Rewilding tropical forests: dung is the key

Rewilding means different things to different people. Basically, it involves restoring a species, or several species to an area from which they have been extirpated by humans. Conservation biologists might study the population size and distribution of the returned species, ecologists might focus on interactions between the returned species and other species, while anthropologists might investigate how humans in the area are adjusting to having a new species in their lives.  One of the most famous examples of rewilding is the return of gray wolves to the Greater Yellowstone Ecosystem in western U.S.A., which can be looked at from the perspective of how the wolf populations are doing numerically, how they affect their prey (elk) or their prey’s prey (willow and aspen in the case of elk), and how they affect ranchers in the surrounding areas.

Conservation ecologists have begun a major rewilding program in Tijuca National Park in Brazil, introducing agoutis in 2010 and brown howler monkeys (Alouatta guariba clamitans) in 2015. Howler monkeys were extirpated from this park over a century ago, so ecologists worried that the monkeys might interact with the remaining species in unexpected ways.  For example, this forest hosts several species of invasive fruit trees, such as the jackfruit (Artocarpus heterophyllus). Luisa Genes and her colleagues were concerned that howler monkeys might eat fruits from these trees, and poop out the seeds in new forest locations, causing the invasive species to spread more rapidly.

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Introduced howler monkey holding the second baby born to her in the forest. Credit: L. Genes.

Even a disturbed rainforest such as Tijuca National Park hosts a large number of plant species, so the interactions can be complex and difficult to study.  As is so often the case in ecology, one very important complex of interactions involves poop.  Specifically, howler monkeys eat fruit off of trees, and poop the seeds out, usually at a new location, effectively dispersing the seeds.  But there is a second link in this seed dispersal interaction.  Twenty-one species of dung beetles use howler monkey poop for food for themselves and their offspring, breaking off small sections into balls and rolling the balls to a new location.  This process of secondary dispersal is nice for the beetles, but also for the seeds within the balls, which can now germinate in a new location without competing with the large number of seeds in the original howler monkey pile.

RafaelBrixDungBeetles

Two dung beetles battle over a dung ball. Credit: Rafael Brix.

Genes and her colleagues were interested in two basic questions.  First, were the howler monkeys eating fruit from a few select tree species, or were they eating from many different types of trees, thereby dispersing seeds from many species?  Before releasing the monkeys (two females and two males), they attached radio transmitters to the monkeys so they could easily track them, and note what they ate.  Based on 337 hours of observation, the howler monkeys ate fruit from 60 different tree species out of 330 possible species in the forest (18.2%).  This is an underestimation of actual howler monkey contribution to seed dispersal, because the researchers observed the monkeys for a relatively brief time, and fruit consumption by the monkeys should increase over time as the population of monkeys (and possibly tree diversity), continues to increase.

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Male howler monkey released in 2016.  Note the radio transmitter on its right rear leg. Credit: L. Genes.

The second question is whether secondary dispersal by dung beetles was reestablished following reintroduction of howler monkeys.  To answer this question quantitatively, Genes and her colleagues set up an experiment that used plastic beads of various sizes instead of seeds. The researchers set up circular plots of 1m diameter with 70 grams of howler monkey poop in the middle.  Each pile was mixed with seeds (actually beads) of four different sizes (3, 6, 10 and 14 mm diameters) to mimic the range of seed sizes. The researchers measured secondary seed dispersal by returning 24 hours later and counting the remaining beads, reasoning that the rest had been moved by dung beetles (along with the poop) to a new location.

Genes and her colleagues discovered that the median rate of seed dispersal (bead removal) was 69% with larger seeds being moved at a significantly lower rate than smaller seeds.  Thus secondary seed dispersal by dung beetles was still operating in this ecosystem even after howler monkeys had been absent for over 100 years.

GenesdFig2

Removal rate of beads (seed mimics) from dung piles by dung beetles in relation to bead size.  Different letters above treatments indicate statistically significant differences between treatments. 

Overall, ecological interactions among howler monkeys, plants, and dung beetles were rapidly reestablished once howler monkeys were reintroduced to the community.  There are plans to introduce five more howler monkeys this year, which should further increase beneficial seed dispersal, and hopefully allow plant diversity to increase as well.  One problematic observation was that howler monkeys also ate invasive jackfruit, which could promote its dispersal within the community.

