Parrotfish put on their big boy pants

While it would be awesome if parrotfish were named for their conversational abilities, it turns out that they earn their moniker for their specialized teeth that are fused together for scraping algae from coral, thus resembling a parrot’s beak. Despite lacking verbal skills these fish are incredible. Approximately 100 species occupy reefs, rocky coastlines and eelgrass meadows in tropical and subtropical waters. Many species are sequential hermaphrodites, beginning life as females and then changing into males after reaching a certain size. While female reproductive success is limited by the number of eggs she can produce, male reproductive success can be much higher if he can fertilize the eggs of many females.  So if a parrotfish transitions into a large male, and can control access to numerous females, he will enjoy greater reproductive success than if he had remained a female.

C. spilurusBrettTaylor

Two Chlorurus spilurus parrotfish show off their teeth and colors.  The large colorful fish on the right is a male, while the smaller darker fish to his left is a female. Credit: Brett Taylor.

Phenotypic plasticity describes the ability of an individual with a particular genetic makeup to vary in a variety of traits (such as what it looks like, or how it behaves) in response to different environmental conditions. About 15 years ago, Nick Gust’s PhD research on tropical reef fish revealed that tremendous variation in parrotfish traits existed over a distance of a few kilometers. But what causes this variation? When funding became available, Brett Taylor jumped at the opportunity to pinpoint the causes, focusing on the diverse parrotfish community in the Great Barrier Reef (GBR).


Eastern slope of the Great Barrier Reef hosts a diversity of fish and coral species. Credit: Brett Taylor.

Taylor and his colleagues surveyed 82 sites within 31 reefs across 6 degrees of latitude in the northern GBR. To standardize data collection, divers, armed with a multitude of cameras and GPS devices, swam at a standardized rate (about 20 meters/minute) for 40 minutes per survey, recording each parrotfish along a 5 m wide swath. They collected data about the habitat and the environment, about the physical traits of each individual parrotfish (such as size and sex), and about the type and abundance of parrotfish and their predators present at each site.


Researcher takes notes while conducting a dive.  Credit Kendra Taylor.

The researchers wanted to identify what factors influenced growth rate, maximum body size, and the size at sex change, and how these factors related to the parrotfish mating system. Four species of parrotfish were sufficiently abundant across the GBR to allow researchers to do this type of analysis.


Four parrotfish species  abundant along exposed outer shelf (yellow sites) and protected inner shelf (blue) regions of the Great Barrier Reef. Males are larger and more colorful.

The GBR varies structurally across a relatively small spatial scale of 40 – 100 km, with outer shelf regions (eastern) exposed to wave action, and inner shelf regions (western) relatively protected. All four species tended to change sex at a larger size in protected sites than they did at exposed sites. However, the differences are only compelling for two of the species: C. spilurus and S. frenatus. There were fewer data points for the other two species, so it is possible (but unknown) that they too would show a more pronounced trend if more data were available.


Proportion terminal phase (sex-changed males) in relation to body size (measured to the fork of the tail) in exposed (yellow) and sheltered (blue) sites.

Not surprisingly, parrotfish grew larger in protected areas. Presumably, less wave action provided a more benign environment for rapid growth, both of parrotfish and their preferred food items (algae growing on rocks and coral).


Standardized maximum size (Lmax) attained by parrotfish in sheltered vs. exposed sites.

The researchers were somewhat surprised that most other factors, such as latitude, coral cover, sea surface temperature, and predator abundance, had very little effect on the size at sex change. Rather, the size at sex change appears to be strongly influenced by the local size distribution. In protected habitats, parrotfish grow large and change sex at a large size, while in exposed habitats, parrotfish are smaller, and change sex at a smaller size.

