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).”

KarbanFig1

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.

KarbanFig4

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.

KarbanFig6

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.

Karbanantpredation

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.

KarbanFig7A

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

Solbreck1AB

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.

Solbreck2B

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

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

Solbreck2Ayes

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.

Solbreck1D

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.

Solbreck2Cyes

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,

Solbreck3yes

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.

Solbreck4yes

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.

Ayco Tack

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.

Mildew_Adam Ekholm

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.

EkholmFig3

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.

Ayco Tack

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).

EkholmFig2

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.

Thecolony

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).

RossFig1

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).

RossFig4b

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.

Subsidized Shorelines: where pelagic meets benthic

Chris Harrod met his wife, Christina Dorador, while both were working at the Max Planck Institute for Limnology in Germany.   Subsequently Dorador began a postdoctoral position in her native Chile, and Harrod went for a visit over Christmas, 2007. He was impressed by the beautiful rocky inshore habitat that was dominated by kelp forests and many species of invertebrates and fish.

Macroalgal forest

Rocky shoreline near Tocopilla, Chile. Credit: Chris Harrod.

As a fisheries biologist, Harrod soon immersed himself in the inshore kelp forest-dominated ocean, and was stunned by the sheer volume of stuff floating around. The water was green rather than blue, and filled with decaying phytoplankton and zooplankton. Where did all this stuff come from? Harrod knew that off the Peruvian and north Chilean coasts, prevailing winds move surface waters away from the shoreline, inducing upwelling of deeper nutrient-rich waters to the surface. This nutrient flux is the basis of a huge anchoveta fishery, which feeds humans, fish, marine invertebrates and marine mammals. He wondered whether the mass of floating debris in the inshore habitat might originate from offshore waters brought in from upwelling, and if the debris actually fueled some of the larger fish and molluscs that dominate inshore kelp forests. The prevailing opinion was that the energy for these fish and molluscs originated from the inshore photosynthetic kelp, rather than from photosynthetic phytoplankton further offshore that get their nutrients from upwelling.

Bilagay

Two bilagay, Cheilodactylus variegatus, swim among green algae in a debris-laden inshore habitat off the coast of Chile. Credit: Chris Harrod.

While you can ask a fish or mollusc what they had for dinner, it is very difficult to get them to respond. Fortunately, ecologists can use stable isotope ratios – the ratio of a rare (and nonradioactive) isotope of an element to its standard common isotope – to help get the answers they need. Harrod collaborated with several researchers in this study, including his Master’s student, Felipe Docmac, who collected and analyzed much of the data and was the first author of the paper. Docmac and his colleagues used the ratio of heavy and light isotopes of carbon (C) and nitrogen (N) to calculate d13C (the ratio of 13C to 12C) and d15N (the ratio of 15N to 14N) to infer where inshore fish were getting their energy.

The basic question was whether the nutrients supporting the food web were primarily from pelagic or benthic sources. In this case, the pelagic source refers to phytoplankton from the offshore areas of upwelling, while the benthic source refers to kelp and green algae that grow on the bottom (benthos) of the inshore habitat. Docmac and his colleagues collected invertebrates and large fish from five different sites along the north Chilean Coast, and calculated 13C and 15N values from tissue samples. Invertebrates were divided into two groups: filter-feeders were represented by mussels, which fed on suspended materials (such as the prolific floating debris), while benthic grazers were gastropods (snails) that fed on benthic kelp and green algae.

Fig1A

Five collection sites along the northern coast of Chile.

I’m going to skip the precise details of how stable isotope analysis actually works; I’ll provide enough information so you can understand the findings. There are two important facts to keep in mind. First an animal’s stable isotope ratio is influenced by the stable isotope ratio of its food source. So an animal feeding on prey with high d13C and d15N will itself have higher stable isotope ratios than will an animal feeding on prey with lower d13C and d15N. Second, the stable isotope ratio increases as we go up the food chain in a predictable manner, because the lighter isotopes of carbon and nitrogen tend to be more readily excreted than are the heavier isotopes.

