Changing climate promotes prolific plants and satiated consumers

Plants in Sweden can have a difficult life, but climate change has provided a more benign environment for some of them, including the white swallow-wort, Vincetoxicum hirundinaria. This perennial herb grows in patches in sun-exposed rocky areas, in forests located below cliffs, and along the edges of wooded areas. The plant forms clumps that are heavily laden with flowers in June and July, and creates pod-like fruits in July and August

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Vincetoxicum hirundinaria growing in rocky outcrop (top photo). Vincetoxicum pods releasing their wind-dispersed seeds (bottom photo).

Christer Solbreck has had a lifelong interest in insect populations, and he has been following the insects that eat Vincetoxicum’s seeds for the past 40 years. As he described to me, surprisingly few population ecologists actually measure the amount of food available to insects. I should add that very few people have the resilience to study the same population of insects for 40 years, either. And interestingly, though this paper discusses the effect of a changing climate on seed production and seed predation, it was not Solbreck’s intent to consider climate change as a variable when he began, as climate change was not a concern of most scientists in the 1970s.

But climate change has happened in southeastern Sweden (and elsewhere), and has affected ecosystems in many different ways. Ecologists can quantify climate change by describing its effect on the vegetation period, or growing season (days above 5°C), which has increased by about 20 days since the mid 1990s.

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Length of growing season (vegetation period) in southern Sweden.

During the same time period the abundance of Vincetoxicum has increased sharply.

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Vincetoxicum abundance, measured as area of the research site covered, during the study.

You will note that “Vincetoxicum” has the word “toxic” in its midst; the seeds are toxic to most consumers, and are important food sources for only two insect species. Euphranta connexa females lay eggs in developing fruits of the host plant, with the emerging larva boring through the seeds and killing most of them. Lygaeus equestris is an all-purpose seed predator; both larvae and adults suck on flowers, on developing seeds within the fruits, and on dry seeds they find on the ground up to a year later.

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Euphranta connexa female lays eggs in an immature seed pod.

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Lygaeus equestra larva feeds on a fallen seed.

Solbreck teamed up with biostatistician Jonas Knape to analyze his data. From the beginning of the study, Solbreck suspected that annual variation in weather – particularly rainfall – might influence Vincetoxicum seed production, and consequent population growth of the two insect species. They discovered something quite unexpected; the dynamics of seed production shifted dramatically in the second half of the study, alternating annually from very high to very low production over that period. This dynamic shift coincides with the extension of the growth season as a result of climate change.

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Seed pod abundance by year.

The researchers argue that there is a non-linear negative feedback relationship of the previous year’s seed production on the current year’s seed production. Negative feedback occurs when an increase in one factor or event causes a subsequent decrease in that same factor or event. In this case, an increase in seed production uses up plant resources, leading to a decrease in seed production the following year. But the effect is non-linear, and does not come into play unless Vincetoxicum produces a huge number of seeds, as shown by the graph below,

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Seed production in the current year in relation to seed production in the previous year. Note that both axes are logarithmic. The curve represents the expected seed pod density generated by the statistical model, with the shaded area representing the 95% credible intervals. Open circles are data for 1977-1996, while closed circles are data for 1997-2016.

The researchers also found that high rainfall in June and July increased seed production.

So how do these wild fluctuations in seed production affect insects and the plant itself? One important finding is that in high seed production years, the proportion of seeds attacked by insects plummets because the sheer number of seeds overwhelms the seed-eating abilities of the insect consumers. Ecologists describe this phenomenon as predator satiation.

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Seed predation rates in relation to seed pod density.  Note that both axes are logarithmic. The curve represents the expected predation rate generated by the statistical model, with the shaded area representing the 95% credible intervals. Points are E. connexa predation rates while triangles are combined predation by both insect species.

As a result of predator satiation, there were, on average, seven times as many healthy (unattacked) seed pods in 1997-2016 than there were in 1977-1996. Presumably, this increased number of healthy seeds translates to an increase in new plants becoming established in the area. An important takehome message is that the entire dynamics of an ecosystem can change as a result of changes to the environment, in this case, climate change. More long-term studies are needed to evaluate how common these shifting dynamics are likely to become in the novel environmental conditions we humans are creating.

note: the paper that describes this research is from the journal Ecology. The reference is Solbreck, Christer and Knape, Jonas (2017), Seed production and predation in a changing climate: new roles for resource and seed predator feedback?. Ecology, 98: 2301–2311. doi:10.1002/ecy.1941. 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.

