness of different methods of protecting livestock.

DingoFencePeter Woodard

The Dingo fence across southeastern Australia. Credit Peter Woodard.

The researchers grouped livestock protection approaches into five different categories: lethal control, livestock guardian animals such as dogs, llamas and alpacas, fencing, shepherding and deterrents. Lethal control includes using poison baits and systematic culling of populations of top predators. Deterrents include aversive conditioning of problem predators, chemical, auditory or visual repellents, and protection devices such as livestock protection collars.

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A guardian dog emerges from the midst of its flock in Bulgaria. Credit: Sider Sedefchev.

Van Eeden and her colleagues then did a meta-analysis to see which approach worked best. You can check out my blog from Aug. 2, 2017 (“Meta-analysis measures multiple mycorrhizal benefits to plants”) for a more detailed discussion of meta-analyses. Very briefly a meta-analysis is a systematic analysis of data collected by many other researchers. This is challenging because each study uses slightly different techniques and has different levels of rigor. For this meta-analysis, van Eeden and her colleagues used only two types of studies. One type is a before/after design, in which researchers kept data on livestock loss before the mitigation treatment as well as after. The second type is a control-impact design, in which there was a control group set aside, which did not receive the mitigation treatment. Each study also needed sample sizes (number of herds and/or number of years), means and standard deviations, and had to be run for at least two months to be used in the meta-analysis.

The researchers searched several databases (Web of Science, SCOPUS and European Commission LIFE project), Google Scholar, and also used more informal sources, to collect a total of more than 3300 records. However, after imposing the requirements for types of experimental design and data output, only 40 studies remained for the meta-analysis. Based on these data, all five mitigation approaches reduced predation on livestock. The effect size in the figure below compares livestock loss with the treatment to livestock loss without the treatment, so that a negative value indicates that the treatment is associated with reduced livestock loss. The researchers conclude that all five approaches are somewhat effective, but the large confidence intervals (the whiskers in the graph) make it difficult to unequivocally recommend one approach over another. The effectiveness of lethal control was particularly variable (hence the huge confidence interval), as three studies showed an increase in livestock loss associated with lethal control.

van EedenFig2

Mean effect size (Hedges’ d) and confidence intervals for five methods used to mitigate conflict between predators and livestock.  More negative effect size indicates a more effective treatment. Numbers in parentheses are number of studies used for calculating mean effect size.

Finding that non-lethal management is as effective (or possibly more effective) than lethal control tells us that we should probably be very careful about intentionally killing large carnivores, since, in addition to being cool animals that deserve a right to exist, they also perform some important ecosystem services. For example, in Australia, there are probably more dingoes northwest of the fence than there are south of the fence, so exclusion may  be working. However there is some evidence that there are also more kangaroos and rabbits south of the fence, which could be an unintended consequence of fewer predatory dingoes. Kangaroos and rabbits eat lots of grass, so keeping dingoes away could ultimately be harming the sheep populations. Dingoes may also kill or compete with invasive foxes and feral cats, which have both been shown to drive native species to extinction, so excluding dingoes may increase foxes and cats, threatening native species.  Van Eeden and her colleagues argue that different mitigation approaches work in different contexts, but that we desperately need evidence in the form of standardized evaluative studies to understand which approach is most suitable in a particular context.

van Eeden Fig.3

Context-specific approach to managing the co-exstence of predators and livestock.

In all contexts, cultural and economic factors interact in mitigating conflict between humans and carnivores. The dingo is officially labeled as a wild dog, which invaded Australia relatively recently (about 4000 years ago), so the public perception is that this species has a limited historical role. Other cultures may have a different view of their predators. For example, the Lion Guardian project in Kenya, which trains and supports community members to protect lions, has successfully built tolerance for lions by incorporating Maasai community cultural values and belief systems.

To use a phrase that President Trump recently forbade the Centers for Disease Control to use in their reports, our decisions about predator mitigation should be “evidence-based.” We need more controlled studies that address the success of different mitigation approaches in particular contexts. We also must understand the costs of removing predators from an ecosystem, as predator removal can initiate a cascade of unintended consequences.

note: the paper that describes this research is from the journal Conservation Biology. The reference is van Eeden, L. M., Crowther, M. S., Dickman, C. R., Macdonald, D. W., Ripple, W. J., Ritchie, E. G. and Newsome, T. M. (2018), Managing conflict between large carnivores and livestock. Conservation Biology, 32: 26–34. doi:10.1111/cobi.12959. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. 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.