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Luisa Genes monitors howler monkeys in the forest. Despite its apparent lushness, the forest still lacks many species and interactions that you would expect to find in an intact forest. Credit: L. Candisani.

The researchers discovered only 21 species of dung beetles, which was somewhat lower than other studies have found.  It is probable that conversion of this land into farmland in the 19thcentury led to the decline and/or demise of some dung beetle species.  With reintroduction of howler monkeys, and the passage of time, Genes and her colleagues expect that this rewilding effort should lead to a more robust ecosystem, with increased howler monkey populations supporting high dung beetle abundance and diversity, and more effective dispersal of many plant species. To understand the overall impact on forests, the researchers recommend that future studies should compare seedling survival and forest regeneration in areas where howler monkeys were reintroduced to areas where howler monkeys are still missing.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Genes, L. , Fernandez, F. A., Vaz‐de‐Mello, F. Z., da Rosa, P. , Fernandez, E. and Pires, A. S. (2019), Effects of howler monkey reintroduction on ecological interactions and processes. Conservation Biology, 33: 88-98. doi:10.1111/cobi.13188. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2019 by the Society for Conservation Biology. All rights reserved.

Coral can recover (occasionally)

Coral reefs have amazing species diversity, which depends, in part, on a mutualism between the coral animal and a group of symbiotic algae that live inside the coral. The algae provide the coral host with approximately 90% of the energy it needs (from photosynthetic product).  In return, the algae are rewarded with a place to live and a generous allotment of nitrogen (mostly fecal matter) from the coral.  Unfortunately, coral are under attack from a variety of sources. Most problematic, humans are releasing massive amounts of carbon dioxide into the atmosphere, which is increasing ocean temperatures and also making the ocean more acidic.  Both processes can kill coral by causing coral to eject their symbiotic algae, making it impossible for the coral to get enough nutrients.

Moorea Coral Reef LTER site

The coral reef at Mo’orea. Credit: Moorea Coral Reef LTER site.

But other factors threaten coral ecosystems as well. For example, the reefs of Mo’orea , French Polynesia (pictured above), were attacked by the voracious seastar, Acanthaster planci, between 2006-2010, which reduced the coral cover (the % of the ocean floor that is covered with coral when viewed from above) from 45.8% in 2006 to 6.4% in 2009.  Then, in Feb 2010, Cyclone Oli hit, and by April, mean coral cover had plummeted down to 0.4%.

Moorea swimmers

Researchers survey the reef at Mo’orea. Credit: Peter Edmunds.

Peter Edmunds has been studying the coral reef ecosystem at Mo’orea for 14 years, and has observed firsthand the sequence of reef death, and the subsequent recovery.  Working with Hannah Nelson and Lorenzo Bramanti, he wanted to document the recovery process, and to identify the underlying mechanisms.  Fortunately Mo’orea is a Long Term Ecological Research (LTER) site, one of 28 such sites funded by the United States National Science Foundation.  Consequently the researchers had long term data available to them, so they could document how coral abundance had changed since 2005.  Their analysis showed the decline in coral cover from 2007 to 2010, but a remarkable rapid recovery beginning in 2012 and continuing through 2017.

EdmundsFig1

% cover (+ SE) of all coral , Pocillopora coral (the species group that the research team focused on). and macroalgae at Mo’orea over a 13 year period based on LTER data. The horizontal bar with COTs above it represents the time period of maximum seastar predation.

What factors caused this sharp recovery? One general process that could be part of the answer is density dependence, whereby populations have high growth rates when densities are low and there is very little competition, and low growth rates when densities are high and there is a great deal of competition between individuals, or in this case, between colonies. The problem is that though density dependence makes intuitive sense, it is difficult to demonstrate, as other factors could underlie the coral recovery.  Perhaps after 2011 there was more food available, or fewer predators, or maybe the weather was better for coral growth.

EdmundsQuadrats

High density (top) and low density (bottom) quadrats of Pocillopora coral established by the research group.

To more convincingly test for density dependence, Edmunds and his colleagues set up an experiment, establishing 18 1m2 quadrats in April, 2016. The researchers reduced coral cover in nine quadrats to 19.1% by removing seven or eight colonies from each experimental quadrat (low density quadrats), and left the other nine quadrats as unmanipulated controls, with coral cover averaging 32.5% (high density quadrats).  They then asked if, over the course of the next year, more recruits (new colonies < 4cm diameter) became established in the low density quadrats.

