We were still at Lebala Camp in Botswana (see Back from Africa: Part 1). I had just met a German couple who were profoundly concerned about dogs – in particular the African wild dog, Lycaon pictus. Only about 6600 individuals remain in this endangered species, but what troubled my friends is that the dogs and lions at Lebala were getting along very poorly. If the emotion of hate can be attributed to nonhuman animals, it can probably be applied to the relationship between lions and African wild dogs. Both compete for the same food, mostly ungulates (mammals with hooves) and lions will kill dogs if given the opportunity. This is what worried my new-found friends, who were deeply concerned about the viability of the pack of 13 individuals within Lebala.
Four African wild dogs from the Lebala pack rest in the tall grass. Credit: Cindy Miller.
It turns out they were right to be concerned. That very day, our local pack was attacked by a group of lions and the alpha female was killed. Nobody really knows what happened, but her body was discovered near the den – which is a hole where the pups are hidden. The pack generally goes out hunting during the day, and the alpha female guards the pups, using distraction to keep predators, usually lions, away from the den.
Most of the Leballa pack with the den entrance in the foreground. Credit: Cindy Miller.
When we arrived at the scene, we were not allowed to look at the remains, as our guide was concerned at how we might react, and, I believe, wanted to show respect for the dogs. The rest of the pack, littermates from the previous year, were five males and one female. Six pups populated the den, and the young adults were feverishly digging them out. There was lots of tail-wagging, butt sniffing, and playing when the pups finally emerged from their subterranean den. It was not clear to me that the dogs were behaving strangely, but our guide assured us that the six young adults were unusually wary.
Pups emerging from the den. Notice one pup is still making its way out. Credit: Cindy Miller.
We were, of course, saddened over the loss of the female, and very concerned about whether the pack would be able to survive. However, the behavior of the pups was incredibly joyful and uplifting. They were so happy to be liberated from their den, and equally happy to be in the company of their beloved family (am I anthropomorphizing a bit?). Everybody was jumping on everybody, with lots of wrestling, batting and yipping, that might be typical of a litter of domestic dogs that had just awakened from a nice siesta. This closeness promotes pack unity as the dogs mature, and helps contribute to their remarkably efficient hunting success. They hunt by chasing prey until they tire them out, and enjoy an unusually high success rate in comparison to other predators (including lions).
The final pup – the runt of this litter – finally emerges. Credit: Cindy Miller
The future for this pack was uncertain. Males stay with the pack, while females usually disperse to other packs. One problem is that as dog populations become more scattered and habitat becomes more fragmented (as a result of human development), it is difficult for females to find a new pack to disperse to. The pups in this pack were still nursing, but old enough so that some of their sustenance came from meat which was regurgitated to them by the young adults.
One of the males regurgitates food for a pup. Credit: Cindy Miller.
However, our guide did not know if these pups were old enough to survive without their mother. Mother’s milk provides pups with nutrients, but at this age, water is very limiting during the dry season. So even if the pups could be adequately fed, it is not clear if they would be hydrated enough to survive.
I know it’s been a while, and I attribute my declining blogging productivity to two factors: needing to devote my attention to the second edition of my textbook (see below), and working under the guidance of a declining population of neurons. It turns out that 71-year-old-brains have some serious limitations.
Recently, six of my closest friends and I were privileged to travel though parts of Botswana and Zimbabwe with the goal of viewing some of the world’s most spectacular animals. Most were terrestrial, but some – like hippos and crocs – spent much of their time in water.
Our accommodations in Lebala Camp in northern Botswana. A sausage tree (scientific name unknown to me) looms above the “tent”. Fruits crashed on our roof, summoning hungry hippos to visit us from the nearby marsh. Credit: Cindy Miller
As a behavioral ecologist, I spent a considerable part of my life exploring the sex lives of dragonflies and spiders. I was particularly enamored with the thought of upping my scale, and observing lions do the deed. Most nights, the sounds of extremely enthusiastic lions reverberated through the early morning hours, but, alas, I never did get to see them in action. But our group of friends did see some fascinating lion behavior. We were in Lebala Camp in northern Botswana (see above), and our guide, Thabo, told us there was a pride of lions nearby, and asked if we would like to see them. “Yes please” we roared. It did not take too long before we came across the mother lode – a group of 19 adult females, subadults of both sexes, and several cubs. But there was something peculiar about the group. As you might expect from the only social cat species (the other 40 cat species are non-social) many lions in this pride are literally on top of each other. Much of their time and energy is devoted to licking, pawing, and wrestling playfully.
Part of the large pride at Lebala Camp. Credit: Frank Singer
Unexpectedly, members of this pride were divided into two groups, separated by a two or three meter wide no-go zone. Several times, a cub from one group attempted to engage a lion from the other group only to be rebuffed with an outstretched swipe of the paw, often accompanied with a nasty-sounding snarl. One subadult male was particularly vigorous in defending the border between the two factions, repeatedly snarling, raising himself up and roaring at a particularly persistent cub from across the no-go zone.
The pride is separated into two factions. Credit: Frank Singer
What was going on? I asked Thabo about it, and he seemed a bit surprised by the apparent rancor. This was a particularly large pride. The three males were off patrolling their territory, while there was also one more female who had recently birthed a litter with an unknown number of cubs – after the birth she took off somewhere and had not been seen since. So the total number of lions in this pride was upwards of 25 – a large number of large animals. Was this pride about to split?