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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.

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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.

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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.

Blinded by the light: victims of the night

In late October, the municipality of Buenavista del Norte on the Canary Island of Tenerife, celebrates the day of the Virgin of Los Remedios, including, among other features, a big light display. As a child, Airam Rodríguez noticed that many shearwaters would also drop in (literally) for the festivities, attracted by the bright lights, but unable, in many cases, to get back in the air. Many of these shearwaters died from a variety of causes, including the impact of flying into the ground, dehydration, predation and poaching. As an adult, Rodríguez collaborated with researchers around the world to evaluate the scope of light-induced shorebird fallout.

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Fallout victim: grounded Short-tailed Shearwater. Credit: Airam Rodríguez

The researchers began their work by searching a science citation index – the Web of Science – for articles on light-induced seabird mortality. They used references from these articles to find additional articles. In addition, they used the internet and social media to find programs in which citizens are encouraged to report grounded birds, and contacted people associated with these programs to get qualitative and quantitative data.

Rodríguez and his colleagues discovered light induced seabird fatality on 47 islands, three continental locations and across all of the world’s oceans. Of 115 species of burrow-nesting petrels, 56 have been reported as grounded by light. Several other groups of birds, including puffins, auklet and eiders also suffer from light-induced fallout, and it is very likely that more species are unreported.

RodriguezFig1

Numbers of reported grounded seabird fledglings across the globe.  Circle size = numbers of birds  reported. Numbers = number of species affected. Circle color = IUCN (endangerment) category for each species as follows: CR = critically endangered, EN = endangered, VU = vulnerable, NT = near threatened, LC = least concern.

Of deep concern is that 24 species are globally threatened. In addition, fallout has been reported at sea, induced by lights used for fisheries and by lights on oil platforms. All of the studies of light-induced fatalities on land documented the highest mortality in fledglings that are grounded during their first flights from their nests toward the ocean.

RodriguezFig2

Numbers of species of threatened seabirds that were rescued across the globe.  Numbers were not available for species with ? symbol.

Researchers don’t know why birds are attracted to lights. Perhaps birds view lights as a source of food; for example some species eat bioluminescent prey. Alternatively, as cavity-nesting birds, the only light these chicks see is from their burrow entrance, particularly when their parents bring in food, so the fledglings might confuse light with a food source. Lastly, artificial lights might override any celestial light cues the birds normally use for navigation, confusing them and causing them to crash to the ground. Supporting this hypothesis, seabirds generally don’t crash into lights, which might be expected if they mistook a light for bioluminescent prey.

Cory's shearwater fledgling at their nest at Tenerife Canary Islands. Photo by Beneharo Rodríguez

Fledgling Cory’s Shearwater first sees the light of day after emerging from its burrow at Arona on southern Tenerife Island. Credit: Beneharo Rodríguez

So what can be done about this problem? Accurate data are hard to come by, as many estimates of fallout-induced mortality come from relatively untrained volunteers, who are less likely to report dead birds. As one example, on Kauai, surveys from a general public rescue program for Newell’s Shearwaters identified 7.7% mortality, whereas later systematic surveys by trained researchers indicated 43% mortality. In some rescue operations, birds are banded and released, which, in theory, allows researchers to estimate the survival rate of rescue birds, but, in practice, these data are usually insufficient for accurate estimates

Rodríguez and his colleagues recommend a multipronged approach to combat seabird fallout. Individuals grounded by artificial lights can be rescued so they don’t succumb to the common causes of death – dehydration, predation and vehicle collision. In many cases the general public takes birds to designated rescue stations, where they are cared for until judged to be ready to release. The first rescue program was set up on Kauai in 1978; since then, people working for 16 rescue programs have released over 40,000 birds.

Release of a grounded shearwater. Photo Nazaret Carrasco (1)

Beneharo Rodríguez releases a Cory’s Shearwater from a cliff at Buenavista del Norte on Tenerife Island. Credit: Nazaret Carrasco.