Is your goose cooked? Climate change and phenological mismatch.

As an undergraduate at the University of Manitoba, Megan Ross investigated nutrient reserves stored up by Lesser Snow Geese before reproduction in southern Manitoba. These reserves of fat and protein are critical to female geese, who then fly thousands of kilometers north to breeding grounds above the Arctic Circle, where they lay eggs and raise their young. For her Master’s thesis (this study), Ross investigated how nutrient levels influence adult reproductive success and recruitment of new goslings into the population.

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Lesser Snow Goose on its nest. Credit: Megan Ross

As climates become warmer and more variable, there is a danger that goose reproduction may fall out of synchrony with the availability of high quality food in the feeding grounds – a phenomenon called phenological mismatch. If eggs don’t hatch until substantially after the grass is well-established, then grass nutritive value may not be high enough to raise a goose family. The problem is that even if geese had the ability to adjust the timing of their migration, it would be very difficult for them to know what feeding conditions are like thousands of kilometers away. Ross and her colleagues explored several questions regarding phenological mismatch and how successfully Snow Geese and Ross’s Geese (a smaller relative of Snow Geese – not named after our senior author) raise their broods.

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Ross’s Goose paddling about. Credit: DickDaniels (http://carolinabirds.org/)

Those of you who hang out near ponds, golf courses, or farms probably know that goose populations are thriving. Over the past few decades, geese at Karrak Lake in Nunavut, Canada, have increased sharply in population, though the growth rate has leveled off in recent years (see graph below).

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Combined estimate of Ross’s Goose and Lesser Snow Goose population size at Karrak Lake. Credit: Megan Ross.

Measuring recruitment of goslings into a population of a million birds is not the easiest task. The researchers used helicopters to herd the birds into portable geese corrals, and then simply calculated the proportion of juveniles as their measure of recruitment. They also weighed, measured and banded all of the captured birds before releasing them, unharmed back into the environment. For each year of the study, they calculated phenological mismatch as the difference between the mean annual hatch date and the NDVI50 date (which stands for the date of 50% annual maximum Normalized Difference Vegetation Index). To calculate NDVI50, researchers use satellite images to estimate the date at which the environment achieved 50% of maximum green-up for the year.

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Small portion of the goose population near Karrak Lake. Credit: Megan Ross

Several factors were related to recruitment. For both species, recruitment was very low in years with considerable phenological mismatch (Graph a). High recruitment was associated with high levels of protein in both species (Graph b), and high levels of fat in snow geese (Graph d). Recruitment was also greatest if nests were initiated early in the year (Graph c).

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Mean annual values for Ross’s Geese (gray circles) and Lesser Snow Geese (black circles) in relation to (a) phenological mismatch, (b) female body protein index, (c) ELI (early late index) – a measure of nest initiation date (for example, ELI = -5 means that nests were initiated 5 days earlier than average on that particular year), and (d) female body fat index.

The number of eggs per clutch, and the number of nests that produced at least one gosling (nest success) were highest when geese initiated their nests earlier in the year. Snow Geese laid, on average, more eggs, than did Ross’s Geese, but Ross’s Geese had somewhat higher nesting success than did Snow Geese. But nutrients also figure into this increasingly complex picture. In years when females stored up more protein, they tended to lay more eggs.

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Three Lesser Snow Goose goslings huddle together. Credit: Megan Ross.

Not surprisingly, the researchers also demonstrated that warmer springs were associated with earlier vegetation growth (NDVI50). The geese were able to adjust somewhat to earlier NDVI50 by initiating nests earlier in the year. However, these adjustments were only partial at best, so that phenological mismatch was very high in years that greened-up early (the distance along the x-axis between the data points and the bold dotted line in the graph below).

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Mean annual hatch date for Ross’s Geese (gray circles) and Lesser Snow Geese (black circles) in relation to the date of the year that NDVI50 is reached.  The bold dotted line is the expected value if there were no phenological mismatch.

From these data, you might ask why don’t the geese migrate earlier in the spring? One problem is that they need enough protein and fat to migrate, to produce eggs and to incubate the eggs during the cool Arctic spring. Another part of the problem is that gonadal development is determined by day length – not temperature – so there is a limit to how early in the year the geese are able to begin courtship and breeding activities. The concern is that if, as expected, environmental warming continues, phenological mismatch could become more extreme, further reducing juvenile recruitment, and putting a seemingly robust population at risk.

note: the paper that describes this research is from the journal Ecology. The reference is Ross, Megan V., Alisauskas, Ray T., Douglas, David C. and Kellett, Dana K. (2017), Decadal declines in avian herbivore reproduction: density-dependent nutrition and phenological mismatch in the Arctic. Ecology, 98: 1869–1883. doi:10.1002/ecy.1856. 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.