Overall, we watched this pride for about two hours. About midway through our vigil, two males returned and everything changed. Several females ran towards the two males, excitedly seeking their attention. The males were rock stars, and their fans – adult females, and subadults of both sexes were doing all they could to attract their heros’ attention. The youngest cubs mostly stayed by our jeep, watching the interactions. Personally, I was aggrieved by this shameless display of unconditional subservience and adulation by the females and subadults of both sexes.
A male surrounded by his adoring fans. A termite mound juts up in the background. Credit: Cindy Miller.
Male lion presence definitely changed the dynamics of interactions within the rest of the pride. Some females took off in a hurry, only to be corralled by the males. Others moved to a central staging area – eventually most of the pride settled in a new location a few hundred meters away. One male ran off in pursuit of a couple of females. I don’t know if they were off having fun, or if he was trying to return them to the pride. According to our guide, even though males are dominant, they prefer if the females are happy and getting along with each other. Pride instability can ruin the males’ chances at reproductive success.
Herbivores, by their nature, damage plants in natural ecosystems and in agricultural systems. And predators, by their nature, do a lot of damage to herbivores, either by eating them, or by harassing them in ways that cause them to change their behavior, or in some cases change their morphology or physiology (these are called nonconsumptive effects). The indirect effect of a trophic cascade in which predators damage herbivores which damage plants, is that predators can benefit plants by their detrimental effect on herbivores.
Much of the research on nonconsumptive effects has focused on aquatic systems because the predator cues are easy to manipulate in the laboratory. Simply let a predator hang out in a water tank for a while, and then add the predator tank water to a tank with a possible prey item, and study the prey’s response. But there has been little work on nonconsumptive effects in terrestrial systems. While there has been some research on how auditory cues emitted by terrestrial predators affect vertebrate herbivores, there has been almost no work on how auditory cues affect invertebrate herbivores. This is surprising, because invertebrates cause enormous damage to agricultural systems. Evan Preisser and his students wondered whether the beet armyworm caterpillar, Spodoptera exigua, a voracious herbivore on many commercially important crops, responded to buzzing emitted by an important predator, the caterpillar-hunting paper wasp (Mischocyttarus sp.). More important, they tested whether the response was substantial enough to have an impact on caterpillar mortality, and subsequent plant development.
Four Spodoptera caterpillars chomp on a soybean leaf. Credit: Michasia Dowdy, University of Georgia, Bugwood.org
Perhaps the biggest challenge was technical. The researchers needed to come up with a mechanism for delivering an auditory cue to one group of caterpillars that would not be detected by any other nearby group. They tried various conformations, including separating the cages with soundproofing foam, which, unfortunately, was not soundproof to wasp buzzes.
One of the failed attempts at auditory isolation. Unfortunately, the auditory stimulus was detectable up to two boxes away from the source. Credit: Zachary Lee.
Nothing worked until one of the students suggested using boxes that dry ice was shipped in, reasoning correctly that it should have good insulating properties. The decibel meter failed to detect any sound from adjacent boxes.
This worked! Credit: Zachary Lee.
Having solved the soundproofing problem, the researchers raised 36 groups of five caterpillars in small cups filled with 25 grams of caterpillar diet. Each cup was placed in a box and subjected to one of three treatments: no-sound control, recorded buzzing of a non-predatory mosquito, or recorded buzzing of a predatory wasp. The volume was the same for both sound treatments. Each tape went for 12 hours per day, with 2 seconds on, followed by 6 seconds off. The researchers found that survival was substantially lower for caterpillars that received the wasp treatment (top graph below). Also, caterpillars that survived the wasp treatment took, on average, longer to develop (bottom graph below), though that difference was not statistically significant.
Survival (top graph ), weight (middle) and time to pupation (bottom) of Spodoptera caterpillars subjected to no sound (green bar), mosquito buzz (yellow) and wasp buzz (red). Different letters above bars indicated statistically significant differences between treatments.
Preisser’s graduate student, Zachary Lee, took the lead in organizing the field experiment. The researchers wanted to know whether the negative effect of wasp buzzes that they detected in the laboratory had real consequences for agricultural systems. They surrounded each tomato plant (72 in all) with a mesh bag (to keep the caterpillars in and other insects out), and placed an average of 96 newborn caterpillars on each plant. Each group of four plants surrounded a speaker that emitted either no sound (control), mosquito buzzing, or wasp buzzing, which were broadcast at levels that caterpillars would experience when an insect was 5 cm away from them. Each sound was played in a loop of 1 minute on, followed by 10 minutes off, for 12 hours per day. Lee and his colleagues let the experiment run for 3 weeks, by which time all caterpillars had either pupated or died. They harvested each plant, and calculated the percentage of leaves that were damaged by caterpillars. Then they dried each plant, including the roots, and weighed them.
Field experiment with four tomato plants positioned equidistant from one central speaker. Each group of four received one of the experimental treatments. Credit: Zachary Lee.
Plant leaves associated with wasp buzzing received the least damage, leaves on control plants received the most damage, and leaves on plants with mosquito buzzing received intermediate damage. Aboveground mass was greater in wasp treated plants than in controls, so the sound of wasp buzzing helps to protect the tomato plants against voracious caterpillar herbivores.
Indirect effects of no sound (green bar), mosquito buzz (yellow) and wasp buzz (red) on tomato plants, via the effects of these treatments on Spodoptera herbivory. Different letters above bars indicated statistically significant differences between treatments.