The birds would be best served if humans behaved in ways that minimized fallout. Researchers need to learn more about why birds are attracted to artificial lights so engineers can develop outside lights that don’t attract them. Existing lights can be turned off when not needed, and dimmed when they are essential. Special accommodation can be made for unusual cases; for example in Cilaos, Reunion, Indian Ocean, streetlights are turned off during the fledging period of Barau’s Petrel. Lights can also be shielded so they illuminate an area for humans, but minimize the light visible to birds. Degraded nesting and breeding habitat can be restored to help compensate for birds that are lost to fallout. Lastly, conservation efforts should benefit the local economies so that residents will be more likely to support conservation initiatives, such as reduced evening lighting, that they might otherwise oppose.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Rodríguez, A., Holmes, N. D., Ryan, P. G., Wilson, K.-J., Faulquier, L., Murillo, Y., Raine, A. F., Penniman, J. F., Neves, V., Rodríguez, B., Negro, J. J., Chiaradia, A., Dann, P., Anderson, T., Metzger, B., Shirai, M., Deppe, L., Wheeler, J., Hodum, P., Gouveia, C., Carmo, V., Carreira, G. P., Delgado-Alburqueque, L., Guerra-Correa, C., Couzi, F.-X., Travers, M. and Corre, M. L. (2017), Seabird mortality induced by land-based artificial lights. Conservation Biology, 31: 986–1001. 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.

River restoration responses

The Lippe River in Germany has been subjected to many decades of channelization, deepening, floodplain drainage, straightening and consequent shortening, with one result being that the modern Lippe is 20% shorter than it was two centuries ago. Beginning in 1996, conservation managers began reversing this trend by widening the river, raising the level of the river bed, constructing small islands within the river and terminating floodplain drainage operations over a stretch of 3.3 km. As a result of these activities, a small portion of the river looks much like it did 200 years ago.

rivrestfig1

A section of the Lippe River before (left) and after (right) restoration.

Over a 21-year period, researchers from Arbeitsgemeinschaft Biologischer Umweltschutz have conducted systematic surveys of fish communities at the restored and unrestored sections of the river. Researchers sampled the fish community with electrofishing – inputting a direct electrical current into the river – which causes the fish to swim towards the boat where they are easily collected with nets, identified by species, and returned unharmed into the river. A data set over this length of time in association with a restoration project is very unusual; oftentimes (in part due to funding issues) only one survey is conducted to assess the fish community response to river restoration.

About eight years ago, while a postdoctoral researcher at Senckenberg Research Institute in Frankfurt, Germany, Stephan Stoll was asked to analyze some river restoration outcomes, and, as he describes, “became hooked to the topic.” To evaluate the response of the Lippe River fish community to restoration, a group of researchers headed by Stephanie Höckendorff, a Master’s student with Stoll, first asked a very simple question – how did fish abundance and species richness (the number of fish species) compare in the restored and unrestored regions of the river.

The graph below shows several striking trends. Abundance peaked about 2-3 years after restoration, declined sharply the next year, and recovered in subsequent years to about three times the abundance found in unrestored sections. Importantly, abundance varied extensively year-to-year. For example, if you had done only one survey in 2000, you would have erroneously concluded that restoration had no effect, which is why the researchers emphasize the importance of collecting data over a long stretch of time.

rivrest2a

Abundance of fish in restored (Rest-gray curve) and unrestored (Cont-black curve) sections of the Lippe River.  The gray vertical bar indicates the start of the restoration project in 1997.

Species richness increased sharply, but did not reach its peak until nine years after restoration. Again, there was extensive year-to-year variation in species richness.

rivrest2b

Fish species richness in restored (Rest-gray curve) and unrestored (Cont-black curve) sections of the Lippe River.  The gray vertical bar indicates the start of the restoration project in 1997.

Höckendorff and her colleagues were intrigued by this delay in species richness, and turned their attention to understanding what types of species benefited most from the restoration. Their analyses indicated that colonizing species, such as common minnows and three-spined sticklebacks, tended to have short life spans, early female maturity, several spawning events per year and a fusiform body shape – a body that is roughly cylindrical and tapers at both ends. Interestingly, some of the most successful colonizers took quite a long time to get well-established within the community.

Minnow

Common minnows, Phoxinus phoxinus. Credit: Carlo Morelli (Etrusko25)

Stickleback

The three-spined stickleback, Gasterosteus aculeatus. Credit: Ron Offermans

The restored habitat was highly dynamic, experiencing periodic flooding and the formation of temporary shallow bays and shifting sandbanks. These types of habitats tend to select for minnows, sticklebacks and other opportunistic species that are attracted to periodic disturbances. These opportunistic species were quick to move in, and continued to increase in abundance over time. Importantly, several rare and endangered species also colonized the restored habitat. However, large, deep-bodied, slow maturing and long-lived species did not benefit (at least over the 17 years of the survey), as these types of species are generally favored in less dynamic habitats, which are more stable and uniform.