Returning in 2017, the researchers discovered substantially greater recruitment in the low density quadrats than in the high density quadrats. This experiment provides strong evidence that the rapid recovery after devastation by seastars and Cyclone Oli was helped by a density dependent response of the coral population – high recruitment at low population density.

EdmundsFig3

Density of recruits just after (left), and one year after (right) the quadrats were established. Solid bars are means (+ SE) for high density quadrats, while clear bars are means (+ SE) for low density quadrats.

In recent years, many coral reef systems around the world have experienced declining coral cover, a loss of fish and invertebrate diversity and abundance, and an increase in abundance of macroalgae.  While many of these reefs continue to decline, others, such as the reefs at the Mo’orea LTER site, are more resilient, and are able to recover from disturbance.  The researchers argue that we need to fully understand the mechanisms underlying recovery – in other words what is causing the density dependent response? Is it simply competition between coral that cause high recruitment under low density, or may interactions between coral and algae be important?  And what types of interactions influence recruitment rates under different densities?  One possibility is that at high densities, coral are eating most of the tiny coral larvae as they descend from the surface after a mass spawning event.  This raises the important question of why many reefs around the world do not show this density dependent response.  Clearly there is much work remaining to be done if we want to preserve this critically endangered marine biome.

note: the paper that describes this research is from the journal Ecology. The reference is Edmunds, P. J., Nelson, H. R. and Bramanti, L. (2018), Density‐dependence mediates coral assemblage structure. Ecology, 99: 2605-2613. doi:10.1002/ecy.2511. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Meandering meerkats

Dispersal – the movement of individuals to a new location – is a complex process that ecologists divide into three stages: emigration (leaving the group), transience through an unfamiliar landscape, and settlement in a suitable habitat. Dispersal is fraught with danger, as dispersers usually have a higher chance of starving, of getting eaten by predators, and may suffer a low reproductive rate.  So why move?

The problem is that there are major issues with not moving.  First, if nobody disperses, population densities could increase alarmingly, putting strains on resources and increasing the incidence of disease transmission.  Second, if nobody disperses, close relatives would tend to live near each other.  If these relatives mate, there would be a high probability of bad combinations of genes being expressed, leading to developmental abnormalities or high offspring mortality (geneticists call this inbreeding depression). In social species, such as meerkats, Suricata suricatta, the issues are even more complex, as dispersal could break up social groups that work well together to detect predators or find resources.  Nino Maag and his colleagues explored what factors influence meerkat dispersal decisions, their survival and reproduction, and how those factors affected overall population dynamics in the Kuruman River Reserve in South Africa.

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A group of vigilant meerkats. Credit: Arpat Azgul

Meerkats live in groups of 2-50 individuals, with a dominant pair that monopolizes reproduction.  While pregnant, the dominant female usually evicts some subordinate females from the group; this coalition of evictees will either remain apart from the group (but within the confines of the territory) and eventually be allowed back in, or else emigrate to a new territory. By attaching radio collars to subordinate females, the researchers were able to follow emigrants to determine their fates.

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Nino Maag collects data in the Kalahari Desert while a meerkat, wearing a radio collar, strolls by. Credit: Gabriele Cozzi.

How does population density affect emigration rates of evicted females?  You might think that meerkats would be most likely to emigrate at high population density, as a way of avoiding resource competition.  As it turns out the story is more complicated.  First, individual females (solid lines in graph below) are more likely to remain with the group (not emigrate) than are groups of two or more females (dashed lines). Second, emigration rates were highest at low population density, intermediate at high population density and lowest at intermediate population density. This nonlinear effect can be explained by low benefits of remaining in a very small group, so evictees are more likely to emigrate.  But as population density (and group size) increase, then the meerkats enjoy higher success as a result of cooperation between individuals  (in particular, detecting and avoiding predators).  But when population densities get too high, there are not enough resources to go around, and evictees are more likely to emigrate.

MaagFig2A

Proportion of evicted female meerkats that had not yet emigrated in relation to time since eviction at low (red), medium (light blue) and high (dark blue) population density.  Solid lines represent individual females, while dashed lines are coalitions of two or more females.

In addition to the density effects we just discussed, association with unrelated males from other groups early after eviction increased the probability that females would emigrate – presumably this increased the probability females would quickly create offspring in their new territory. Females also dispersed longer distances if unrelated males did not meet up with them, possibly to avoid inbreeding with closely-related males from neighboring groups.

