Crawling with caterpillars courtesy of climate change – and ants

In the book of Exodus, Yahweh inflicts upon the Egyptians ten plagues, several of which have biological bases. Plagues two three, four and five are frogs, lice, wild animals and diseased livestock. But it is the eighth plague that is relevant to today’s tale – the locust explosion. As it turns out, insect populations have periodically exploded throughout recorded history (and no doubt before), and for many years ecologists have been trying to understand why insect populations are so variable. Rick Karban has taught a field course at Bodega Marine Reserve, California since 1985, and, as he describes “In some years, the bushes are dripping with caterpillars and in others they are very difficult to find.  The wooly bears (Platyprepia virginalis) are so conspicuous and charismatic that I couldn’t help wondering what was responsible for their large swings in abundance (they are more than 1,000 times as abundant in big years than in lean ones).”

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Wooly bear caterpillar density during annual surveys conducted in march of each year.

The early stage caterpillars are most common in wet marshy habitats, but as they develop, they move to dryer upland habitats where they pupate, metamorphose into moths and mate. Young caterpillars live in leaf litter, eating vegetation and decaying organic matter.

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Late instar (close to pupation) wooly bear caterpillar feeding on bush lupine. Credit Rick Karban.

Karban and his colleagues recognized that insect populations are sensitive to climate, and wondered whether climate change may be playing a role in Platyprepia population explosions. But there’s much more to climate change than global warming; for example, many areas of the world expect much more variable precipitation patterns, with more big storms and more droughts. Karban and his colleagues wanted to know whether variable precipitation might affect wooly bear populations. So they examined rainfall records between 1983 and 2016, and found that numerous heavy rainfall events (over 5 cm) in the previous year were correlated with increases in caterpillar abundance.

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Change in caterpillar abundance in relation to number of heavy rainfall events (over 5 cm) during the previous year. Note the y-axis is the natural logarithm of the change in abundance.

Karban and his students explored three hypotheses for why caterpillars increased following a year with numerous heavy rainfall events. First, perhaps more rain causes more plant growth and deeper litter, providing extra food for caterpillars. Second, heavy rains may reduce the number of predacious ground-nesting ants. Lastly, heavy rains may produce deeper denser litter providing refuge from predacious ants.

The researchers tested litter as food hypothesis by comparing caterpillar growth rates during the summer, which usually has very little rainfall. They weighed individual caterpillars, placed them into cages and supplied them with litter from either wet or dry sites. After 30 days, they reweighed the caterpillars and found that all of them had lost weight, and that there were no significant differences in weight change between wet and dry sites. Thus, at least during the summer, there was no evidence that wet sites had better food for caterpillars.

Karban and his colleagues turned their attention to ants.

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If ants stayed away from wet sites, that would suggest that rainy years may benefit caterpillars by reducing the number of ants in their habitat. To measure ant abundance, the researchers set out bait stations supplied with a sugar-laced cotton ball and 1 cm3 of hot dog. They discovered many more ants, and in particular, many more Formica lasioides (a fearsome caterpillar-killer) ants were recruited to dry sites than wet sites. This suggested that years with numerous rainfall events might reduce ant abundance, at least in the wet areas preferred by young caterpillars.

The researchers tested the ant predation hypotheses by caging caterpillars in plastic deli containers that had either window screen bottoms that allowed ants to enter but prevented the caterpillars from leaving, or had spun polyester bottoms that prevented ant access. At each of 12 field sites, the caterpillars were caged with litter that matched the depth and wetness of litter found at that site. All caterpillars protected from ants survived, while 40% of the unprotected caterpillars from dry sites and 23% of the unprotected caterpillars from wet sites were killed by predators. So ants are clearly fearsome predators, but more so under dry conditions.

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A Formica lasioides ant subdues an early install wooly bear caterpillar within the confines of a deli box. Credit Rick Karban.