We are now ready to look at the data. First, notice that while there is some variation from location to location, the (Pelagic) mussels tend to have consistently lower d13C values than do the (Benthic) gastropods (X-axis of graph), but fairly equivalent d15N values (Y-axis of graph). The benthivorous fish have, as we would expect from animals higher up the food chain, much higher d15N values than either of the invertebrates. But here is the key. The benthivorous fish have a much lower d13C value than do the benthic invertebrates (gastropods). If gastropods (and presumably other grazers) were in the benthivorous fish food chain, then we would expect the fish to have a higher d13C value than do the benthic gastropods. The researchers thus conclude that these fish are deriving most of their energy from the pelagic debris that is washing in from ocean currents.

Fig1B

d13C (X-axis) and d15N (Y-axis) stable isotope values in benthivorous fish (black circles).  Bars emanating from each point indicate 95% confidence intervals (CI). Numbers inside symbols indicate the site of origin for each sample (see map above), Also shown are values for filter-feeding mussels (red up-pointing triangles) and grazing gastropods (blue down-pointing triangles). Gray lines indicated predicted values of diets that were based solely (100%) on pelagic or benthic sources.

The researchers were stunned by these findings. Going into the study, Harrod did not know what he would find, but would not have been surprised by a 15% contribution from pelagic sources, or maybe even 30%. But he was blown away that the data indicated estimates of greater than 90% pelagic contribution at most of the sites. Ecologists have long known that one ecosystem may subsidize a second ecosystem with resources. For example, salmon carcasses can provide nutrient subsidies to trees near riverways, or even deeper into the forest after being transported by bears. But the extent of the subsidy in this study is unprecedented. Docmac and his colleagues urge researchers to explore exactly how the pelagic materials get into the food web, and to see whether such subsidies are common near other upwelling zones worldwide so that coastal resources can be managed more effectively.

note: the paper that describes this research is from the journal Ecology. The reference is Docmac, Felipe, Miguel Araya, Ivan A. Hinojosa, Cristina Dorador, and Chris Harrod. 2017. Habitat coupling writ large: pelagic‐derived materials fuel benthivorous macroalgal reef fishes in an upwelling zone. Ecology doi:10.1002/ecy.1936. It was published online on Aug. 2, 2017, and should appear in print very soon. 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.

Biodiversity: it’s who you are

It is a massive understatement that ecologists and conservation biologists are profoundly interested in how disturbance affects biological diversity. Humans are disturbing ecosystems by degrading or destroying habitat, by fragmenting habitat into pieces that are too small to sustain populations, by directly overexploiting species for consumption or other purposes, and by introducing non-native species (and there’s more!). Some biologists argue that disturbance has gotten so severe that we need to modify our worldview of ecosystems. They argue, for example, that intact grasslands are so rare that we should stop talking about them as an ecosystem (or biome), but rather should more realistically explore the ecology of different types of croplands, which are, in actuality, primarily disturbed grasslands.

Some types of ecosystems, such as rainforests, have survived human impact more than others, but all have been highly disturbed. So it is fitting that conservation ecologists devote their attentions to understanding how disturbance influences biological diversity. Working in Cameroon in 1998, John Lawton and his colleagues assessed species richness (number of different species) in relation to level of disturbance experienced by eight different animal groups: canopy beetles, flying beetles, butterflies, canopy ants, leaf-litter ants, nematodes, termites, and birds. They discovered that more intense disturbances were associated with a significant reduction in species richness for many of the groups.

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Tropical forest in Cameroon. Credit: Earwig via Wikimedia Commons

Nigel Stork worked with Lawton on the original study, and recently reanalyzed the data in the context of changes that have occurred in how conservation biologists view biological diversity. For example, many biologists now argue that conserving biological diversity requires understanding which species are affected by disturbance, rather than the number of species. In addition, not all disturbances have similar impacts on biological diversity. For example, logging with heavy equipment removes trees and compacts soil, while logging with lighter equipment does not compact soil, so the two treatments may have very different impacts. Finally, it may be more informative to group species according to ecosystem function rather than by taxonomic group.