Coalitions were more likely to return to the group if females were not pregnant – in fact 62% of pregnant evictees aborted their litters before being allowed back into the group.  Of the ones that did not abort before returning, only 42% of their litters survived to the first month.

The period of transience, when emigrators are seeking new territories can be prolonged and dangerous.  The mean dispersal distance was 2.24 km, and averaged about 46 days.  Larger coalitions with males present tended to disperse the shortest distances (left graph below). Dispersers took longest to settle at high population density – perhaps there were fewer available territories under those conditions (right graph below).

MaagFig4

A. Effect of coalition size and presence of unrelated males on dispersal distance. B. Effect of population density on transience time (interval between emigration and settling).

Large coalitions settled more quickly than did small coalitions, particularly if accompanied by unrelated males.  Once settled, females successfully carried through 89% of their pregnancies (compare that to the 62% abortion rate of females that returned to their original group).  These females had a litter survival rate (to the first month) of 65%.

Social and non-social species are influenced by population density in different ways.  The situation is relatively simple for non-social species; as population size increases, competition between individuals increases, so dispersal is more likely.  However, even for non-social species, we might expect dispersal at very low population levels, if there are no mates available. For social species such as meerkats, the situation is more complex.  Cooperation enhances survival and reproduction, so it is better to be in a larger group (with more cooperators). At the same time, if the group is too large, then resource competition starts being an increasingly disruptive factor. As ecologists collect more dispersal data from other social species, they will be able to test the hypothesis that population density in many species influences dispersal in a non-linear way.

note: the paper that describes this research is from the journal Ecology. The reference is Maag, N. , Cozzi, G. , Clutton‐Brock, T. and Ozgul, A. (2018), Density‐dependent dispersal strategies in a cooperative breeder. Ecology, 99: 1932-1941. doi:10.1002/ecy.2433. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Climate changes a bird’s life in shrinking grasslands

Back in graduate school, a couple of my grad student buddies and I would get together to fish for brown trout in the Kinnickinnic River in western Wisconsin.  We were students at the University of Minnesota (Twin Cities), but the Kinni was the closest trout stream.  Tired of catching small brown trout, we consulted a trout fishing map and discovered that the headwaters of the Kinni were rich in brook trout. So early one morning, map in hand, we followed strange paths and found our sacred brook trout haven. Alas, the only thing it was rich in was corn, now about two feet high – though there was a modest depression where trout waters once had flowed. Our personal depression was perhaps more than modest – having been robbed of brook trout, and the opportunity to experience some pristine waters flowing through a beautiful grassland.

Grasslands, one of the biomes native to parts of Wisconsin and Minnesota, are globally one of the most endangered biomes, because they usually are relatively easy to convert into farmland and suburban developments. Native grasslands harbor a wide biological diversity; consequently conservation biologists are concerned about their continued loss.

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Cool-season grassland in southwest Wisconsin. Credit: John Dadisman.

Ben Zuckerberg, Christine Ribic and Lisa McCauley wanted to know how environmental factors influenced the nesting success of grassland birds, in particular, because as obligate ground nesters, they might be susceptible to changing  weather conditions that will be affecting the climate in coming decades.  A nest built on the ground is much less insulated from the environment than one built in or on a tree or even a ledge.

Bobolink 7 days (Carolyn Byers)

Seven day old bobolink chicks in a ground nest. Credit: Carolyn Byers.

Zuckerberg and his colleagues used Google Scholar and the ISI Web of Science to comb the literature (1982-2015) for studies that explored the nest success of obligate grassland birds in the United States. They identified 12 bird species from 81 individual studies of 21,000 nests. Based on their experience and the literature, both precipitation and temperature were likely to influence nest success, which is the proportion of nests that fledge at least one young. They considered three precipitation time periods: (1) Bioyear – previous July through April of the breeding season, (2) May of the breeding season, (3) June – August of the breeding season. They considered breeding season temperatures during May, and during the period from June-August. The researchers were also interested in the size of the grassland (grassland patch size), reasoning that a larger grassland might provide more diverse microclimates, so, for example, a bird might be able to find a dry microhabitat for nesting in a large grassland, even in a wet breeding season.

ZuckFig1

Map of the identity and location of species considered for this study.

