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.

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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.

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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.

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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.

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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.

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.

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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.

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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.

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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.

Biological control: birds vs. (insects vs. insects)

We all know that birds eat crop-destroying bugs, so we might think that farmers would welcome insectivorous birds to their fields with radiant rakes or happy hoes. But not so fast! Research by Ingo Grass and his colleagues alerts us to the reality that not all insects are created equal. Some insects eat crops, but some insects eat insects that eat crops.

Aphids are one of the worst scourges of the agricultural world. They suck the phloem sap from many plant species; this action can kill the plant directly, and also cause infections by plant pathogens and viruses. Fortunately for farmers, many animals enjoy eating aphids, including birds such as the Eurasian Tree Sparrow, Passer montanus, and insects such as ladybird beetles and hoverfly larvae.

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Hoverfly larva consumes an aphid while a second aphid looks on. Credit: Beatriz Moisset.

Grass and his colleagues knew that sparrows eat both aphids and hoverflies, but they did not know how the effects of bird predation on these insects cascaded down to the oats and wheat crops grown near Gottingen, Germany. Their research tested the hypothesis that sparrows eat so many hoverflies that aphid abundance actually increases (despite also being eaten by sparrows), and oat and wheat abundance decreases (top food web in the diagram below). If so, they reasoned that removing the birds would increase hoverfly abundance, thereby decreasing aphids and increasing grain abundance (bottom food web).

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Agricultural food web with (top) and without (bottom) sparrows. Arrows show consumption, with dashed arrows indicating weak effects, and solid arrows and doubled organisms indicating strong effects.

The researchers set up an experiment with 11 nest boxes strategically placed between an oat field and a wheat field. Each box was equipped with a camera, so the researchers could see what the parents fed to their nestlings. In addition, Grass and his colleagues set up eight 4 X 5 meter plastic mesh exclosures which excluded birds, but allowed insects free access. They periodically surveyed 50 plants in each exclosure and in equal-sized control plots for hoverflies and aphids over the course of the sparrow breeding season. Because these birds can have three broods, this project kept them (the sparrows and the researchers) busy from early May to late July.

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The birds fed very little on the two grain fields during the first brood, but towards the end of their second brood, they turned their attention to feeding on insects from the two grain fields, and later to eating the ripening grain. One important finding is that bird predation severely reduced hoverfly abundance. By early July hoverfly abundance was about 1 per 50 shoots when birds were present, and more than 3 per 50 shoots when birds were excluded (top graph below).

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How did hoverfly consumption translate to aphid abundance? As you can see from the bottom graph, by early July, aphid abundance without birds was considerably lower than aphid abundance in the presence of birds. Taken together, these findings indicate that European Tree Sparrows consume hoverflies, which ultimately leads to an increase in aphid abundance.

Grass and his colleagues conclude that insectivorous birds can interfere with natural pest control of cereal production in central Europe. When birds were experimentally excluded, aphid densities declined 24% in wheat and 26% in oat crops. European Tree Sparrows were doubly bad for the crops, as they also harvested substantial quantities of grain from these fields to feed their third brood. The researchers argue that management of biological control systems for agriculture requires a broad food-web perspective that accounts for trophic cascades, such as the interactions that occur among sparrows, hoverflies, aphids and various types of economically important grain crops.

note: the paper that describes this research is from the journal Ecology. The reference is Grass, Ingo, Katrin Lehmann, Carsten Thies, and Teja Tscharntke. 2017. Insectivorous birds disrupt biological control of cereal aphids. Ecology 98 (6): 1583-1590Thanks 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.

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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.

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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.

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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.

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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).

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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.

Fires foster biological diversity on the African savanna

As an ecology student back in days of yore, I was introduced to the classic mutualism between ants and swollen-thorn acacia trees. In this mutually beneficial relationship, ants protect acacia trees by biting and projecting very smelly substances at hungry herbivores, and by pruning encroaching branches of plant competitors. In return for these services, acacia trees provide the ants with homes in the form of swollen thorns, and in some cases also provide food for their defenders.

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Swollen thorns of Acacia drepanlobium occupied by C. nigriceps. Credit: Ryan L. Sensenig.