StorkFig1

Locations of sampling plots within the Mbalmayo Forest Reserve, Cameroon.  The three blown-up sites had multiple plots with different levels of disturbance, as indicated by the key.

Stork and his colleagues only had data for six of the original eight taxonomic groups. They categorized intensity of disturbance based on how much tree biomass was removed, level of soil compaction, time since disturbance, and tree cover and diversity at time of sampling. This allowed the researchers to assign a disturbance index to each plot, with 0 indicating least disturbed and 1.0 indicating most disturbed. This analysis showed no significant relationship between disturbance and species richness in five of the six taxonomic groups, with only termites declining in richness in response to disturbance.

StorkFig3

Species richness in relation to intensity of disturbance for six taxonomic groups considered in the study.

Stork and his colleagues used a slightly different approach to assess the response of species composition (the identity of species that are actually present in the community) to disturbance. They compared each pair of surveyed plots in relation to how different they were in disturbance. Plots with very different levels of disturbance had disturbance dissimilarities close to 1.0, while plots with similar levels of disturbance had disturbance dissimilarities near 0. They then looked at community dissimilarity to explore changes in species composition. Plots with a community dissimilarity near 1.0 had very different species, while plots with a community dissimilarity near 0 had very similar species.

Here’s what they found. For five of six groups, disturbance dissimilarity was associated with significant (solid line) or borderline significant (dashed line) increases in community dissimilarity. So even though the number of species was not affected very much by disturbance (excepting termites), species composition was affected in all groups, with the exception of canopy ants. They conclude that a disturbed forest has very different types of species in it, but not necessarily fewer species.

StorkFig2

Community dissimilarity in relation to disturbance dissimilarity. For five taxonomic groups, plots that had the greatest differences in disturbance also had the greatest differences in species composition.

Lastly, this study shows that response to disturbance is related to the functional group – the role that each species plays within the community. For example, beetles showed a strong response to disturbance, but in reality the strong response was only true for the herbivorous beetle functional group. Beetles that ate fungi or were predators or scavengers showed relatively little change in species composition in relation to disturbance.

So what should conservation ecologists do with this information? Given the diversity and intensity of disturbance globally, we need to develop a better understanding of how species and communities respond to global change. Species composition may be a more sensitive indicator of disturbance than is species richness. Functional groups may be more helpful than taxonomic groups in identifying how disturbance influences how ecosystems actually work. Perhaps monitoring particular functional groups can give us insight into how unrelated groups with similar ecology might respond to a world that promises to experience increasing levels of disturbance.

note: I discuss two papers in this blog.  The original is from the journal Nature. The reference is Lawton, J.H., Bignell, D.E., Bolton, B., Bloemers, G.F., Eggleton, P., Hammond, P. M., Hodda, M., Holt, R.D., Larsen, T.B., Mawdsley, N.A., Stork, N.E., Srivastava, D.S., and Watt, A.D. 1998. Biodiversity inventories, indicator taxa and effects of habitat modification in tropical forest. Nature, 391: 72-76. The second paper that reanalyzes the original data is from the journal Conservation Biology. The reference is Stork, N.E., Srivastava, D.S., Eggleton, P., Hodda, M., Lawson, G., Leakey, R.R.B. and Watt, A.D., 2017. Consistency of effects of tropical‐forest disturbance on species composition and richness relative to use of indicator taxa. Conservation Biology 31 (4): 924-933. 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.

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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.

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.

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.

Ecology Fig1

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.

EcologyFig2

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.

Life and death in a diminutive ecosystem

Ecosystems are big things, as they encompass an entire community of organisms and the nonliving factors (such as nutrients and water) that interact with the community. So we’re accustomed to thinking about the Serengeti as an ecosystem, as it includes (among many things) the large animals, such as lions, wildebeest and buffalo that live there, the animals and plants they eat, and the soils and nutrients that feed these plants.