The researchers discovered that both temperature and precipitation were important.  Nest success increased steadily with bioyear precipitation (Figure (a) below).  Presumably, more rain led to more plant growth and more insect survival, which would help feed the young.  Taller plants could also help shade or hide the nests. In contrast, nest success declined sharply with precipitation during spring and summer of the breeding season (Figure (b) and (c)). Heavy rains during the breeding season can flood nests, and also decrease the foraging efficiency of parents who might need to spend more time incubating nests during rainstorms. Lastly, extreme (low or high) May temperatures depressed nest success, which was highest at intermediate temperatures (Figure (d)). Egg viability depends on maintaining a constant temperature, and the parents may be more challenged to thermoregulate at extreme temperatures.  Temperatures later in the breeding season did not affect nest success.

ZuckFig2

Effects of (a) bioyear precipitation (previous July – April of the breeding season), (b) May precipitation during the breeding season, (c) June – August precipitation during the breeding season, and (d) May temperature on nest success. Shaded area represents 95% confidence interval.

But all is not straightforward in the grassland nest success world. These main findings about precipitation and temperature interacted with grassland size in interesting ways.  For example high bioyear precipitation, which overall increased nest success, only did so for smaller grassland patches (dashed line in top graph below), but not for larger patches (solid line).  Extreme May temperatures had different effects on nest success in relation to grassland patch size.  Low May temperatures were associated with high nest success in small patches (dashed line in bottom graph) and with low nest success in large patches (solid line).  High May temperatures were associated with high nest success in large patches, and with low nest success in small patches.

ZuckFig3

Predicted nest success of grassland birds in relation to bioyear precipitation (top graph) and May temperature (bottom graph) in relation to grassland patch size.  Solid lines represent large grasslands, while dashed lines represent small grasslands.  Shaded area is 95% confidence interval.

The researchers were surprised to discover that patch size affected how weather influenced grassland bird nesting success. Some of the patterns seem intuitively logical; for example, in unusually hot breeding seasons birds had higher nest success in larger grasslands than in smaller grasslands.  Presumably, birds were more likely to find a cooler microclimate for their nests in a large grassland.  However it is puzzling why in unusually cold breeding seasons birds had higher nest success in smaller grasslands. The researchers are planning a follow-up study to better document and measure the existence of microclimates in grasslands of different sizes, and explore how different microclimates influence the nesting success of vulnerable grassland birds.  Finding that warmer temperatures and drought generally reduce nest success to the greatest extent in small grassland patches is strong incentive for conservation mangers to establish large core grasslands as a tool to maintain bird populations in the wake of present and future changes to the climate.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Zuckerberg, B. , Ribic, C. A. and McCauley, L. A. (2018), Effects of temperature and precipitation on grassland bird nesting success as mediated by patch size. Conservation Biology, 32: 872-882. doi:10.1111/cobi.13089. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. All rights reserved.

 

Recruiting rhinoceros

Despite their immense size and unfriendly disposition, we humans have done an excellent job decimating the black rhinoceros (Diceros bicornis) population from several hundred thousand individuals around 1900 to fewer than 3000 individuals by 1990. Three subspecies are extinct, one is on the brink, while even the most successful remaining subspecies, the south-central black rhinoceros, is extinct over much of its former range, or only found in nature reserves.  Humans prize its horns, which historically were used for making wine cups, ceremonial daggers, and a variety of medicines that purportedly revive comatose patients, detoxify infections, and aid male sexual stamina. Trade of rhinoceros horn has been illegal since 1977, but poaching abounds.

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Rhinoceros horn products seized by the Hong Kong Government. Credit: U.S. Government Accountability Office from Washington, DC, United States [Public domain], via Wikimedia Commons

This population crisis has motivated conservation ecologists to evaluate the best approaches to conserving the black rhinoceros, and to restoring it to parts of its former range. Translocation, moving rhinoceroses from one location where they are relatively well-established, to another where they are extinct or at very low numbers, is a viable approach to restoring populations. However, translocation did not always work well, as some rhinoceroses died following translocation, or failed to reproduce even if they survived translocation. While a post-doctoral researcher at the Zoological Society in San Diego, California, Wayne Linklater recognized that there were large datasets collected by government and non-government agencies that might answer the question about what drives better rhinoceros survival and breeding.  Unfortunately some of these datasets were difficult to access or interpret, but Jay Gedir, Linklater and several other colleagues persevered and combed through the data to identify the factors associated with successful translocation.