But sex is never simple. Nick Gust’s PhD research showed that C. spilurus had different patterns of sexual allocation in protected vs. exposed areas. In protected areas, the mating system is haremic, with a large male defending a territory and servicing a harem of females. In exposed areas, the mating system is mixed; there still are large territorial males with their harems, but they compete with many more small males, and group spawning is much more prevalent. Theoretically, the presence of these small males may make it less worthwhile for a female to transition into a male, and may influence the optimal size for transitioning in exposed reefs. Given that we still don’t know the mating system details of the other parrotfish in this study, it will be fascinating to see if they too show similar patterns of haremic vs. mixed mating systems in relation to habitat structure.

note: the paper that describes this research is from the journal Ecology. The reference is Taylor, B. M., Brandl, S. J., Kapur, M., Robbins, W. D., Johnson, G., Huveneers, C., Renaud, P. and Choat, J. H. (2018), Bottom-up processes mediated by social systems drive demographic traits of coral-reef fishes. Ecology 99(3): 642-651. doi:10.1002/ecy.2127. 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.

Snails grow large to fight fear

In a recent post (Jan 12), I discussed research showing that song sparrow parents reduce provisioning to their offspring when threatened by predators, ultimately reducing offspring survival rates.  But in a turnabout that highlights the natural world’s dazzling diversity, a recent study by Sarah Donelan and Geoffrey Trussell revealed a very different impact of fear on the development of snail offspring. Donelan had worked as Trussell’s laboratory technician for two years and became fascinated by the egg capsules laid by the carnivorous snail Nucella lapillus, an ecologically important species in rocky intertidal communities. Earlier work had shown that predator-induced fear reduced snail feeding and growth rates, so Donelan decided that for her PhD work she would see how predator-induced fear influenced offspring development.


Adult Nucella alongside ca. 100 egg capsules. Credit: Sarah Donelan.

The researchers recognized that the fear environment experienced by parents before or during reproduction, and by the embryos during early development, could influence growth and development of those embryos. At their research site along the Massachusetts, USA coast, the predatory green crab, Carcinus maenas, can be a source of fear for these adult and embryonic snails. Donelan and Trussell exposed snails to fear by housing separately one male and one female snail in adjacent protected perforated containers (with six blue mussels in each container to feed them) that were set within a large plastic bucket. This bucket also had a somewhat larger perforated container (the risk chamber) containing the dreaded green crab (and two snails to feed it). The control risk chamber had two snails, but no crab.


Experimental setup with buckets containing egg capsules in perforated cages experiencing different exposure to fear. Credit: Sarah Donelan.

In late spring of 2015 and 2016, field-collected female and male snails were matched to create a total of 80 parental pairs. Donelan and Trussell set up experiments to explore the effects of parental experience with predation risk, embryonic experience with predation risk, and duration of embryonic experience.

Parent snails were exposed to a risk chamber (with a crab in the experimental group, and without a crab in the control group) for three days, and then placed together for four days (without risk) to mate. If an egg capsule was laid, the researchers removed it, and immediately exposed it to an experimental or control risk chamber for a week. Embryonic risk duration was further manipulated by continuing to expose half of the egg capsules to risk for a total of six weeks. The table below summarizes the treatments received by parents and offspring.



Mean (+ standard error) shell length (top graph) and tissue mass (bottom graph) of snail embryos exposed to predation risk. Parents were either exposed (solid circles) or not exposed (open circles) to risk before mating.


When parents were not exposed to risk, but their offspring were exposed, these offspring had shorter shells and reduced tissue mass compared to all other groups. When both parents and offspring were exposed to risk, offspring shell length increased by 8% and offspring mass increased by a whopping 40% over risk-exposed offspring whose parents were not exposed to risk (left data points in figures a and b). If embryos were not exposed to risk, parental exposure had no significant impact on embryonic development (right data points on figures a and b). Embryonic risk duration had no impact on development.


In addition, risk-exposed offspring of risk-exposed parents emerged from their egg capsules an average of 4.1 days sooner than other offspring.


Mean (+standard error) number of days until emergence of snail offspring that experienced the presence or absence of predation risk during early development.  Their parents were exposed to risk (solid circle) or no risk (open circle) before mating.