The researchers did not study caterpillar behavioral changes because these caterpillars are easily disturbed, either freezing or dropping off of plants when approached. Lee and his colleagues point out that we know very little about how invertebrates, in general, respond to sound cues, as their survey of the literature on prey response to sound cues showed that 181/183 experiments used vertebrate prey. Given how widespread invertebrates are in agricultural systems, and in ecosystems in general, we need more studies to get a better handle on how invertebrates respond to sound, and most important, how their response influences agricultural systems and ecosystem structure and functioning.
Chiroptophobia, the fear of bats, is widespread throughout the world, but also subject to the cultural biases of different regions. In Europe, bats were historically associated with the Devil, evil spirits and witchcraft. Dante’s Inferno describes the Devil’s wings as being very much like bat wings in form and texture. Vampirism was well established in Eastern European folklore before Bram Stoker’s depiction of Count Dracula routinely transforming himself into a huge vampire bat. Other regions of the world are historically more nuanced in their perspectives. For example, in Madurai, India, worshippers of the Muni god revere the Indian Flying Fox, Pteropus medius, and protect bat colonies from harm. In Pudukkottai, Pteropus bats are guardians of sacred groves, while in Bihar these same bats bring wealth. But in the Punjab region of India magicians use bat blood to do malevolent magic, and across the border in some regions of Pakistan, bats are associated with evil witchcraft. This is only the tip of the humans/bats cultural iceberg. For a thorough consideration, you should go to https://www.intechopen.com/chapters/80107.
Can ecologists help us resolve this conundrum? The answer is also nuanced. On the negative side, bats live in dense colonies, are very social and relatively long-lived. Taken together, these traits allow them to harbor many pathogens, including rabies and coronaviruses, which may be passed on to humans. On the positive side, bats consume many insects including those that carry diseases. Recent research has also shown that bats consume insects that eat crops. Thus, in agricultural ecosystems, there exists a trophic cascade in which bats reduce insect abundance, which leads to an increase in crop production. Armed with this knowledge, and a recent finding by Tim Divoll that some bats eat insects that defoliate oak and hickory trees, Elizabeth Beilke and Joy O’Keefe decided to explore how important bats were in forested ecosystems. Does a similar trophic cascade exist, in which bats reduce herbivorous insect abundance, which leads to an increase in tree production?
Underside of oak leaf showing caterpillars hard at work. Credit: Lis Kernan.
To explore the trophic cascade hypothesis, Beilke and O’Keefe set up a three-year experiment (during 2018 – 2020) in the Yellowwood State Forest in Indiana, USA. They built 6 X 7 X 7 meter exclosures that were covered with nylon-mesh netting large enough to allow most insects but small enough to exclude bats.
Researchers set up a bat exclosure in the forest. A series of ropes and pulleys allowed them to raise the netting each evening and take it down in the morning. Credit: Elizabeth Beilke.
Each experimental unit was a control exclosure without netting, and an experimental exclosure in which the netting was raised during the night to exclude bats, and lowered during the day so that birds could forage. This allowed the researchers to attribute any treatment effects exclusively to nocturnal animals – basically bats. They set up seven pairs of exclosures each year; unfortunately one exclosure was destroyed when three trees fell on it during a violent storm. Within each exclosure Beilke and O’Keefe monitored 9 or 10 oak and hickory seedlings during the treatment period. They counted the number of insects on oak and hickory leaves in May, when the enclosures were set up, and August, when they were taken down.
Basic experimental design. Control plots allowed both bats and birds, while experimental plots allowed birds but excluded bats.
Did bat exclusion increase insect density? The answer is a resounding “yes” with bat exclusion associated with a 300% increase in insect density in comparison to control plots.
Mean number of insects (+95% confidence intervals) per seedling at the beginning of the field season (left Figure a) and at the end of the field season (right Figure B). Gray dots represent data generated by a statistical model.
Most important, did this increase in insect density lead to greater defoliation of the trees? Beilke and O’Keefe found that both oaks and hickories suffered greater defoliation when bats were excluded. The impact on oaks was substantially greater than the impact on hickories.
(Figure a – left) Mean defoliation when bats were permitted (top) and excluded (bottom). (Figure b – middle) Mean (+95% Confidence interval) defoliation when bats were permitted (control) or excluded from oak trees. (Figure c – right) Mean (+95% Confidence interval) defoliation when bats were permitted (control) or excluded from hickory trees.
There is some evidence that bats tend to eat more insects that feed on oak trees than insects that feed on hickories. For example, the most common bat in the forest, the eastern red bat, consumed three times more oak-defoliating than hickory-defoliating insect species. Thus bats could be affecting forest composition by preferentially protecting oaks over hickories. However, given recent declines in bat abundance from white-nose fungus and habitat destruction by humans, losing this protection may be contributing to oak declines in the Eastern United States.
Beilke and O’Keefe point out that bats can negatively influence herbivorous insects directly or indirectly. Direct effects involve eating herbivorous insects, which are positioned directly on leaves. Indirect effects can include eating the non-herbivorous adult insects (e.g. butterflies and moths) that produce the herbivorous caterpillars. In addition, some insects are sensitive to the ultrasonic sounds emitted by echolocating bats and may tend to avoid areas populated by bats. Overall, the bat/herbivorous insect/tree trophic cascade results in forests benefitting bats by providing food and places to roost, while bats benefit forested ecosystems by protecting them from herbivory. We now have one more reason to embrace our local bats.