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Black rhino is airlifted to temporary captivity before being translocated to a release site. Credit: Andrew Stringer

Many translocation studies use a short-term measure of success, such as survival or fecundity (fertility) of the translocated individuals.  The researchers reasoned that the most important measure, when it is available, is the number of offspring produced by translocated females that survive to an age that they too can reproduce, which in the case of rhinoceros is four years. Based on existing long-term studies, Gedir, Linklater and their colleagues compiled the offspring recruitment rate (ORR), which combines the variables of survival, fecundity, and offspring survival to sexual maturity. They found that ORR was greatest when mature females were translocated into a population that had a female-biased sex ratio.

conbiofig1

Offspring recruitment rate (per year) in relation to age at release and sex ratio bias of the recipient population. Female bias is greater than 60% female, male bias is greater than 60% male. Numbers above graph are sample size for each category. Error bars are 95% confidence intervals.

So why does sex-ratio matter?  The researchers are not certain, but females are subjected to considerable sexual harassment by very aggressive males, so a female-biased sex ratio may lead to less harassment and improved survival and reproductive success for translocated females.

Translocated juveniles took longer to produce their first calf after reaching sexual maturity than did adults after being released. Again this effect was stronger with a male-biased sex ratio.

conbiofig2a

Mean time (years) to produce their first calf after reaching sexual maturity for juveniles, or after release for adults.

Many females (47%) produced no surviving offspring. This pattern of recruitment failure was most common in juveniles, and least common in adults translocated into populations with a female-biased sex ratio.

conbiofig2b

Recruitment failure of translocated females in relation to age at release and sex ratio bias of the recipient population.

Several factors can cause recruitment failure: 23% of females died following translocation and 24% of surviving females never produced calves. However, calf survival to sexual maturity was a robust 89%, and this survival rate was independent of age at translocation or population sex ratio. Among surviving translocated females, juveniles were about twice as likely as young or old adults to fail to produce a calf, but were equally successful at raising the calves they were able to produce.

Linklater was surprised at how important sex ratios (and presumably social relationships) were, particularly given that black rhinoceroses spend much of their time alone or with one offspring.

Neto and Gwala size each other up

Neto (the ranger) and Gwala (the rhino) size each other up.  Credit: Wayne Linklater.

The study did not support a major role for many other factors that had previously been considered important in translocation success, such as habitat quality, population density, number of rhinoceroses released and reserve size. Based on their analysis, the researchers recommend that conservation biologists should translocate mature females into populations with female-biased sex ratios to reduce rates of recruitment failure.  If juveniles must be translocated, they too should be moved into populations that already have a female-biased sex ratio to reduce levels of sexual harassment by males after they mature.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Gedir, J. V., Law, P. R., du Preez, P., & Linklater, W. L. (2018). Effects of age and sex ratios on offspring recruitment rates in translocated black rhinoceros. Conservation Biology32(3), 628-637. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. All rights reserved.

Homing in on the micro range

I’ve always been fascinated by geography. As a child, I memorized the heights of mountains, the populations of cities, and the areas encompassed by various states and countries. I can still recite from memory many of these numbers – at least based on the 1960 Rand McNally World Atlas. Part of my fondness for geography is no doubt based on my brain’s ability to recall numbers but very little else.

Most geographic ecologists are fond of numbers, exploring numerical questions such as how many organisms or species are there in a given area, or how large an area does a particular species occupy? They then look for factors that influence the distribution and abundance of species or groups of species. Given that biologists estimate there may be up to 100 million species, geographic ecologists have their work cut out for them.

As it turns out, most geographic ecologists have worked on plants, animals or fungi, while relatively few have worked on bacteria and archaeans (a very diverse group of microorganisms that is ancestral to eukaryotes).

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Two petri plates with pigmented Actinobacteria. Credit: Mallory Choudoir.

Until recently, bacteria and archaeans were challenging subjects because they were so small and difficult to tell apart. But now, molecular/microbial biology techniques allow us to distinguish between closely related bacteria based on the sequence of bases (adenine, cytosine, guanine, and uracil) in their ribosomal RNA. Bacteria which are identical in more than 97% of their base sequence are described as being in the same phylotype, which is roughly analogous to being in the same species.

As a postdoctoral researcher working in Noah Fierer’s laboratory with several other researchers, Mallory Choudoir wanted to understand the geographic ecology of microorganisms. To do so, they and their collaborators collected dust samples from the trim above an exterior door at 1065 locations across the United States (USA).