What could be causing these differences in size and rate of development? Donelan and Trussell hypothesized that embryonic snails could grow larger and more quickly if they were somehow able to reduce their metabolic rate. With a reduction in metabolic rate, more energy could be diverted to growth and development, resulting in larger and faster-growing snails. The researchers used an oxygen meter to measure oxygen consumption rates of individual egg capsules (from the eight different treatments in the first experiment) six weeks after deposition, about a week before embryos would begin to emerge. They exposed some of the capsules to predation risk during the experiment (current risk graph below), and left other capsules unexposed. When tested under risky conditions, capsules from parents who were exposed to risk, and that experienced risk as embryos during early development, had 56% lower metabolic rates than the other three groups (left graph), and similarly low metabolic rates as capsules tested without risk (right graph).


Mean (+ standard error) respiration rate of egg capsules that were (left graph) or were not (right graph) exposed to current predation risk.  During early development, the embryos in these capsules experienced risk or no risk, and were produced by parents exposed to risk (solid circles) or no risk (open circles) before mating.

Overall, parental experience with predation risk enhances offspring growth and development in the presence of risk. If the parents lack this exposure, risk-exposed offspring suffer the costs associated with small size and slower development. Currently Donelan and Trussell are trying to figure out what these costs are. Smaller snails have less energy reserves, may feed on a less diverse group of prey, and are less likely to remain in safer habitats than are larger juveniles. But we still don’t know whether these effects on early stages of life have lasting impacts as a snail gets older and larger. More generally, we don’t know whether there are similar types of interactions between parental and embryonic experiences of other stressors, most notably environmental stresses that are already being imposed by climate change.

note: the paper that describes this research is from the journal Ecology. The reference is Donelan, S. C. and Trussell, G. C. (2018), Synergistic effects of parental and embryonic exposure to predation risk on prey offspring size at emergence. Ecology, 99: 68–78. doi:10.1002/ecy.2067. 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.

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).


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).


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.


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).


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 phyloype 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.


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.


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.


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.



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.


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.


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.


Predators and livestock – “stayin’ alive.”

President Donald Trump was elected on a platform that included building a great wall whose purpose was to keep out unwanted intruders from the south, and that would be paid for (apparently magically) by these same intruders.  The idea of building a great wall has been around for a long time; the Great Wall of China was constructed over a time period of almost two thousand years to keep out unwanted intruders (this time from the north). Not surprisingly, the cost of that Great Wall was not borne by the unwanted intruders. More recently, in the 1880s, the government of Australia constructed a 5500 km fence designed to keep unwanted dingoes away from sheep that pasture in southeastern Australia. As Lily van Eeden describes, the Australian government spends about $10 million dollars per year to maintain the fence but there are almost no data to compare livestock losses on either side of the fence. Thus she and her colleagues decided to look at what was being done globally to evaluate the effectiveness of different methods of protecting livestock.

DingoFencePeter Woodard

The Dingo fence across southeastern Australia. Credit Peter Woodard.

The researchers grouped livestock protection approaches into five different categories: lethal control, livestock guardian animals such as dogs, llamas and alpacas, fencing, shepherding and deterrents. Lethal control includes using poison baits and systematic culling of populations of top predators. Deterrents include aversive conditioning of problem predators, chemical, auditory or visual repellents, and protection devices such as livestock protection collars.

Screen Shot 2018-01-23 at 10.28.16 AM

A guardian dog emerges from the midst of its flock in Bulgaria. Credit: Sider Sedefchev.

Van Eeden and her colleagues then did a meta-analysis to see which approach worked best. You can check out my blog from Aug. 2, 2017 (“Meta-analysis measures multiple mycorrhizal benefits to plants”) for a more detailed discussion of meta-analyses. Very briefly a meta-analysis is a systematic analysis of data collected by many other researchers. This is challenging because each study uses slightly different techniques and has different levels of rigor. For this meta-analysis, van Eeden and her colleagues used only two types of studies. One type is a before/after design, in which researchers kept data on livestock loss before the mitigation treatment as well as after. The second type is a control-impact design, in which there was a control group set aside, which did not receive the mitigation treatment. Each study also needed sample sizes (number of herds and/or number of years), means and standard deviations, and had to be run for at least two months to be used in the meta-analysis.