In his massive elegy, “In Memorium A. H. H.”, Alfred, Lord Tennyson laments the death of his friend, Arthur Henry Hallam, at 22 years old. Tennyson writes,
“Who trusted God was love indeed
And love Creation’s final law
Tho’ Nature, red in tooth and claw
With ravine, shriek’d against his creed”
Thus Tennyson accuses the natural world of being rife with strife and violence.
It would be wrong to dispute Tennyson’s complaint outright, but ecologists can present mutualisms, interactions in which both species benefit, as a counterpoint to his argument. One of the best studied is the ant/acacia tree mutualism, in which acacia trees provide food and living accommodations to ants, which protect their home tree against herbivores, including immense creatures such as elephants and giraffes! Previous research had shown that acacias usually grew better if they harbored a colony of protective ants, even though they were providing the ants with costly resources. These resources included swollen thorns (domatia) which ants may use as homes or fungal gardens, and specialized structures (nectaries) which provide ants with sugar.
Swollen thorns (domatia) on an Acacia drepanolobium tree that is hosting Crematogaster nigriceps ants. Credit: Patrick Milligan.
As an undergraduate at the University of Florida, Patrick Mulligan learned about how ecology could be thought of as the study of the economy of nature. Keeping with the economic metaphor, Mulligan recognized that the tiny ants and relatively large trees trade in the same currency: carbon. He realized that tree growth is simply a measure of how much carbon a tree has to spend on itself. So he asked if ants might be influencing how much carbon is available for both themselves and the tree.
Acacia drepanolobium, the dominant tree in the savanna. Credit Patrick Milligan.
In Laikipia, Kenya, four ant species compete for Acacia drepanolobium host plants, the dominant woody plant in the savanna (see photo above). These ants differ in several traits including how much protection they actually provide, whether they consume tree-produced nectar, how they modify the tree, and how they influence a tree’s water relations (see photo and table below). If a tree can’t get enough water, it is forced to close the stomata on its leaf surface to reduce water loss from transpiration. When stomata are closed, carbon dioxide import is drastically curtailed, and photosynthetic rates (and carbon production) are reduced.
The four ants species studied by Patrick Milligan and his colleagues are Crematogaster sjostedti, C, mimosae, C. nigriceps and Tetraponera penzigi. Credit: Todd Palmer.
To determine how the four ant species influence carbon fixation and water relations in these acacias, Milligan and his colleagues set up a five-year ant-removal experiment between 2013-2018. They found 48 matched pairs of trees that harbored each ant species (12 pairs of trees per ant species), and then removed all of the ants from one of the two trees by fogging with a short-lived insecticide. The researchers restricted ant recolonization by applying to the base of each tree an annoyingly sticky substance that ants generally avoid.
After five years (in 2018), Milligan and his colleagues measured photosynthesis and transpiration rates in leaves of each tree, using tools that were specialized for those purposes. They then extrapolated from these leaf measurements to photosynthetic and water exchange rates for the entire tree crown (where most of the action is). They discovered that trees with C. mimosae (Cm) and T. penzigi (Tp) had substantially higher photosynthetic rates than trees with C. sjostedti(Cs) and C. nigriceps (Cn). But trees that had their ants removed were statistically indistinguishable in their photosynthetic rates (graph (a) below). In other words, removing ants caused Cm and Tp-trees to reduce their photosynthetic rates, and Cs and Cn tree to increase their photosynthetic rates, so they were equivalent after five years of ant removal.
(Graph a) Mean (+SE) photosynthetic rate at the tree crown and (Graph b) transpiration rate at the tree crown for acacia trees with ants present or removed. The letters to the side of each data point indicate when two species have statistically significant differences in their value. For example, in graph a, comparing the case where ants were present, the photosynthetic rates for Cm and Tp are not different from each other, but both are significantly greater than the photosynthetic rates for Cn and Cs. However, Cn and Cs have similar photosynthetic rates.
Looking at the table above, you will note that both Cs and Cn do some major alterations to the trees that might compromise carbon production. Though Tp does remove nectaries, it also consumes no nectar, so that interaction may be a wash. Based on these observations, we might suspect that Cs and Cn are actually tree parasites, while while Cm and Tp are closer to true mutualists that actually benefit the host trees. Supporting this idea, removing Cs sharply increased leaf area and also increased water exchange rate (graph (b) above). And trees that were continuously occupied by Cn also showed reduced leaf area, lower photosynthetic rates (graph a above) and water exchange rates (graph b above) at the tree crown than Cm or Tp. But there is more to the story.
Cn is an aggressive defender against would-be herbivores. However, it also eats large portions of the tree it inhabits focusing on the nectaries (which produce sugars) and the reproductive structures. One puzzling consequence of this behavior is that Cn-occupied trees are significantly better than other ant-occupied trees at bringing up subsurface water, perhaps helping the tree to survive droughts. The researchers plan to measure the root systems of all the trees in hopes of seeing whether Cn-occupation actually alters root development in a way that improves water uptake.
Complicating the story further is a consideration of carbohydrate production. Trees hosting Cs (the stem excavator) had much less starch in their stems than did trees hosting the other species. Starch is an important source of energy for all plants; in fact trees with Cs removed still had low starch levels after five years. Presumably the trees that were freed from hosting Cs prioritized growing new branches, or repairing cavities and defending against beetle infestation, over producing more starch for storage.
Trees occupied by Cm (a nectar consumer) had much higher glucose levels than trees hosting the other three species. Removing Cm caused the glucose levels to drop sharply (see graph below). Trees hosting the other nectar consumer (Cn) did not show this increase in glucose, possibly because Cn prunes the leaves and eats the flowers, leaving the host tree with insufficient nutrients to increase glucose levels.