But does litter wetness help protect against predacious ants? To investigate this question, the researchers placed caterpillars in deli containers that permitted ant access. At each site, two containers were placed side-by-side; one contained a caterpillar + litter from a wet site, while the other contained a caterpillar + litter from a dry site. Both containers were completely filled with litter and left in the field for 48 hours. The researchers discovered that caterpillars were 26% more likely to avoid predation if they were in a container stuffed with litter from a wet site. This suggests that litter from wet sites acts as a refuge for caterpillars against predators.

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Caterpillar survival rate in relation to litter wetness.

Unfortunately, no long-term data on ant abundance are available, so we don’t know the relationship between ant and caterpillar abundance over time. But when ants were excluded, caterpillars survived well, and when ants were present, caterpillars survived best in wet sites with deep litter. It is not clear why caterpillars survive ant predation better in wet litter. One possibility is that caterpillars are more active than ants at cooler temperatures, and may be more likely to avoid them in wet and cool conditions. A second possibility is that dry litter is structurally less complex than wet litter, and ants may be more likely to move efficiently to capture caterpillars in dry terrain.

Given the predictions for more rainfall variability in coming years, Karban and his colleagues expect caterpillar abundance to fluctuate even more dramatically from year to year. In this system, and presumably other insect populations as well, multiple factors interact to determine whether there will be a population outbreak reminiscent of Pharaoh’s experience early in recorded history.

note: the paper that describes this research is from the journal Ecology. The reference is Karban, Richard, Grof-Tisza, Patrick, and Holyoak, Marcel (2017), Wet years have more caterpillars: interacting roles of plant litter and predation by ants. Ecology, 98: 2370–2378. doi:10.1002/ecy.1917. 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.

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.

Powdery parasites pursue pedunculate oak

Studying disease transmission is tricky for many reasons. Most humans frown on what might seem like the easiest experimental protocol – release a disease into the environment and watch to see how it spreads. For his doctoral dissertation in 2006, Ayco Tack settled on a different experimental protocol – bring the potential hosts to the disease. In this study, staged in Finland, the hosts were pedunculate oak trees, Quercus robur, and the disease was the powdery mildew parasite, Erysiphe alphitoides. Almost 10 years later, Adam Ekholm continued research on the same system, with Tack as his co-supervisor.

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Trees on the move. Credit: Ayco Tack.

But before moving trees around, the researchers first needed to see how the disease moved around under field conditions.  Within a tree stand, powdery mildew success will depend on how many trees it occupies, how many trees it colonizes in the future, and how many trees it disappears from (extinction rate). The researchers measured these rates over a four year period (2003 – 2006) on 1868 oak trees situated on the island of Wattkast in southwest Finland. They also measured spatial connectivity of each tree to others in the stand. In this case connectivity is a measure of the distance between a tree and other trees, weighted by the size of the other trees. So a tree that has many large neighbors nearby has high connectivity, while a tree with a few distant and mostly small neighbors has low connectivity. Results varied from year-to-year, but in general, the researchers found higher infection rates, lower extinction rates, and some evidence of higher colonization rates in trees with high connectivity.

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Oak leaf infected with powdery mildew parasite. Credit: Adam Ekholm.

The importance of connectivity indicated that the parasites simply could not disperse efficiently to distant trees. But perhaps the environment might play a role in colonization rates as well. For example, fungi like powdery mildew tend to thrive in shady and humid environments. Thus a tree out in the open might resist colonization by powdery mildew more effectively than would a tree deep in the forest. To test this hypothesis, Tack and his colleagues placed 70 trees varying distances (up to 300 meters) from an infected oak stand. On one side of the oak stand was an open field, while the other side was closed forest. Thus two variables, distance and environment, could be investigated simultaneously.

Ayco Tack inspecting a potted tree_Tomas Roslin

Ayco Tack inspects an oak tree placed in an open field. Credit: Tomas Roslin.

The researchers collected infection data twice; once in the middle of the growing season (July) and a second time at the end of the growing season (September). Not surprisingly, infection rates were higher by the end of the growing season. In general, infection rates, and infection intensity (mildew abundance) were higher in the forest than in the field, indicating a strong environment effect. In the July survey, trees further from the oak stand had lower infection intensity, but as infection rates increased over the course of the season, the effects of distance diminished, particularly in the forest.