But ecosystems can also be tiny. Let’s think about an individual tank bromeliad, Quesnelia arvensis, which can hold up to 3 liters of water in tanks formed where individual leaves come together. Gustavo Romero has identified over 140 species of invertebrates that live within these natural tanks, including large predators such as damselfly and tabanid larvae, and many species of smaller predators (mesopredators) including a diverse group of chironomid midges. The larger predators eat the smaller predators, while predators of both sizes eat a very diverse group of detritivores – animals that feed on the remains of dead organisms. The terrestrial fauna in the immediate vicinity are spiders. Visitors from the surrounding forest ecosystem include 12 bird species and 6 frog species, which forage on larvae within the bromeliads.

Cantorchilus longirostris on bromeliad (Quesnelia arvensis) leaf

Long-billed marsh wren perches on the tip of bromeliad leaf.  This bird can use its long beak to probe for invertebrates living within the bromeliad tank. Credit: Crasso Paulo Bosco Breviglieri

Crasso Paulo Bosco Breviglieri and his colleagues had previously done research demonstrating how insectivorous birds hanging out near bromeliads inhibited dragonflies from ovipositing (laying eggs) within the bromeliad tank. As these birds were much larger than the animals living within the tanks, Breviglieri and Romero hypothesized that the birds would focus on eating the largest items offered to them by this ecosystem. By removing the largest items (the top predators), birds increase the biomass of the prey of these top predators, including detritivores. Thus bird predation should indirectly increase decomposition rate and nutrient availability.

Breviglieri food web

Effects of birds and frogs on bromeliad trophic cascades. Solid arrows are direct effects and dashed arrows are indirect effects (for example frogs eat top predators, thereby indirectly increasing mesopredators).  Wider arrows are stronger effects.

Trophic cascades, a process in which the effects of consumption within an ecosystem cascade down from higher to lower feeding levels, can be difficult to study. The problem is that one favorite approach is to remove predators (the top trophic level) and see if prey abundance increases while the food of these prey decreases, and so on. This is extremely challenging when top predators are lions or wolves and ecosystem area encompasses thousands of kilometers, but much easier when predators are birds or frogs, and each ecosystem is a tank bromeliad. Simply put a cage over a tank bromeliad and presto!, no birds or frogs can get in.

Dr. Crasso Paulo B. Breviglieri building the cages that isolated the bromeliads

Breviglieri with a caged bromeliad. Credit: Jennifer Tezuka

Breviglieri and Romero collected 30 tank bromeliads from the forest, and meticulously cleaned each plant to remove all organisms and organic matter. They filtered and homogenized the water from the bromeliads, and returned 1 liter of water to each plant so that each plant began the experiment with the same quantity of water and microorganisms. The researchers then added equal numbers of organisms to each bromeliad from all of the trophic levels, ranging from apex predators such as damselflies down to detritivores, such as shredders, which eat dead plant leaves and begin the break down process. They also added 10 leaves to each tank for detritivore consumption and further decomposition.

For their experiment, Breviglieri and Romero had three different treatments, with 10 bromeliads per treatment: (1) caged, with each bromeliad enclosed within a steel mesh that allowed insects through but restricted birds and frogs, (2) open-cage control, with each bromeliad only partially enclosed so predators had free access, (3) uncaged control. They returned these to the field at 40 meter intervals, and allowed 155 days to pass.