I always assumed there were limits to what these ants could do. I knew that elephants were a constant problem for trees trying to get established on the African savanna. I figured, wrongly, that ants could not do much to counter a determined thick-skinned elephant. But as Ryan Sensenig describes, ants will swarm any intruding elephant, rushing into the elephant’s very sensitive trunk and mouth, biting it and, in some cases, exuding a chemical compound that is very offensive to an elephant’s keen sense of smell. So don’t mess with these ants if you can help it!

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The Laikipia Plateau has one of the few growing elephant populations in East Africa. Credit: Ryan L. Sensenig.

Fires play an important role in savanna ecosystems, killing many trees before they can get established, and creating a mosaic of burned and unburned areas which vary in grass quality and quantity, and in the abundance of acacia trees (and other species as well). Recently burned grasslands tend to be lower in grass abundance and higher in grass nutrient levels. In a previous study of controlled burns, Sensenig and his colleagues showed that larger animals, such as elephants, tended to graze in unburned areas, which had more grass – albeit of lower quality. Returning seven years after the burn, he was surprised to find that elephants, which eat both trees and grass, had shifted to the burned sites in preference to unburned sites. He thus wondered whether fire was having an impact on the ant-acacia mutualisms that defend acacias from elephants and other large herbivores.

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Sunset strikes an Acacia xanthophloea on Mpala Research Centre in Laikipia, Kenya. Credit: Ryan L. Sensenig.

Ants do not share trees. In Mpala Research Centre in the Laikipia Plateau of Kenya, there are four mutually-exclusive species of ants that live in Acacia drepanolobium trees: Crematogaster sjostedti, C. mimosae, C. nigriceps, and Tetraponera penzigi.

Sensenig and his colleagues wanted to know whether the controlled burns had a long-lasting effect on ant species distribution on acacia trees. The researchers surveyed 12 plots that had been burned seven years previously and an equal number of unburned plots to see how burns affected which ant species were present.

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Goshen College research students estimate ant densities on Acacia drepanolobium trees in the Kenya Longterm Exclosure Experiment. Credit: Ryan L. Sensenig.

They found that C. nigriceps was more common in acacias from burned areas while the other three species were more common in trees from unburned areas.

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Why were there more C. nigriceps ants in previously burned areas? One explanation is that perhaps C. nigriceps is better at avoiding getting burned by fire, or else is better at recolonizing after a fire. To look for species difference in response to fire, the researchers simulated fires by burning elephant dung and dried grass in 3-gallon metal buckets, creating a small sustained smoke source. They stationed observers every 50 meters along a 500 meter transect for the first experiment, and a 1.8 km transect for the second experiment. They then measured ant-evacuation rate by counting the number of ants moving down the trunk. There were some very pronounced differences, with C. nigriceps having the highest evacuation rate, C. mimosae also showing a strong smoke response, and the other two species showing little evidence of any response.

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Evacuation rate for each species in response to smoke.

C. mimosae generally prevails when it battles a colony of C. nigriceps. These results indicate that the subordinate C. nigriceps is able to maintain its presence in the community, in part, by taking advantage of its superior performance when it encounters a fire. The researchers also found some evidence that C. nigriceps is better at recolonizing after a fire than is C. mimosae. So despite being the subordinate species, C. nigriceps is abundant in this ecosystem.

Returning to those elephants, the researchers describe one final experiment in which some plots had a series of fences that excluded herbivores, while other plots were open to herbivores, including elephants.

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In this experiment, as well, there were burned and unburned plots. In general, there were more ants present when herbivores were present, as the trees invested more in swollen thorns and in ant food (in the form of nectar) to attract protective ants. In addition, ants were more abundant in unburned plots than in plots that had been previously burned, with the exception of C. nigriceps when herbivores were excluded.

Ecologists have long known that fire maintains savanna ecosystems by preventing the grasslands from being overgrown by trees. This study shows that fires shift ant community structure in favor of the subordinate ant species (C. nigriceps), resulting in a higher diversity of ant species overall. The researchers suggest that if fires become more common in savannas, elephants may become more attracted to acacias that harbor a reduced (or nonexistent) cast of defenders, which could lead to a further reduction in the abundance of acacia trees and their mutualistic ants.

note: the paper that describes this research is from the journal Ecology. The reference is Sensenig, R. L., Kimuyu, D. K., Ruiz Guajardo, J. C., Veblen, K. E., Riginos, C., & Young, T. P. (2017). Fire disturbance disrupts an acacia ant–plant mutualism in favor of a subordinate ant species. Ecology, 98(5), 1455-1464.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.