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Upper two graphs show the impact of habitat type on (a) proportion of trees infected and (b) mildew abundance. The lower two graphs are the influence of distance from parasite source on mildew abundance of trees set in (c) a forest habitat and (d) an open field. Mildew abundance was scored on an ordinal scale with 0 = none and 4 = very abundant.

Ten years later, Adam Ekholm, as part of his PhD dissertation that studies the effect of climate on the insect community on oak trees, added a third element to the mix – the influence of genes on disease resistance. He wondered whether certain genotypes were more resistant to powdery mildew infection. The researchers grafted twigs from 12 large “mother” trees, creating 12 groups of trees, with between 2 – 27 trees per group (depending on grafting success). Each tree in a given group was thus genetically identical to all other trees within that group.

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Oak tree placed in the forest. Credit: Ayco Tack.

The researchers chose a site that contained a dense stand of infected oaks, but was surrounded by a grassy matrix that contained only an occasional tree. To study the impact of early season exposure, Ekholm and his colleagues divided the trees into two groups; 128 trees were placed in the matrix at varying distances from the infected stand, while 58 trees were placed directly in the midst of the stand for about 50 days, and then moved varying distances away. The researchers scored trees for infection at the end of the growing season (mid-September).

 

Trees that spent 50 days within the oak stand had much higher infection frequency and intensity than trees that were initially placed in the matrix. Some genotypes (for example genotype I in graphs C and D below) were much more resistant to infection than others (such as genotypes D and J). Finally trees further from the source of infection were less susceptible to become colonized over the course of the summer (data not shown).

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Proportion of trees infected (A) and proportion of leaves infected (B) in response to early season exposure to stand of oaks infected with the powdery mildew parasite (oak stand) or no early season exposure (matrix). Proportion of trees infected (C) and proportion of leaves infected (D) in relation to tree genotype. Genotypes are labeled A – L; numbers in parenthesis are sample size for each group.

These findings illustrate how dispersal, host genotype and the environment influence the spread of a parasite under natural conditions. The parasite exists as a metapopulation – a group of local populations inhabiting networks of somewhat discrete habitat patches. Some populations go extinct while others successfully colonize each year, depending on distance from a source, tree genotype and environment. Ekholm and his colleagues encourage researchers to use similar experimental approaches in other host-parasite systems to evaluate how general these findings are, and to explore how multiple factors interact to shape the dynamics of disease transmission.

note: the paper that describes this research is from the journal Ecology. The reference is Ekholm, Adam; Roslin, Tomas; Pulkkinen, Pertti and Tack, Ayco. J. M. (2017). Dispersal, host genotype and environment shape the spatial dynamics of a parasite in the wild. Ecology. doi:10.1002/ecy.1949. The paper should come out in print very soon. Meanwhile you can also link to Dr. Tack’s website at www.plantmicrobeinsect.com 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.

Meta-analysis measures multiple mycorrhizal benefits to plants

Plants and fungi sometimes live together in peace and harmony. Arbuscular mycorrhizal associations are associations between plant roots and fungi, in which the fungal hyphae (usually branched tubular structures) grow between root cells, penetrating some cells with a network of branches or arbuscules.  Oftentimes these are mutualistic associations with both the plants and the fungi benefiting from living together. Though plants with arbuscular mycorrhizal fungi (AMF) tend to grow better than plants without AMF, it not always clear what causes them to do so.

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Kura clover, Trifolium ambiguum, grown with AMF (left) and without AMF (right). Credit: Liz Koziol.

Ecologists have traditionally viewed arbuscular mycorrhizal associations as a straightforward nutrient-carbon exchange. Fungal hyphae, with their vast surface area, pick up nutrients (such as nitrogen and phosphorus compounds) from the soil, which they deliver to the root cells in exchange for plant-produced carbon molecules.