Mean (+SE) glucose levels in the stems of trees hosting each ant species. Notice the sharp drop in glucose concentration five years after Cm removal.
I asked Patrick Milligan how trees get occupied by a particular ant species. He responded that there are battles for occupancy both between ant species, and sometimes within ant species. An ant from one colony locks in a death grip with an ant from another colony, they then fall from a branch and kill each other on the ground. So the bigger colony wins a battle by virtue of having some surviving ants to colonize the tree. One exception is Cs, which has slightly larger and presumably stronger ants, and will sometimes survive a head-to-head battle. Currently, Milligan and his colleagues are investigating how a tree may adjust its leaf physiology when paired with a new ant species, perhaps by activating different genes in response to the novel species. Though trees cannot choose their ant colonizers, they may be able to adjust to whichever species uses their services.
The cane toad has the distinction of being the world’s largest toad. It was introduced to Australia in 1935 to control cane beetles that were eating sugarcane (see A toxic brew: toad vs. quoll). Since their introduction, cane toads have expanded their range by over 2000 km from their release sites, which would be fine if all they did was eat cane beetles. As it turns out, they are worthless at eating cane beetles, but are very good at being eaten by many predators, including the northern quoll (Dasyurus hallucatus). This turns out poorly for the quolls, as cane toads are loaded with toxins, which quickly convert a cane-toad-fed quoll into a quoll corpse. Consequently, quoll populations are collapsing across much of Australia.
A northern quoll sports a radio collar. Credit: Chris Jolly
For his PhD work, Chris Jolly was hoping to explore whether he could use behavioral conditioning techniques to train quolls to avoid cane toads before he released them back into the environment. Unfortunately, while in captivity, the quolls lost their fear of predators, and became easy prey for dingoes, which resulted in a failed reintroduction to Kakadu National Park. In an interesting twist, another graduate student was releasing quolls onto Indian Island for a different purpose, and Jolly decided to regroup and focus his attention on how the prey population responded to a novel predator. In 2017, 54 quolls were released on the northern part of the island, which set up a natural experiment in which quolls were present in the north, and absent in central and southern Indian Island
Ben Phillips and John Moreen release the first batch of northern quolls on Indian Island (Kabarl), Northern Territory, Australia. Credit: Chris Jolly
Working with several researchers, Jolly established four research sites in the north and three in the south. At each one-hectare site, the researchers set up a 10 X 10 grid of live-traps which they baited with balls of peanut butter, rolled oats and honey (100 traps at each site). The target species was the grain-eating rodent, Melomys burtonia. Over the course of the study, 439 individual melomys were captured, weighed, sexed and implanted with a microchip for identification purposes. The researchers wanted to know how the presence of predaceous quolls influenced melomys abundance, and whether melomys adjusted behaviorally to quoll presence.
Research sites on Indian Island. Quolls were introduced to the northern part of the island in 2017.
They discovered that the three southern sites (without quolls) maintained relatively steady numbers of melomys throughout the study. In contrast, the four northern sites (with quolls) showed a sharp decrease in melomys abundance. Complicating the issue, a wildfire broke out in August 2017, affecting only the northern part of the island. The researchers believe this fire did not affect the melomys in any significant way, as wildfires are common in the area, and several previous studies have shown no effect of wildfires on melomys abundance.
Melomys population estimates at three southern sites (left graph) and four northern sites (right graph). The dashed orange line denotes quoll introduction, while the dashed red line indicates the wildfire in 2017. Error bars are 95% confidence intervals.
Shyness can be an adaptive behavior if predators are in your environment. Jolly and his colleagues wanted to know if there was any difference in the shyness (or conversely – the boldness) of melomys from the north (with quolls) and south (without quolls). They set up arenas that were baited with the aforementioned peanut butter balls, and placed a live-trap with a melomys at the door to the arena. The researchers then opened up the trap door and recorded whether the melomys entered the arena within 10 minutes.
Experimental setup testing melomys responses to open-field tests. Credit: Chris Jolly.
After 10 minutes, each melomys was rounded up and placed back in its trap, and a red plastic bowl was put into the arena. The trap was then reopened and the researchers recorded whether the melomys interacted with the red bowl.
Looking at the left graph, you can see that in 2017, north island melomys were much shyer than melomys from the predator-free south island. But by 2019, this difference was mostly gone. But when it comes to exploring a novel object (right graph), the northern melomys still retained some of their fear in comparison to southern melomys.
Figure 4
Left graph.Proportion (+ 95% confidence intervals) of melomys that emerged from live traps within 10 minutes in the open-field test. Right graph. Proportion of melomys that interacted with the novel object in the experiment that tested for neophobia (fear of novel objects).
Lastly, Jolly and his colleagues tested the effect of living with quolls on melomys foraging behavior. At nightfall, the researchers placed one wheat seed at 81 locations in each site. Control (unmanipulated) seeds were set out at 40 locations while seeds that had been stored with quoll fur (and presumably smelled like quoll) were set out at 41 locations. At daybreak, the researchers counted the number of remaining seeds, so they could calculate seed removal. In the first session conducted shortly after quoll release, they found no evidence of discrimination based on predator scent in either melomys population. But over time, the northern melomys began to discriminate based on quoll scent, while southern quolls continued to forage at the same rate on control and quoll-scented seeds.
Figure 5B
Mean seed take bias (the number of scented seeds – the number of control seeds) taken by north and south island melomys. Error bars are 95% confidence intervals.