The researchers searched several databases (Web of Science, SCOPUS and European Commission LIFE project), Google Scholar, and also used more informal sources, to collect a total of more than 3300 records. However, after imposing the requirements for types of experimental design and data output, only 40 studies remained for the meta-analysis. Based on these data, all five mitigation approaches reduced predation on livestock. The effect size in the figure below compares livestock loss with the treatment to livestock loss without the treatment, so that a negative value indicates that the treatment is associated with reduced livestock loss. The researchers conclude that all five approaches are somewhat effective, but the large confidence intervals (the whiskers in the graph) make it difficult to unequivocally recommend one approach over another. The effectiveness of lethal control was particularly variable (hence the huge confidence interval), as three studies showed an increase in livestock loss associated with lethal control.

van EedenFig2

Mean effect size (Hedges’ d) and confidence intervals for five methods used to mitigate conflict between predators and livestock.  More negative effect size indicates a more effective treatment. Numbers in parentheses are number of studies used for calculating mean effect size.

Finding that non-lethal management is as effective (or possibly more effective) than lethal control tells us that we should probably be very careful about intentionally killing large carnivores, since, in addition to being cool animals that deserve a right to exist, they also perform some important ecosystem services. For example, in Australia, there are probably more dingoes northwest of the fence than there are south of the fence, so exclusion may  be working. However there is some evidence that there are also more kangaroos and rabbits south of the fence, which could be an unintended consequence of fewer predatory dingoes. Kangaroos and rabbits eat lots of grass, so keeping dingoes away could ultimately be harming the sheep populations. Dingoes may also kill or compete with invasive foxes and feral cats, which have both been shown to drive native species to extinction, so excluding dingoes may increase foxes and cats, threatening native species.  Van Eeden and her colleagues argue that different mitigation approaches work in different contexts, but that we desperately need evidence in the form of standardized evaluative studies to understand which approach is most suitable in a particular context.

van Eeden Fig.3

Context-specific approach to managing the co-exstence of predators and livestock.

In all contexts, cultural and economic factors interact in mitigating conflict between humans and carnivores. The dingo is officially labeled as a wild dog, which invaded Australia relatively recently (about 4000 years ago), so the public perception is that this species has a limited historical role. Other cultures may have a different view of their predators. For example, the Lion Guardian project in Kenya, which trains and supports community members to protect lions, has successfully built tolerance for lions by incorporating Maasai community cultural values and belief systems.

To use a phrase that President Trump recently forbade the Centers for Disease Control to use in their reports, our decisions about predator mitigation should be “evidence-based.” We need more controlled studies that address the success of different mitigation approaches in particular contexts. We also must understand the costs of removing predators from an ecosystem, as predator removal can initiate a cascade of unintended consequences.

note: the paper that describes this research is from the journal Conservation Biology. The reference is van Eeden, L. M., Crowther, M. S., Dickman, C. R., Macdonald, D. W., Ripple, W. J., Ritchie, E. G. and Newsome, T. M. (2018), Managing conflict between large carnivores and livestock. Conservation Biology, 32: 26–34. doi:10.1111/cobi.12959. 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.

Successful scavengers

Scavengers have a bad reputation. They reputedly eat foul smelly stuff, and are too lazy or incompetent to track down prey on their own, depending on “noble” beasts such as lions to kill prey, and then sneaking a few bites when the successful hunters are not looking (or after they’ve stuffed themselves). Of course the reality is that scavenging is simply one way that animals make a living. Many different species, including lions, will scavenge if given the opportunity, and from a human perspective, scavengers provide several important ecosystem services. As one example described by Kelsey Turner and her colleagues, ranchers in parts of Asia gave diclofenac, a non-steroidal anti-inflammatory drug, to their cattle, which had the unintended consequence of killing much of the vulture community. Losing vultures from the scavenging community increased the prevalence of rotting carcasses, which caused feral dog and rat populations to skyrocket, resulting in a sharp increase of human rabies cases in India. The take-home message is that we need to understand what factors influence scavenging behavior and scavenging success.


Golden eagle overwintering in South Carolina scavenges a pig carcass in a clearcut. Credit: Kelsey Turner.