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.

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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.

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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).

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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.

Scientists MARCH against MADNESS (in April)

Back in my formative college years, my friends and I would indulge in many spontaneous gatherings, in which the question of “What is reality” occupied the stage front and center. As consummate dabblers in multiplistic world views, we considered all conceivable answers, and chose none. But time shuffled on, and so did we, to new adventures in which the reality problem no longer seemed so central, nor so puzzling. We recognized that reality is observable, but that your senses might betray you sometimes. That seemed like enough.

Going back a bit before my formative college years, Copernicus upset this sensory world view by publishing (almost on his deathbed) “De Revolutionibus”, which proposed, and gave some evidence for the hypothesis that Earth revolved around a fixed sun (heliocentrism). Originally this provocative alternative was mostly ignored, but many years later it raised some serious issues (particularly for Galileo) as it became more seriously considered. One major objection was that the reality imparted by our senses told us that the world was standing still – otherwise would we not be blown away by a world that was racing around a sun (and rotating at a frenzied pace to boot)? A second major objection was that the consensus of scientists at the time believed that that the world was standing still and occupied the central position. A third major objection was that a heliocentric world view, if taken literally, seemed at odds with some parts of the Bible, in particular when Joshua asked the sun to stand still so the Israelites had more time to deal with the Gibeonites.

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Figure of the heavenly bodies – An illustration of the Ptolemeic geocentric system by Portuguese cosmographer Bartolomeu Velho, 1568 (Bibliotheque Nationale, Paris)

The reality of our senses is a powerful argument. Copernicus, Galileo and scientists to follow would need to come up with a great deal of physical evidence to sway humanity from the commonsense observation that Earth is still. They did so with astronomical observations (aided by the invention of the telescope) and by developing theories of inertia, momentum and gravity, which propelled our understanding of universal laws for many different applications. As the scientific evidence became more compelling, scientific consensus shifted, and now most people accept the Sun as the center of the solar system, with Earth as one of eight (or nine) orbiting planets, even though these people (including many scientists) don’t understand the physics or the underlying mathematics. Lastly, even fundamentalist Christians and Jews can now argue that Joshua was simply using the language of his time when he issued his request to the Sun.

Advancing in time to 1896, Svante Arrhenius published a paper that proposed that atmospheric CO2 levels could influence atmospheric temperatures in ways that are now familiar to us. Like Copernicus before him, Arrhenius’ ideas were initially rejected by most scientists, until new technology was applied to measuring atmospheric CO2 levels, and to developing models of how the atmosphere and climate interacted. Ultimately, these new approaches led to the development of a scientific consensus that climate is changing, that Earth’s surface is warming, and that human behavior is responsible. Over the past 60 years we have measured the changes, we have developed a more coherent scientific understanding of atmospheric processes, we have made mathematical models that generate projections and we have validated these models empirically. Unlike Copernicus and Galileo, we can observe climate change using the reality imparted by our senses (either online, in books, or by journeying to shorelines or to polar regions that are losing their cool). Unlike Copernicus and Galileo, the consensus of the scientific community is in our camp. Unlike Copernicus and Galileo, the Bible does not make any claims about climate or CO2. This reality should be a no-brainer!

But it isn’t, and I lack the omniscience to understand why this reality is being denied. One hypothesis is that the geocentric hypothesis has been replaced by the corporate-centric hypothesis, which states that corporations and their shareholders are at the center of the universe, and that financial earnings are the currency of reality. The power of this system is that these earnings, if they are maximized and judiciously applied, can be used to purchase some people’s perceptions of reality, so that their reality denies the scientific consensus. This new corporate-centric hypothesis denies scientific facts, and downgrades them with alternative facts that claim to be equally valid.

On April 22 we march across the globe to celebrate and affirm the reality of our senses, the truth of our observations, and the beauty of our complicated world. We celebrate a universe with no center, and a world with millions of different species that interact with each other and their environment in meaningful and mysterious ways. We celebrate the pursuit of rational inquiry into the processes underlying these interactions, and the deepening of our understanding of who we are as humans, and how we can, as scientists, apply real knowledge to allow our Earth to flourish.