The researchers conclude that introduction of quolls as a novel predator influenced melomys in two distinct ways. First, quolls preyed on them and reduced melomys abundance. But equally important, quolls changed melomys behavior. Soon after quoll introduction, invaded melomys populations were substantially shyer than the non-invaded populations. But this changed over the next two years, with a reduction in general shyness in the invaded populations, and an increase in predator-scent aversion. In effect, melomys were fine-tuning their behavioral response to quoll invasion.
Unfortunately, the researchers can’t evaluate whether these behavioral changes result from learning, or from natural selection. Melomys has a short generation time, so natural selection could be strong, even over a short timespan. Unfortunately, because of low survival from one year to the next, there were not enough melomys to test for whether individual behavior changed over time as a result of learning. It is certainly plausible that natural selection and learning operate together to change melomys behavior following quoll introduction.
If you are into wine, the Matorral of central Chile is viticulture heaven. This Mediterranean biome has very warm and dry summers and moderate, rainy winters – ideal conditions for grapes. The Matorral’s natural vegetation is a diverse sclerophyll forest composed of trees and shrubs with hard, short and often spikey leaves. Many of these trees and shrubs are endemic – found in the matorral and nowhere else, as are some of the animals that depend on the vegetation for sustenance, making this region a “biodiversity hotspot”. Humans enjoy its benign climate as well, which is why most of Chile’s population and largest cities occupy this bioregion.
Mattoral ecosystem dominates central Chile. Credit: A. Muñoz-Sáez
Unfortunately, the demands of humans for wine and domiciles can come into conflict with the Matorral’s biological diversity. Much of the natural vegetation has already been cleared and most is privately owned, so there is little potential for setting up large preserves. As a long-time bird enthusiast, Andrés Muñoz-Sáez wondered whether even small pockets of natural vegetation could help maintain the biologically diverse bird community in the region. So he and his colleagues conducted a series of systematic surveys to see whether the presence of remnant natural vegetation in the immediate area, or the presence of a continuous forest nearby, increased bird diversity within a vineyard.
A vineyard in central Chile shrouded by fog and surrounded by a sclerophyll forest. Credit: A. Muñoz-Sáez
The researchers conducted 6 auditory and visual surveys for birds in 2014 at 20 vineyards that differed in the amount of surrounding natural vegetation. They repeated this process early and late in the 2015 breeding season, for a total of 360 surveys. There were three types of surveys: (1) Within the vineyard with no natural vegetation remnants within 250 meters, (2) within remnants within the vineyard, and (3) within native vegetation adjacent to the vineyard. The mean size of a remnant was 0.17 hectares. All told, the researchers recorded 5068 birds belonging to 48 species.
A burrowing owl keeps watch while perched on a vineyard fencepost. Credit: A. Muñoz-Sáez
Both species richness (left graph below) and overall bird abundance (right graph below) were lowest in the vineyards without remnants nearby, and highest in remnants and in the surrounding matorral. Richness and abundance were very similar in remnants compared to the surrounding matorral.
Species richness (mean number of species – left graph) and mean number of birds (right graph) per survey conducted in surrounding matorral (M), remnants within a vineyard (R) and in vineyard with no nearby remnants (V). Error bars are 1 standard error. Horizontal bars with *s above bars indicate statistical differences between treatments. * = P < 0.05. *** = P < 0.001.
From the standpoint of species composition (which species were present), bird communities in vineyards with remnants were more like those found in surrounding matorral than like those in vineyards without remnants. Perhaps most important from the standpoint of conserving biological diversity, the mean number of endemic bird species was greatest in matorral (3.02 endemic birds per survey), intermediate within remnants (1.11) and negligible within the vineyard without remnants nearby (0.03).
Muñoz-Sáez and his colleagues advocate retaining remnant native vegetation within vineyards to provide local habitat for native birds. Their surveys indicated that insectivorous birds were more than six times as likely in remnants than in vineyards far removed from remnants. From the standpoint of providing ecosystem services to humans, insectivorous birds can benefit vineyard production by removing unwanted insect pests. Given that many remnants are in less productive areas such as steep slopes, or along streams, the costs of maintaining and not developing these remnants are relatively minor, while the benefits to the viticulturist and the ecosystem can be substantial.
The endangered black lion tamarin, (Leontopithecus chrysopygus), lives in mostly degraded and highly fragmented landscape in the state of Sao Paulo, Brazil. Olivier Kaisin is a PhD student who wants to know whether declining environmental conditions are causing increased stress to the tamarins. Researchers often use glucocorticoid (GC) levels as a measure of physiological stress, as many animals, including primates, produce and release GCs in response to stress. Many researchers have argued that prolonged elevation of GC levels has a negative impact on individual survival or reproduction, but it is not clear whether this is true for most primates. Given that 60% of primate species are currently threatened with extinction, it would be nice to know whether conservation biologists could use GC levels to identify populations that are at risk.
The black lion tamarin, Leontopithecus chrysopygus.
One of the unadvertised features of graduate programs is that students need to learn about their study system before doing research. In this spirit, before beginning his tamarin study, Kaisin (working with several other researchers) did a meta-analysis of all studies (published until 2020) that compared cortisol levels in primates from disturbed vs. undisturbed habitats to see if the type of disturbance influenced GC levels. Disturbance types included hunting, tourism, habitat loss, ongoing logging, habitat degradation and other human activities. Habitat loss was a reduction in forest fragment size to less than 500 hectares. Habitat degradation resulted from logging in the past 20 years that led to changes in forest structure and diversity, but did not substantially reduce the size of the forest habitat. Other human activities did not fit into the five disturbance types, and included activities such as mining, urbanization and access to rubbish.