Overall, these findings demonstrate the benefits of river restoration to the fish communities they harbor. But some species are more likely to benefit than others, and the time-scale over which recolonization occurs is highly variable. Surveys must be repeated over a long time-scale to tell conservation managers whether their restoration efforts are successful, and how they might change their future river restoration efforts.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Höckendorff, S., Tonkin, J. D., Haase, P., Bunzel-Drüke, M., Zimball, O., Scharf, M. and Stoll, S. (2017), Characterizing fish responses to a river restoration over 21 years based on species’ traits. Conservation Biology, 31: 1098–1108. doi:10.1111/cobi.12908. 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.

Sushi in Disguise

As an ecology researcher, I’ve always been attracted to systems where you might be able or inclined to eat your organism after you completed your experiment or observations. Alas, I spent my research career studying spiders, dragonflies and zebrafish, all of which are high on nutrients but low on succulence. Thus I read with considerable gastronomic anticipation an article by Demian Willette and his colleagues that studied nine different species of fish served up at local sushi restaurants in Los Angeles, California.

Sushi

Mackerel, salmon and tuna (front to back) served at a Los Angeles sushi restaurant. Credit Demian Willette.

One of the co-authors, Sara Simmonds, had a great idea when she was a teaching assistant for the Introduction to Marine Science course at UCLA in 2012. Simmonds suggested that students in the class could investigate whether seafood served at sushi restaurants were always what they claimed to be, or might they sometimes travel under false identities. For example, is red snapper (which does not occur in California waters) really red snapper, or might merchants substitute one of 13 rockfish species in its stead? This project allowed students to investigate a real world marine-related topic, while also getting some experience using and applying molecular genetics tools.

Over the course of the four-year study, students ordered sushi from 26 different restaurants, confirmed the species identification with the wait-staff, and collected tissue samples from each order. They then subjected the samples to DNA barcoding, which amplifies and sequences an approximately 650 base pair segment of the mitochondrial COI gene. Once they determined the DNA sequence, students then compared it with known sequences using the Basic Local Assignment Search Tool database (National Center for Biotechnology Information).

Each year, between 40 and 52% of the fish were mislabeled. Though previous studies by other researchers had identified mislabeling, Willette and his colleagues were surprised that all 26 restaurants had at least one case of mislabeling, and that the mislabeling rate was so consistent from one year to the next.

SushiFig1

Percentage of sushi mislabelled (left y-axis – bar symbol) and number of restaurants sampled (right y-axis – diamond symbol) by year.  Number in bar is sample size for that year.

Overall substitution rates varied dramatically from one species to another. All fish species, except bluefin tuna, were mislabeled at least once, and two species – red snapper and halibut – were always mislabeled. Red snapper was often replaced with red seabream, while halibut was usually replaced with flounder.

SushiFig2

Percentage mislabeled (+ standard error) for each species in the study. Numbers above bars are number mislabeled (left) and total sample (right).  For example 6 out of 47 salmon were mislabeled.

Why should we care if we’re served the wrong species of fish, as long as it tastes good? As it turns out, there are several reasons. About 33% of halibut are substituted with olive flounder, which can harbor the parasite Kudoa septempunctata, which is known to cause severe food poisoning. In addition, some of the other halibut substitutes are actually overfished flounder species, so substituting these for halibut is depleting already at-risk fisheries. Similar problems, in which an at-risk species substitutes for the mislabeled species, were common in tuna and yellowtail as well.

The researchers recommend that seafood mislabeling must be attacked at all stages of the seafood supply chain. All seafood should be labeled to species, place of origin, and the type of fishing practice used. Inspectors must be trained to identify seafood – perhaps using portable, hand-held DNA sequencers. Retailers should be told when they sell mislabeled species, so they can insist that their suppliers deliver the correct goods. Finally social media can be used to inform the public of consistent mislabeling, so consumers can pressure retailers to make sure that a red snapper is what it claims to be.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Willette, D. A., Simmonds, S. E., Cheng, S. H., Esteves, S., Kane, T. L., Nuetzel, H., Pilaud, N., Rachmawati, R. and Barber, P. H. (2017), Using DNA barcoding to track seafood mislabeling in Los Angeles restaurants. Conservation Biology, 31: 1076–1085. doi:10.1111/cobi.12888. 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.