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Dr. Val McKenzie collects a dust sample from the top of a door sill. Credit: Dr. Noah Fierer.

The researchers sequenced the ribosomal RNA from each sample to determine the bacterial and archaeal diversity at each location. Overall they identified 74,134 gene sequence phyloypes in these samples – that took some work.

On average, each phylotype was found at 70 sites across the USA, but there was enormous variation. By mapping the phylotypes at each of the 1065 locations, the researchers were able to estimate the range size of each phylotyope. They discovered a highly skewed distribution of range sizes, with most phylotypes having relatively small ranges, while only a very few had large ranges (see the graph below). As it turns out, we observe this pattern when analyzing range sizes of plant and animal species as well.

Choudoir1C

Mean geographic range (Area of occupancy) for each phylotype in the study.  The y-axis (Density) indicates the probability that a given phylotype will occupy a range of a particular size (if you draw a straight line down from the peak to the x-axis, you will note that most phylotypes had an AOO of less than 3000 km2

Taxonomists use the term phylum (plural phyla) to indicate a broad grouping of similar organisms. Just to give you a feel for how broad a phylum is, humans and fish belong to the same phylum. Some microbial phyla had much larger geographic ranges than others. Interestingly, it was not always the case that the phylum with the greatest phylotype diversity had the largest range. For example, phylum Chrenarchaeota had the greatest median geographic range (see the graph below), but ranked only 19 (out of 50 phyla) in number of phylotypes (remember that a phylotype is kind of like a species in this study).

Choudoir3

Box plots showing range size distribution for individual phyla. Middle black line within each box is the median value; box edges are the 25th and 75th percentile values (1st and 3rd quartiles).  Points are outlier phylotypes. Notice that the y-axis is logarithmic.

With this background, Choudoir and her colleagues were prepared to investigate whether there were any characteristics that might influence how large a range would be occupied by a particular phylotype. We could imagine, for example, that a phylotype able to withstand different types of environments would have a greater geographic range than a phylotype that was limited to living in thermal pools. Similarly, a phylotype that dispersed very effectively might have a greater geographic range than a poor disperser.

The researchers expected that aerobic microorganisms (that use oxygen for their metabolism) would have larger geographic ranges than nonaerobic microorganisms, which are actually poisoned by oxygen. The data below support this prediction quite nicely.

Choudoir4a

Geographic range size in relation to oxygen tolerance.  In this graph, and the graphs below, the points have been jittered to the right and left of their bar for ease of viewing (otherwise even more of the points would be on top of each other).

Some bacterial species form spores that protect them against unfavorable environmental conditions. The researchers expected that spore-forming bacteria would have larger geographic ranges than non-spore-forming bacteria.

Choudoir4BC

Geographic range in relation to spore formation (left graph) and pigmentation (right graph).

Choudoir and her colleagues were surprised to discover exactly the opposite; the spore forming bacteria had, on average, slightly smaller geographic ranges. Choudoir and her colleagues also expected that phylotypes that are protected from harsh UV radiation by pigmentation would have larger geographic ranges than unpigmented phylotypes – this time the data confirmed their expectations.

The researchers identified several other factors associated with range size. For example, bacteria with more guanine and cytosine in their DNA or RNA tend to have larger geographic ranges. Some previous studies have shown that a higher proportion of guanine and cytosine is associated with greater thermal tolerance, which should translate to a greater geographic range. Choudoir and her colleagues also discovered that microorganisms with larger genomes (longer DNA or RNA sequences) also had larger ranges. They reason that larger genomes (thus more genes) should correspond to greater physiological versatility and the ability to survive variable environments.

This study opens up the door to further studies of microbial geographic ecology. Some patterns were expected, while others were surprising and beg for more research. Many of these microorganisms are important medically, ecologically or agriculturally, so there are very good reasons to figure out why they live where they do, and how they get from one place to another.

note: the paper that describes this research is from the journal Ecology. The reference is Choudoir, M. J., Barberán, A., Menninger, H. L., Dunn, R. R. and Fierer, N. (2018), Variation in range size and dispersal capabilities of microbial taxa. Ecology, 99: 322–334. doi:10.1002/ecy.2094. 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.