The graph below shows the effects of the different disturbance types. “Hedges g” is a test statistic used in meta-analyses to look for effects of different variables. The midpoint of the bar (or the diamond in the case of the overall effect) is the mean value of Hedges g, while the endpoints of each bar (or diamond) indicate the 95% confidence interval. If the entire interval does not overlap 0, then we can conclude that there is a statistically significant effect of that variable. Based on this analysis, both hunting and habitat loss were associated with significant increases in glucocorticoid levels in primates, contributing to a significant overall increase in glucocorticoid levels in response to disturbance.
The influence of six types of disturbance on GC levels of 24 different primate species. * indicates statistically significant effects.
As Kaisin and his colleagues point out, six of the studies actually showed a significant decrease in GC levels in association with disturbance. For example, howler monkeys had reduced GC levels in response to ongoing logging. The researchers interpret this surprising GC decrease on the elimination of large predators from the logged forest, which substantially reduces howler monkey stress levels. As a second example, in Madagascar, an invasive tree species in the degraded site provided important fruits for red-bellied lemurs, leading to well-fed lemurs with reduced GC levels. Unfortunately, these confounding variables cannot be easily controlled, so researchers need to consider each study on a case-by-case basis. Some families of primates were more influenced by stress than others. In particular, hominids (great apes) and atelids (New World monkeys such as howler, spider and woolly monkeys) both showed significantly greater GC levels in association with stress. Three families showed smaller increases while three other families of primates were basically unaffected.
The influences of disturbance on eight different primate families (as measured by Hedges g). CI (95%) is the 95 percent confidence interval. Weight is a measure of the contribution of each primate family to the overall effect. Families with more species/studies contribute more weight to the overall effect
The researchers emphasize that many more studies are needed in order to understand when we should expect stress to elevate GC levels in primates. For example, only one of the studies looked at stress effects on Asian primates. Future studies in endocrinological primatology should relate how prolonged stress influences fitness – including survival, growth and development and reproductive success. In turn, this would allow the conservation community to understand the relationship between stress and future population viability.
Red foxes were introduced to Australia in the mid-19th century to provide hunting opportunities for the English colonists. Since then, the fox population has exploded and spread throughout the continent, creating happy hunters, but probably leading to the decline of many native mammal species. As a result, conservation ecologists have attempted to reduce the fox population, primarily using a program of poison baits, but also by reintroducing other predators, such as dingos, that might be able to outcompete the foxes.
A red fox on the hunt
There are many challenges associated with eliminating foxes and restoring endangered native mammal populations. As it turns out, red foxes are primarily nocturnal so they are not so easy to hunt, and some of their prey have either gone extinct or are reduced to very small remnant populations. In cases where fox prey have been reduced but not eliminated, conservation ecologists want to understand what the numerical response of a recovering population will look like. Will the recovering population increase immediately until another factor, such as food availability, becomes limiting, and then level out at a stable equilibrium? Or might the recovering population show boom-bust dynamics, increase rapidly until it overeats its resources, then decline sharply from food deprivation, which allows food availability to recover, at which point the recovering population may go through another boom phase? If these boom-bust dynamics (also known as eruptive dynamics) are predictable, that knowledge would allow conservation ecologists to know how long they need to monitor a recovering population to establish its long-term trajectory.
Richard Duncan and his colleagues used data from two types of sources. Most of the data were population abundance time series of at least seven years (mean = 17 years) from 169 populations of 20 native Australian mammalian species that were recovering following fox control programs. In addition, the researchers compared their Australian data with time series from seven populations of ungulates that were translocated to northern or mountain regions of Canada, Alaska and Europe.
More than half of the populations were either unchanged or continued to decline following fox removal. Duncan and his colleagues suggest that fox control might have been inadequate in these cases, or that some other factor continued to limit the native mammalian populations. But 46% of the populations did increase following fox control. Some of these species, for example the brushtail possum, increased to much higher abundance, and then leveled off.
The brushtail possum in Austin’s Ferry, Tasmania. Credit: J. J. Harrison.
Abundance of the brushtail possum following intensive red fox control that began in 2003 in Boodoree National Park in eastern Australia. The black-dotted, blue-dashed and solid red curves (in this graph and the graph below) were generated by three different models that were fitted to the data. In this case, the blue dashed curve was the best fit.
But most (56%) of the populations that increased following red fox control showed evidence of eruptive dynamics. For example, the long-nosed bandicoot increased sharply following intensive fox control for about two years, but then crashed sharply, approaching pre-removal levels after another three years.
The long-nosed bandicoot at Craters Lake National Park in Queensland, Australia. Credit: Joseph C. Boone.
Abundance of the long-nosed bandicoot following intensive red fox control that began in 2004 in Boodoree National Park in eastern Australia. In this case the solid red curve was the best fit.
Species with higher maximum rates of increase tended to reach their eruptive peak more rapidly. In addition, larger species, such as the translocated ungulates, took longer to reach their eruptive peaks.
Time until a mammal population reaches its eruptive peak in relation to the maximum annual rate of population growth (top graph), and the mean body mass of each species (bottom graph). The solid line is the best fit generated by the model, while the dashed lines represent 95% confidence intervals. Both axes use logarithmic scales.