But recently researchers have identified numerous other potential ways that the fungi help the plants, including the following: (1) promoting water uptake and transport, (2) helping to spread allelochemicals – toxic chemicals that some plants release to rid themselves of nearby competitors, (3) inducing chemical defenses against herbivores, (4) enhancing disease resistance, and (5) promoting soil aggregation or clumping, which stabilizes the soil near the roots, reduces erosion and promotes stable water flow.

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Camille Delavaux and her colleagues wondered whether these other plant benefits might actually be more important than we originally thought. Delavaux was planning to write a review paper for a 1 credit independent study, but she found so many papers on this topic that she decided to collaborate with fellow students Lauren Smith-Ramesh and Sara Kuebbing on a full-scale meta-analysis.

A meta-analysis is a systematic analysis of data collected by many other researchers. Delavaux and her colleagues used the Web of Science database to find 4410 studies on how AMF supplied plants with nutrients and 1239 studies on how AMF provided other plant benefits. That’s a lot of studies! But for the meta-analysis, the authors only used a small fraction of these studies because they set certain restrictions. For example, to be used in the meta-analysis the authors required each study to show some measure of variation for the data (such as standard deviation or standard error). In addition, the authors required each study to compare plants grown under two conditions: with AMF and without AMF.  In many studies the researchers collected soil, which they sterilized in a hot oven, and then set up a test group, which they inoculated with AMF spores or a plug of soil or root fragments that contained AMF. In addition, these studies also had a control group of plants that received only sterilized soil with no AMF added.

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A collection of eight different species of AMF spores. Credit: Liz Koziol.

Delavaux and her colleagues compared how plants performed with and without an AMF. Because each study was different, one might only have been looking at the effects of AMF on nitrogen uptake performance, while a second study might consider how AMF influenced soil aggregation. Effect size (Hedges d+) compares mean performance of the AMF plant to mean performance of non-AMF plants for a particular variable (such as nitrogen uptake or soil aggregation). A positive effect size means that the AMF plant did better. Of course we need to know how much better is biologically meaningful, so for each variable the researchers calculated the 95% confidence intervals of the mean effect size. If the 95% confidence intervals were positive, then Delavaux and her colleagues could be 95% confident that there was a biologically important effect of AMF on plants for that particular measure of performance.

As expected, the researchers found a positive effect of AMF on plant nitrogen uptake. The mean effect size was 0.674 with a 95% confidence interval of 0.451- 0.912. We can interpret this to mean that we are 95% confident that the true mean effect size on nitrogen uptake is between 0.451 and 0.912. But the greatest effect of AMF on plants was on soil aggregation (mean effect size = 1.645, 95% confidence interval = 1.032 – 2.248). AMF also had significant positive effects on phosphorus uptake, water flow and disease resistance.

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Mean effect size (Hedges’ d+) of AMF on different factors considered in the meta-analysis.  The horizontal error bars are the 95% confidence intervals. n = number of observations.  If the error bars do not cross zero, inoculation with AMF had a significant positive effect relative to plants without AMF.

This meta-analysis shows that AMF help plants in many different ways. Researchers knew about the AMF impact on nitrogen and phosphorus uptake, but may be surprised to learn of equally strong effects on water flow, disease resistance and soil aggregation. Consequently, AMF may be very useful for forest management, agriculture, conservation and habitat restoration. As examples, conservation biologists and forest managers may need to consider adding AMF to soils that have suffered severe burns from fires, which may kill the existing soil fungi. Or agriculturalists intent on growing a particular crop may want to inoculate the soil with a specific group of AMF spores that enhance soil aggregation and water uptake, so their crop may thrive in a habitat that might otherwise not be suitable.

More than 3/4 of land plants form associations with AMF. Consequently, any attempts to restore habitats or to maintain high levels of species diversity in existing ecosystems require understanding what types of AMF inhabit the soils, and how these AMF influence ecosystem functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Delavaux, C. S., Smith-Ramesh, L. M. and Kuebbing, S. E. (2017), Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology, 98: 2111–2119. doi:10.1002/ecy.1892. 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.

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.

scheele-fig-1.png

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).

scheele-figure-2.png

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.