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.

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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.

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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.

Rice fields foster biodiversity

Restoration ecologists want to restore ecosystems that have been damaged or destroyed by human activity.  One approach they use is “rewilding” – which can mean different things to different people.  To some, rewilding involves returning large predators to an ecosystem, thereby reestablishing important ecological linkages.  To others, rewilding requires corridors that link different wild areas, so animals can migrate from one area to another.  One common thread in most concepts of rewilding is that once established, restored ecosystems should be self-sustaining, so that if ecosystems are left to their own devices, ecological linkages and biological diversity can return to pre-human-intervention levels, and remain at those levels in the future.

ardea intermedia (intermediate egret). photo by n. katayama

The intermediate egrit, Ardea intermedia, plucks a fish from a flooded rice field. Credit: N. Katayama.

Chieko Koshida and Naoki Katayama argue that rewilding may not always increase biological diversity.  In some cases, allowing ecosystems to return to their pre-human-intervention state can actually cause biological diversity to decline. Koshida and Katayama were surveying bird diversity in abandoned rice fields, and noticed that bird species distributions were different in long-abandoned rice fields in comparison to still-functioning rice fields.  To follow up on their observations, they surveyed the literature, and found 172 studies that addressed how rice field abandonment in Japan affected species richness (number of species) or abundance.  For the meta-analysis we will be discussing today, an eligible study needed to compare richness and/or abundance for at least two of three management states: (1) cultivated (tilled, flood irrigated, rice planted, and harvested every year), (2) fallow (tilled or mowed once every 1-3 years), and (3) long-abandoned (unmanaged for at least three years).

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Three different rice field management states – cultivated, fallow and long-abandoned – showing differences in vegetation and water conditions. Credit: C. Koshida.

Meta-analyses are always challenging, because the data are collected by many researchers, and for a variety of purposes.  For example, some researchers may only be interested in whether invasive species were present, or they may not be interested in how many individuals of a particular species were present. Ultimately 35 studies met Koshida and Katayama’s criteria for their meta-analysis (29 in Japanese and six in English).

Overall, abandoning or fallowing rice fields decreased species richness or abundance to 72% of the value of cultivated rice fields. As you might suspect, these effects were not uniform for different variables or comparisons. Not surprisingly, fish and amphibians declined sharply in abandoned rice fields – much more than other groups of organisms. Abundance declined more sharply in abandoned fields than did species richness.  Several other trends also emerged.  For example, complex landscapes such as yatsuda (forested valleys) and tanada (hilly terraces) were more affected than were simple landscapes.  In addition, wetter abandoned fields were able to maintain biological diversity, while dryer abandoned fields declined in richness and abundance.

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The effects of rice field abandonment or fallowing for eight different variables.  Effect size is the ln (Mt/Mc), where Mt = mean species richness or abundance for the treatment, and Mc = mean species richness for the control.  The treated field in all comparisons was the one that was abandoned for the longer time.  A positive effect size means that species richness or abundance  increased in the treated (longer abandoned) field, while a negative effect size means that species richness or abundance declined in the treated field. Numbers in parentheses are number of data sets used for comparisons.

When numerous variables are considered, researchers need to figure out which are most important.  Koshida and Katayama used a statistical approach known as “random forest” to model the impact of different variables on the reduction in biological diversity following abandonment.  This approach generates a variable – the percentage increase in mean square error (%increaseMSE) – which indicates the importance of each variable for the model (we won’t go into how this is done!).  As the graph below shows, soil moisture was the most important variable, which tells us (along with the previous figure above) that abandoned fields that maintained high moisture levels also kept their biological diversity, while those that dried out lost out considerably.  Management state was the second most important variable, as long-abandoned fields lost considerably more biological diversity than did fallow fields.

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Importance estimates of each variable (as measured by %increase MSE).  Higher values indicate greater importance.

Unfortunately, only three studies had data on changes in biological diversity over the long-term.  All three of these studies surveyed plant species richness over a 6 – 15 year period, so Koshida and Katayama combined them to explore whether plant species richness recovers following long-term rice field abandonment. Based on these studies, species richness continues to decline over the entire time period.

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Plant species richness in relation to time since rice fields were abandoned (based on three studies).

Koshida and Katayama conclude that left to their own devices, some ecosystems, like rice fields, will actually decrease, rather than increase, in biological diversity.  Rice fields are, however, special cases, because they provide alternatives to natural wetlands for many organisms dependent on aquatic/wetland environments (such as the frog below). In this sense, rice fields should be viewed as ecological refuges for these groups of organisms.

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Rana porosa porosa (Tokyo Daruma Pond Frog). Credit: Y. G. Baba

These findings also have important management implications.  For example, conservation ecologists can promote biological diversity in abandoned rice fields by mowing and flooding. In addition, managers should pay particular attention to abandoned rice fields with complex structure, as they are particularly good reservoirs of biological diversity, and are likely to lose species if allowed to dry out. Failure to attend to these issues could lead to local extinctions of specialist wetland species and of terrestrial species that live in grasslands surrounding rice fields. Lastly, restoration ecologists working on other types of ecosystems need to carefully consider the effects on biological diversity of allowing those ecosystems to return to their natural state without any human intervention.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Koshida, C. and Katayama, N. (2018), Meta‐analysis of the effects of rice‐field abandonment on biodiversity in Japan. Conservation Biology, 32: 1392-1402. doi:10.1111/cobi.13156. 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.