These findings demonstrate that it is not sufficient to show that a threatened population is recovering following removal of an invasive species such as the red fox. It is possible that even with continued fox control, the recovery will be short-lived, only to be followed by a population crash. Density dependent factors – factors that become more important at high population densities – are probably responsible for many of the observed population crashes. We have already discussed food availability dynamics; other density dependent factors could include predators being attracted to large prey populations, or disease being more easily transmitted when populations reach a certain level. Because they take longer to reach their eruptive peak and then crash, larger species need to be monitored by conservation ecologists for a longer period of time than do smaller species. Conservation managers need to anticipate these eruptive dynamics as they create their species recovery plans following predator removal.
Biological diversity is one part of “ecosystem structure”. Other components of ecosystem structure include which species are present, how abundant they are, whether some species are particularly important for the ecosystem to function, and how all the species interact with each other and the environment. So ecosystem structure is a pretty loaded concept, and figuring out what controls ecosystem structure has captured the intellect and imagination of many ecologists for a long time.
Two mutually non-exclusive theories have emerged in discussion of control of ecosystem structure. The bottom-up control hypothesis argues that the producers (primarily plants) are key, so factors influencing plants (such as sun, water and soils), are paramount for understanding ecosystem structure. The top-down control hypothesis argues that carnivores eat herbivores and herbivores eat plants, so we should focus our attention on the carnivores who directly influence herbivore abundance, and indirectly (by virtue of their effects on herbivores) influence plant abundance and diversity.
Rong Wang, his research advisor Xiao-Yong Chen, and several other researchers recognized that Thousand Island Lake would be a perfect place to explore these hypotheses about control of ecosystem structure. Construction of the Xin’an River Dam in 1959 created the lake of 573 km2 that is dotted with more than 1000 islands of varying size. This creates a natural laboratory for ecologists interested in understanding how island size influences ecosystem structure and specifically to explore the relative importance of bottom-up vs. top-down effects. In addition, these islands are actually forest fragments surrounded by a matrix that is inhospitable to terrestrial species. Ecologists are very interested in how fragmentation influences ecosystem structure, because development projects (residential, commercial, public works, etc.) invariably produce fragments of habitat of varying size. Lastly, when establishing nature preserves or conservancies, conservation ecologists need to know how large their reserves should be in order to optimize biological diversity and ecosystem functioning.
The Thousand Island Lake showing a few of its thousand+ islands. Credit: Xiao-Yong Chen.
The major producer in this ecosystem is the evergreen tree, Castanopsis sclerophylla.
Two Castanopsis sclerophylla trees. Credit: Xiao-Yong Chen.
Their seeds are eaten by two species of rodents, which in turn are eaten by carnivores – primarily snakes, cats and weasels. The researchers knew about these interactions before beginning the study, but they wanted to understand precisely how each player affected ecosystem structure, and how the size of the ecosystem influenced these different levels. They also wanted to explore possible bottom-up effects; for example how does environmental quality affect ecosystem structure.
Hypothesized top-down (orange arrows) and bottom up (green arrows) processes within the ecosystem.
For their study, Wang and his colleagues established research sites on habitats of three different size classes: four small islands (0.6 – 3.2 ha), three medium islands (13-51 ha) and six large habitats (three on the only large island of 875 ha and three on the mainland forest). Initially the researchers conducted surveys of Castanopsis sclerophylla seedling density, rodent density and environmental conditions. They discovered that seedlings were much more abundant on the mainland and large island (graph a below), while rodents were much more abundant on medium islands (graph b). However, small islands were more subject to drought due to lower soil moisture content and higher temperatures – a result of greater surface area exposed to the sun along the perimeter of each small island (graph c and d). Ecologists call this the edge effect. If you refer back to the first photo in this blog, you will note that the small island in the foreground has a great deal of exposed edge.
Over several years, the researchers systematically placed 12,500 seeds of Castanopsis sclerophylla on the surface across all of the sites, and tracked seed predation and seed dispersal. Seeds on medium islands survived much more poorly than did seeds on the other habitats (top graph below). Wang and his colleagues also planted 2,750 seeds of Castanopsis sclerophylla in transects across all four sites. In this case seedling emergence and survival was much lower on small islands than any of the other three habitats (bottom graph).
Top Graph. Survival rates of Castanopsis sclerophylla seeds after being moved away by rodents to a new location (left graph) and overall survival rates until the next spring (right graph). Bottom graph. Emergence rate of 2750 planted seeds (bottom left), and survival through summer (middle) and over the following winter (right).
Piecing together these data, we can see both top-down and bottom-up forces influencing ecosystem structure depending on the size of the habitat. On the mainland and on large islands there are several different types of predators which feed on rodents. But medium and small islands are just too small to support viable populations of predators. Thus rodents are super-abundant on medium islands, and eat the seeds that are on the surface. This is an example of top-down effects causing a trophic cascade, with predators eating rodents, which leads to high seed survival on large habitats. However on medium islands, predators are absent causing rodents to increase sharply and consume most of the seeds.
But bottom-up effects prevail on small islands, which are so small that that they support only a few rodents. Seeds that are broadcast on the surface survive predation from the small rodent population relatively well, but seeds that are planted have poor survival because of low soil moisture and high temperature (the edge effect). I asked Chen whether he thought we could generalize that top-down effects might be more important on large scales and bottom-up effects on small scales. He responded that both types of regulation are likely to be scale-dependent in many different ecosystems, but that species composition and resource availability would determine how top-down vs. bottom-up control ultimately influences ecosystem structure.
Fred's Ecology and Environmental Tales (AKA: The FEET) 