Seagrass scourge: when nutrient enrichment reaches the tipping point

Sean Connell has watched as south Australia has lost vast expanses of kelp forest and seagrasses over the past years. One of the primary culprits associated with loss of seagrass meadows is excessive nutrients, particularly nitrogen, which enters the ecosystem with runoff, and causes an increase in algal epiphytes (epiphytes are small plants that grow on other plants). Epiphytes can negatively affect seagrass by blocking sunlight needed for photosynthesis, and indirectly, by increasing the rate of cellular respiration within the ecosystem, thus using up oxygen needed by seagrass for metabolic processes.

DolphinConnell

Two dolphins swim above a bed of seagrass off the south Australian coast.

Connell and his colleagues noticed that seagrass loss was often sudden; a large seagrass meadow would appear to be in good shape, and then it would abruptly disappear. They suggested that there might be a threshold effect in nutrient levels that seagrasses can tolerate; that these systems function well until a certain threshold in nutrient levels is crossed, above which there is an abrupt loss of seagrasses. They tested this hypothesis by subjecting plots of the seagrass Amphibolis antarctica to seven different concentrations of dissolved inorganic nitrogen (DIN) over a 10 month period, and monitored the abundance of epiphytes and seagrass over that timespan.

The meadows were about two km offshore from Lady Bay, Fleurieu Penninsula, Australia, in about 5 meters of water. Different amounts of nitrogen fertilizer were wrapped in nylon bags (for slow continuous release of DIN) and staked to the ocean floor. Amphibolis antarctica grows by producing new leaves at the top of each leaf cluster, but at the same time it drops old leaves. Leaf turnover, the researchers’ measure of growth, is simply new leaf production minus old leaf drop. The researchers tied on a small nylon cable at known locations on selected plants, noted how many leaves were above and below each tie at the beginning of the experiment, and recounted leaf number 10 months later. Finally, the researchers measured epiphyte growth by microscopically viewing a sample of seagrass leaves, and counting the number seagrass leaf cells that were covered by epiphytes.

Seagrass growth was relatively unaffected by all tested DIN levels.

ConnellFigA

Leaf production per day in relation to concentration of DIN.

However, leaf drop showed a strong threshold effect; leaf drop rates increased sharply between 0.13 – 0.15 mg/L of DIN.

ConnellFigB

Leaf drop per day in relation to concentration of DIN.

Putting these two graphs together, you can see (below) that leaf turnover switched from positive to negative at 0.13 – 0.15 mg/L of DIN. Negative leaf turnover translates to a sudden loss of seagrass at that threshold. At least in this system, at this location, 0.13 – 0.15 mg/L of DIN is the tipping point, beyond which the seagrass system suddenly goes into decline.

ConnellFig1

Leaf turnover per day (left y-axis and red data), and Epiphyte cover (% – right y-axis and green data), in relation to concentration of dissolved inorganic nitrogen.

The graph also shows that the tipping point coincides with an epiphyte cover of approximately 60%. It is possible that increased epiphyte cover may reduce seagrass photosynthetic rates (particularly in lower leaves), so that leaf turnover suddenly shifts into the negative zone, but the study was not designed to identify the underlying mechanism.

Seagrass meadows perform important ecosystem services, such as absorbing excess nutrients from the sediment, and providing habitat and food for a diverse group of grazers and indirectly, for their consumers. Thus seagrass conservation is vital. The danger here is that moderate levels of nutrients do not appear to have much effect on seagrass populations, but there is an abrupt shift to seagrass loss once the nutrient threshold is crossed. This makes the system very difficult to manage, because the loss occurs without warning. Australian ecologists have repeatedly failed to restore lost seagrass meadows, as simply reducing nutrient levels does not reverse the process. Thus anticipating seagrass loss before it happens is the most viable management solution for this critical ecosystem.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Connell, S. D., Fernandes, M., Burnell, O. W., Doubleday, Z. A., Griffin, K. J., Irving, A. D., Leung, J. Y.S., Owen, S., Russell, B. D. and Falkenberg, L. J. (2017), Testing for thresholds of ecosystem collapse in seagrass meadows. Conservation Biology, 31: 1196–1201. doi:10.1111/cobi.12951. 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.