Turner and her colleagues were particularly interested in whether the size of a carcass, the habitat in which an animal dies, and the time of year, influence scavenging dynamics.   The researchers varied carcass size by using three different species: rats (small), rabbits (medium) and pigs (large). Habitats were clearcuts, mature hardwood, immature pine, and mature pine forest. Time of year was divided into two seasons: warm (May – September) and cool (December – March). I should point out that the cool season was mild by many standards, as the research was conducted at the Savannah River Site in South Carolina, with a mean winter temperature of about 10 ° C.


Map of Savannah River Site showing the study sites and diverse habitats.

The researchers collected data by laying down carcasses of varying size in each of the habitats in both summer and winter. Each carcass was observed by a remote sensing camera that captured the scavenging events, allowing the researchers to identify the species of each scavenger and how long it took for the carcass to be detected and consumed.


Two coyotes captured by a remote sensing camera scavenging a pig carcass on a rainy day. Credit: Kelsey Turner.

Scavengers discovered 88.5% of the carcasses placed during the cool season, but only 65.4% of carcasses placed during the warm season. Carcass size was also important, with only 53.9% of rats detected, in contrast to 78.5% of rabbits and 97.8% of pigs detected. But habitat interacted with these general findings: for example scavengers consumed all (23) rabbits in clearcuts, but only about 70% of rabbits placed in the other three habitats.

Detection time also varied with carcass size; in general scavengers found pigs more readily than rats or rabbits. As the graphs below show, this relationship was quite complex. Pigs were detected much more quickly than the smaller carcasses in clearcuts, and somewhat more quickly in mature pine. Additionally, this difference between pigs and the other species is stronger in the warm season (left graph) than in the cool season (right graph). In fact, there is no difference in detection time of pigs, rabbits and rats placed in mature pine during the cool season.


Natural log of mean detection time (in hours) of rat, rabbit and pig carcasses in warm season (left) and cool season (right) in different habitats.  CC = clearcut, HW = mature hardwood, IP = immature pine, MP = mature pine.

Not surprisingly pigs tended to persist longer (before being totally consumed) than the other two species. More strikingly, persistence time for all three species was much greater in the cool season than in the warm season.


Natural log of mean carcass persistence time (in hours) of rat, rabbit and pig carcasses during the cool and warm seasons.

Turner and her colleagues identified 19 different scavenger species; turkey vultures, coyotes, black vultures, Virginia opossums, raccoons and wild pigs were the most frequent. The first scavengers to detect pig carcasses were usually turkey vultures (76.0%) or coyotes (17.3%). An average of 2.8 different species scavenged at pig carcasses, in contrast to 1.5 at rabbit carcasses and 1.04 at rat carcasses. As you might imagine, most scavengers made short work of rat carcasses, so there was not much opportunity for other individuals or species to move in. Carcasses that persisted longer generally had a greater diversity of scavengers; for example, carcasses scavenged by 1, 2 or 3 species persisted, on average, for 90.5 hours, while those scavenged by 4, 5 or 6 species persisted, on average for 216.5 hours.


A flock of turkey vultures in a clearcut surround and scavenge a pig carcass. Credit: Kelsey Turner.

Early ecologists viewed feeding relationships within an ecological community as a linear process in which plants extract nutrients from soils and calories from the air, which they pass onto herbivores and then to carnivores, with considerable energy being lost in each transfer. Now, we use a food web perspective, which considers the essential contributions of scavengers and decomposers (among others) to these feeding relationships. Carcasses decompose much more quickly during the warm season, returning calories and nutrients to lower levels of the food web. Microbial decomposers are, in essence, competing with vertebrates for carcasses, and being metabolically more active in warm months, are able to extract a greater portion of the resources from the carcass than they can during the winter. Slow decomposition in winter allows longer carcass persistence, leading to a greater number and greater diversity of scavengers. As a bonus for those who believe in human primacy, these same scavengers help to create a cleaner and healthier world.

note: the paper that describes this research is from the journal Ecology. The reference is Turner, K. L., Abernethy, E. F., Conner, L. M., Rhodes, O. E. and Beasley, J. C. (2017), Abiotic and biotic factors modulate carrion fate and vertebrate scavenging communities. Ecology, 98: 2413–2424. doi:10.1002/ecy.1930. 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.