Larva of zygoptera on bromeliad (Quesnelia arvensis)leaf

Bromeliad with a damselfly larva (top predator) that for unknown reasons has climbed out of the tank onto a leaf.  A bird flew to a nearby perch, but the alert damselfly dove back down into the tank, earning a 9.6 from the judges. Credit: Crasso Paulo Bosco Breviglieri

After 155 days, Breviglieri and Romero collected all of the bromeliads, and identified, counted and weighed (dry weight) all of the organisms. They discovered that the dry mass of invertebrates was much greater in the caged treatments than either control (Figure A). The abundance of apex predators (damselflies and tabanids) did not increase; but the size of individuals increased dramatically (Figure B). Mesopredators increased in abundance (Figure C), while shredder abundance declined sharply (Figure D). Shredder larvae forage on sediment and are a favorite damselfly food item, so it is not surprising that shredders declined, given the sharp increase in damselfly size, and presumably appetite.

BreviglieriFig3ABCD

Lower shredder abundance in the caged bromeliads led to a sharp decline in decomposition rates (left graph below). In theory, this should make fewer nutrients available to the bromeliads and reduce bromeliad growth. In contrast to expectations, caged bromeliads actually grew more leaves (right graph below), despite the reduction in decomposition rates. Breviglieri and Romero remind us that the greater mass of larvae were producing a much greater mass of fecal matter and prey carcasses, both of which are very nutrient rich. Also, higher predation rates can cause some insects to mature and leave their tank at a smaller size, consuming fewer nutrients while in the larval form, and leaving more nutrients for each plant to use for its own growth.

BreviglieriFig3EF

Decomposition rate measured as detrital mass lost (left graph), and growth rate measured as new leaves grown by the bromeliads (right graph), for caged, open-caged and uncaged controls.

Clearly, there are many unanswered questions about this trophic cascade. For example, why don’t the number of top predators increase in abundance when birds and frogs are excluded? When I asked him this question, Breviglieri suggested that two processes could explain this finding. First, top predators eat smaller larvae of their own species. Second, female insects can chemically sense the presence of predators in these bromeliads, and refrain from ovipositing in plants hosting large predators.

Perhaps most important, can we extend the conclusions from these small ecosystems to larger ecosystems? In nature there are many analogous ecosystems in which predators have strategies for crossing boundaries and influencing ecosystem processes. For example, many birds dive into lakes searching for fish and invertebrates. Moving in the opposite direction, banded-archerfish spit out water jets to dislodge invertebrates from adjacent vegetation into the water, and crocodiles leave rivers to grab and consume convenient gnus. In these systems, as in bromeliads, predators cross ecosystem borders to feed, and it is important for us to understand if there are any general patterns in how these visitors from the outside affect ecosystem functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Breviglieri, Crasso Paulo Bosco, and Gustavo Q. Romero. 2017. Terrestrial vertebrate predators drive the structure and functioning of aquatic food webs. Ecology. doi:10.1002/ecy.1881.  It was published online on June 12, and should appear shortly in print. 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.

Limpet larvae and their fantastic voyage

As he began his PhD program, Takuya Yahagi was puzzled by some laboratory findings. Juvenile red blood limpets, Shinkailepas myojinensis, seemed to survive and grow extraordinarily well at temperatures between 15-25° C. Adult limpets live in deep sea vent communities, where temperatures generally range between 6-11° C.

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Adult Shinkailepas myojinensis.  These are approximately 6 mm in length. Credit: Takuya Yahagi.

Yahagi and his colleagues wondered why limpets are making babies that survive and grow at much higher temperatures than they are likely to experience after hatching.

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Deep sea hydrothermal vent community at 795 meters depth at Myojinsho Caldera in the northwest Pacific. White patches on the rocks are vast communities of chemosynthetic bacteria which are being grazed by purple/pinkish limpets. You can also see the white feathery feeding legs of a barnacle population in the upper portion of the photo. Credit: JAMSTEC

Yahagi reasoned that perhaps, in the natural world, the limpet juveniles live in different (warmer) environments than do their parents. If they migrated closer to the sea surface, their world would be somewhat warmer. But limpet babies are microscopic, so capturing them near the sea surface (and knowing that you had captured them!) is very challenging. Working with three other researchers, Yahagi decided to collect indirect evidence to test the hypothesis that baby limpets migrate to the surface where they feed and grow before returning to the ocean depths.