Languishing Leatherbacks

Leatherback turtles, Dermochelys coriacea, are the largest of all sea turtles, tipping the scales at up to 900 kg. Unlike other sea turtles, the leatherback lacks a carapace covered with scutes; instead its carapace is covered by thick leathery skin that is embedded with small bones forming seven ridges running along its back. This turtle has a wonderful set of anatomical and physiological adaptations, such as huge flippers and an efficient circulatory system, that make it a powerful swimmer and deep ocean diver. Males spend their entire lives at sea, while females usually return to their birthplace along sandy beaches to dig nests and lay eggs.

karla-hernc3a1ndez.jpg

Leatherback female on the beach at Las Baulas National Park. Credit: Karla Hernández.

Unfortunately, from the perspective of conserving awesome animals in our world, some populations of leatherbacks are declining rapidly, and many are now listed as critically endangered by the IUCN Red List. Pilar Santidrian Tomillo wanted to know why leatherback populations in the Eastern Pacific Ocean have declined so much in recent years. Working at Las Baulas National Park in northwestern Costa Rica since 1993, Tomillo and her colleagues have tagged 1927 nesting females so they could measure survival and return rates to the nesting shoreline. They discovered an alarming trend of sharp decline as described by the graph below.

TomilloFig1Tomillo and her colleagues knew that many leatherbacks were killed every year as a consequence of bycatch – capture by fishing nets or lines cast by fishermen who are targeting other species. But leatherback bycatch is very difficult to monitor accurately, as few fishermen keep accurate records of dead turtles, and turtles may die after being entangled and subsequently freed. The researchers also suspected that climate variability could influence leatherback population size. El Niño Southern Oscillation (ENSO) is a large-scale atmospheric system that affects global climate. In leatherback foraging areas, El Niño years are associated with high atmospheric pressure and warm sea temperatures, while La Niña years are associated with low atmospheric pressure and cool sea temperatures. Importantly, cool sea temperatures stimulate upwelling of nutrient-rich water to the surface, increasing production of phytoplankton, thereby increasing the abundance of  jellyfish and other favored leatherback food items. So the researchers hypothesized that the leatherbacks might do better in La Niña years than in El Niño years.

But what do they mean by doing better? There are two important factors influencing population growth: survival and reproduction. Either one could be affected by climate. By recapturing marked individuals, Tomillo and her colleagues were able to measure both survival and one important aspect of reproduction, which is how often females return to lay eggs. Reproduction is a very energetically demanding process for leatherback females, as they must migrate long distances (often thousands of kilometers) from their feeding grounds, and their eggs are large and plentiful, so females require a huge investment in resources to reproduce. Consequently, at Tomillo’s field site, only 4.5% of females reproduced in consecutive years, while the average interval between reproductive events was 3.65 years.

Let’s consider leatherback survival. As you can see from the data below, annual survival probability is very variable from year to year, ranging from about 30% in 2012 to near 100% in several years. Disturbingly, the long-term trend is downward, and the overall mean adult survival rate of 0.78 is very low in comparison to viable populations of sea turtles. If survival rates do not increase, the future is very bleak for this population.

Tomillo Fig4

Annual survival probability of adult females tagged at Las Baulas National Park. Vertical bars indicate 95% confidence intervals.

How does climate variation influence survival and reproduction? The Multivariate ENSO Index (MEI) measures ENSO strength, with positive numbers (X-axis on graphs below) indicating El Niño years (with poor food availability), and negative numbers indicating La Niña years (with good food availability). The researchers found no climate effect on survival (top graph below), but a high reproductive rate associated with La Niña events (bottom graph below).

TomilloFig5

The question remains, why is survival so low? Climate does not appear to affect survival, so that brings us back to human impact. Tomillo and her colleagues recommend reducing bycatch levels and implementing beach conservation measures to eradicate egg poaching. They also warn us that increases in global temperatures reduce egg hatching success, and pose a severe stress to this and other critically endangered leatherback populations throughout the world.

note: the paper that describes this research is from the journal Ecology. The reference is Santidrian Tomillo, P., N. J. Robinson, A. SanzAguilar, J. R. Spotila, F. V. Paladino, and G. Tavecchia. 2017. High and variable mortality of leatherback turtles reveal possible anthropogenic impacts.  Ecology 98: 2170–2179. 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.