Treefall gaps deliver diversity

When John Terborgh began research at Cocha Cashu Biological Station in Peru back in 1974, he probably did not expect to still be working there 43 years later, doing research and publishing papers about the astounding species diversity in its tropical floodplain rainforest.

JT_TreefallLisa Davenport

John Terborgh leans against a fallen tree that has created a gap in the forest canopy. Credit: Lisa Davenport.

One contributor to species diversity in tropical forests is treefall gaps, which form when a mature tree falls down, opening up a gap in the overhead canopy. The most obvious change associated with treefall gaps is an increase in light that reaches the canopy floor. In comparison to the closed canopy, treefall gaps may be dryer, warmer, have increased plant transpiration rates, and may host many different species that colonize the new environment.

Treefallgap Irina Skinner

Small treefall gap in a dense rainforest. Credit: Irina Skinner

While it’s clear that gaps influence the physical environment of the forest floor, it is not clear how a changed physical environment translates to biological diversity of the treefall gap community. Comparing treefall gaps to closed canopy communities, Terborgh and his colleagues explored this relationship.

First the researchers asked whether the seed rain into tree gap communities is different from the seed rain into closed canopy communities. Seed rain describes the types and abundance of seeds that are dispersed into communities. Usually seeds are blown into communities by the wind, or enter attached to the bodies or excrement of animals. Alternatively, some seeds are autochorous – self-dispersing, in some cases aided by a change in fruit shape that causes seeds to be ejected explosively.

To do this analysis Terborgh and his colleagues needed a systematic way to measure seed rain. The researchers set up a regularly-spaced grid of small containers (seed traps) that collected a portion of the seeds that entered the community. They also needed a way to describe whether the canopy was closed, somewhat open, or very open as in a treefall gap. For each seed trap they calculated a canopy cover index (CCI), which measured the amount of vegetation found at different levels directly above the traps. A value of 0 indicated no vegetation (a completely open canopy), while a value of 6 indicated dense vegetation at all levels (a completely closed canopy).

As the graphs below indicate, there were some dramatic differences between gaps and canopies. Note that the x-axis has been log-transformed so CCI = 1 transforms to a log(CCI) = 0, and a CCI = 6 transforms to log(CCI) = 0.778. All four major groups of animal seed dispersers dispersed many more seeds into closed canopy forest than into treefall gaps. The relationship between seed abundance and canopy cover was strikingly linear for primates and small arboreal animals. This makes sense, as these animals tend to sit on trees, and spread seeds either through defecation of already eaten fruit, or by eating fruits and inadvertently spilling some seeds in the process. So very few trees in treefall gaps translates to many fewer seeds in treefall gaps, with most (76%) being blown in by the wind.


The log abundance of potentially viable seeds (PV seeds on y-axes) collected in seed traps in relation to the log (canopy cover index) for six different types of seed dispersal agents/mechanisms.

Terborgh and his colleagues realized that differences in seed dispersal could profoundly influence the number and types of plants that were recruited into the population. Despite the scarcity of animals in tree fall gaps, most of the saplings (79%) that recruited into gaps were animal dispersed, whereas wind-dispersed species made up only 1% of the saplings.

Sapling species diversity was greater under a closed canopy.


Sapling species diversity (measured as log(Fisher’s alpha)) in relation to canopy cover (measured as log (canopy cover index)).

Though species diversity was lower in tree fall gaps in comparison to the closed canopy, species composition (the types of species found there) was very different in treefall gaps. There were many species that recruited only under gaps, and were never found under a closed canopy. Interestingly, there is good evidence that the small treefall gaps in this study recruited a different set of tree species than do larger treefall gaps, which tend to recruit species that do best under conditions of very bright sunlight. Thus the researchers conclude that treefall gaps, small and large, offer a wide range of environmental conditions not found in the closed canopy,  that ultimately help to promote astoundingly high tropical forest tree diversity.

note: the paper that describes this research is from the journal Ecology. The reference is Terborgh, J., Huanca Nuñez, N., Alvarez Loayza, P. and Cornejo Valverde, F. (2017), Gaps contribute tree diversity to a tropical floodplain forest. Ecology, 98: 2895–2903. doi:10.1002/ecy.1991. 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.