“Notes from Underground” – cicadas as living rain gauges

Given recent discussions between Donald Trump and Kim Jong-un about whose button is bigger, many of us with entomological leanings have revisited the question of what insects are most likely to dominate a post-nuclear world. Cicadas have a developmental life history that predisposes them to survival in the long term because some species in the eastern United States spend many subterranean years as juveniles (nymphs), feeding on the xylem sap within plants’ root systems. Magicicada nymphs live underground for 13 or 17 years, depending on the species, before digging out en masse, undergoing one final molt, and then going about the adult business of reproduction. This life history of spending many years underground followed by a mass emergence has not evolved to avoid nuclear holocausts while underground, but rather to synchronize emergence of billions of animals. Mass emergence causes predator satiation, an anti-predator adaptation in which predators are gastronomically overwhelmed by the number of prey items, so even if they eat only cicadas and nothing else, they still are able to consume only a small fraction of the cicada population.

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Mass Magicicada emergence picturing recently-emerged winged adults, and the smaller lighter-colored exuviae (exoskeletons) that are shed during emergence. Credit: Arthur D. Guilani.

Less well-known are the protoperiodical cicadas (subfamily Tettigadinae) of the western United States that are abundant in some years, and may be entirely absent in others. Jeffrey Cole has studied cicada courtship songs for many years, and during his 2003 field season noted that localities that had previously been devoid of cicadas now (in 2003) hosted huge numbers of six or seven different species. He returned to those sites every year and high diversity and abundance reappeared in 2008 and 2014. This flexible periodicity contrasted with their eastern Magicicada cousins, and he wanted to know what stimulated mass emergence.

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Protoperiodical cicadas studied by Chatfield-Taylor and Cole.  Okanagana cruentifera (top) and Clidophleps wrighti (bottom). Credit Jeffrey A. Cole.

Cole and his graduate student, Will Chatfield-Taylor, considered two hypotheses that might explain protoperiodicity in southern California (where they focused their efforts). The first hypothesis is that cicada emergence is triggered by heavy rains generated by El Niño Southern Oscillation (ENSO), a large-scale atmospheric system characterized by high sea temperature and low barometric pressure over the eastern Pacific Ocean. ENSO has a variable periodicity of 4.9 years, which roughly corresponds to the timing Cole observed while doing fieldwork. The second hypothesis recognized that nymphs must accumulate a set amount of xylem sap from their host plants to complete development. Sap availability depends on precipitation, and this accumulation takes several years in arid habitats. So while ENSO may hasten the process, the key to emergence is a threshold amount of precipitation over a several year timespan.

Working together, the researchers were able to identify seven protoperiodical species by downloading museum specimen data (including where and when each individual was collected) from two databases (iDigBio and SCAN). They also used data from several large museum collections, which gave them evidence of protoperiodical cicada emergences back to 1909. Based on these data, Chatfield-Taylor and Cole constructed a map of where these protoperiodical cicadas emerge.

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Maps of five emergence localities discussed in this study.

The researchers tested the hypothesis that protoperiodical cicada emergences follow heavy rains triggered by ENSO by going through their dataset to see if there was a correlation between ENSO years and mass cicada emergences. Of 20 mass cicada emergences since 1918, only five coincided with ENSO events, which is approximately what would be expected with a random association between mass emergences and ENSO. Scratch hypothesis 1.

Let’s look at the second hypothesis. The researchers needed reliable precipitation data between years for which they had good evidence that there were mass emergences of their seven species. Using a statistical model, they discovered that 1181 mm was a threshold for mass emergences, and that three years was the minimum emergence interval regardless of precipitation. Only after 1181 mm of rain fell since the last mass emergence, summed over at least three years, would a new mass emergence be triggered.

ColeFig2

Cumulative precipitation over seven time periods preceding cicada emergence.

The nice feature of this model is that it makes predictions about the future. For example, the last emergence occurred in the Devil’s punchbowl vicinity in 2014. Since then that area has averaged 182.2 mm of precipitation per year. If those drought conditions continue, the next mass emergence will occur in 2021 at that locality, which is longer than its historical average. Only time will tell. Hopefully Mr. Trump and Mr. Jong-un will be able to keep their fingers off of their respective buttons until then.

note: the paper that describes this research is from the journal Ecology. The reference is Chatfield-Taylor, W. and Cole, J. A. (2017), Living rain gauges: cumulative precipitation explains the emergence schedules of California protoperiodical cicadas. Ecology, 98: 2521–2527. doi:10.1002/ecy.1980. 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.