YahagiFig3

Larval S. myojinensis limpet 156 days after hatching. sh=shell, f =foot, e=eye, vl=velar lobe.

Initially, the researchers needed to determine what temperatures these growing limpets preferred. With the help of a remotely operated submarine, they collected adult limpets laden with egg capsules, and placed newly hatched larvae into separate containers under different conditions. Some larvae were fed and raised at one of six different temperatures: 5, 10, 15, 20, 25 and 30° C. Other larvae were starved at 5, 15 or 25° C to see how long they survived at different temperatures. If the larvae were migrating upwards to warmer waters, it was important to see how long they could survive until they arrived at the richer food sources near the surface.

Starved larvae survived up to 150 days at the lowest temperature, and for more than three weeks at 25° C, which provided ample time for upward migration (even at very mellow baby limpet swimming speeds). Fed larvae grew much more quickly at warmer temperatures, with best growth at 25° C, and no growth at 5-10° C, which is the approximate temperature at hydrothermal vents.. Larvae initially grew quickly at 30° C, but long term exposure to that temperature killed them.

YahagiFig4

Growth (shell length) of fed larvae at different temperatures.

These temperature profiles corresponded to temperatures at the sea surface down to about 100 meters, which ranged between 19-28° C. This correspondence supported the hypothesis that juveniles migrated upwards in the water column after hatching. But could Yahagi and his colleagues find any direct evidence for this vertical migration? To answer this question, they video-recorded new hatchlings in a clear plastic bath, and measured how fast these limpets swam, and what direction they preferred. They discovered that new hatchlings constantly swam upward in their test bath, and swimming speed was considerably faster at warmer temperatures.

The sea surface is a wonderful place to find food, because sunlight is abundant, so there are abundant phytoplankton to satisfy even the most voracious juvenile limpets. But sea surfaces also have very strong currents which can whisk juvenile limpets hundreds or thousands of kilometers away. The upshot is that vertical migration and wide dispersal of juveniles by ocean currents can introduce new genes into far-away limpet populations.

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A hot vent animal community at 700 meters depth at Minami-Ensei Knoll in the northwest Pacific. Prevalent groups include lobsters (white), two species of shrimp, mussels and two different limpet species. Credit: JAMSTEC.

Gene flow – the movement of genes from one population to another – has some important genetic impacts. Without gene flow, two populations that are separated from each other can become genetically distinct. But the mixing of genes from long-distance dispersal can prevent this from occurring. The researchers compared 1218 base pairs of the COI gene from 77 adult limpets that were collected from four different sites which were separated, in some cases, by more than 1000 kilometers. In support of the gene flow hypothesis they found no evidence of any genetic differentiation among the four populations.

Yahagi Fig1

Hydrothermal vent fields in the northwest Pacific Ocean.  Black squares are limpet collection sites for this study.  Notice the vast distances separating these populations.

Gene flow requires long distance dispersal, and the adult limpets travel very little along the sea floor. This finding of no genetic differentiation among the geographically separated populations supports the hypothesis that the juveniles migrate upwards, feed on abundant phytoplankton, and are carried to new distant environments. There, they mature and settle into new ocean vent communities where they can feed on the superabundant chemosynthetic bacteria associated with the ocean vents. But we still don’t know how limpets find a new ocean vent community – do they migrate, checking out possible vent habitats, while they are still juveniles and still capable of swimming? Do they have sense organs that pick up environmental cues such as hydrogen sulfide content, water temperature, turbulence or noise from vent emissions, to help them complete their fantastic ocean voyage?

note: the paper that describes this research is from the journal Ecology. The reference is Yahagi, Takuya, Hiromi Kayama Watanabe, Shigeaki Kojima, and Yasunori Kano. 2017. Do larvae from deep‐sea hydrothermal vents disperse in surface waters? Ecology 98: 1524-1534Thanks 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.