Successful scavengers

December 31, 2017 by fredsingerecology

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

December 4, 2017 by fredsingerecology

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.

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.

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.

Cat and fox: agents of Australian extinctions

November 15, 2017 by fredsingerecology

River restoration responses

November 7, 2017 by fredsingerecology

The Lippe River in Germany has been subjected to many decades of channelization, deepening, floodplain drainage, straightening and consequent shortening, with one result being that the modern Lippe is 20% shorter than it was two centuries ago. Beginning in 1996, conservation managers began reversing this trend by widening the river, raising the level of the river bed, constructing small islands within the river and terminating floodplain drainage operations over a stretch of 3.3 km. As a result of these activities, a small portion of the river looks much like it did 200 years ago.

A section of the Lippe River before (left) and after (right) restoration.

Over a 21-year period, researchers from Arbeitsgemeinschaft Biologischer Umweltschutz have conducted systematic surveys of fish communities at the restored and unrestored sections of the river. Researchers sampled the fish community with electrofishing – inputting a direct electrical current into the river – which causes the fish to swim towards the boat where they are easily collected with nets, identified by species, and returned unharmed into the river. A data set over this length of time in association with a restoration project is very unusual; oftentimes (in part due to funding issues) only one survey is conducted to assess the fish community response to river restoration.

About eight years ago, while a postdoctoral researcher at Senckenberg Research Institute in Frankfurt, Germany, Stephan Stoll was asked to analyze some river restoration outcomes, and, as he describes, “became hooked to the topic.” To evaluate the response of the Lippe River fish community to restoration, a group of researchers headed by Stephanie Höckendorff, a Master’s student with Stoll, first asked a very simple question – how did fish abundance and species richness (the number of fish species) compare in the restored and unrestored regions of the river.

The graph below shows several striking trends. Abundance peaked about 2-3 years after restoration, declined sharply the next year, and recovered in subsequent years to about three times the abundance found in unrestored sections. Importantly, abundance varied extensively year-to-year. For example, if you had done only one survey in 2000, you would have erroneously concluded that restoration had no effect, which is why the researchers emphasize the importance of collecting data over a long stretch of time.

Abundance of fish in restored (Rest-gray curve) and unrestored (Cont-black curve) sections of the Lippe River. The gray vertical bar indicates the start of the restoration project in 1997.

Species richness increased sharply, but did not reach its peak until nine years after restoration. Again, there was extensive year-to-year variation in species richness.

Fish species richness in restored (Rest-gray curve) and unrestored (Cont-black curve) sections of the Lippe River. The gray vertical bar indicates the start of the restoration project in 1997.

Höckendorff and her colleagues were intrigued by this delay in species richness, and turned their attention to understanding what types of species benefited most from the restoration. Their analyses indicated that colonizing species, such as common minnows and three-spined sticklebacks, tended to have short life spans, early female maturity, several spawning events per year and a fusiform body shape – a body that is roughly cylindrical and tapers at both ends. Interestingly, some of the most successful colonizers took quite a long time to get well-established within the community.

Common minnows, Phoxinus phoxinus. Credit: Carlo Morelli (Etrusko25)

The three-spined stickleback, Gasterosteus aculeatus. Credit: Ron Offermans

The restored habitat was highly dynamic, experiencing periodic flooding and the formation of temporary shallow bays and shifting sandbanks. These types of habitats tend to select for minnows, sticklebacks and other opportunistic species that are attracted to periodic disturbances. These opportunistic species were quick to move in, and continued to increase in abundance over time. Importantly, several rare and endangered species also colonized the restored habitat. However, large, deep-bodied, slow maturing and long-lived species did not benefit (at least over the 17 years of the survey), as these types of species are generally favored in less dynamic habitats, which are more stable and uniform.

Overall, these findings demonstrate the benefits of river restoration to the fish communities they harbor. But some species are more likely to benefit than others, and the time-scale over which recolonization occurs is highly variable. Surveys must be repeated over a long time-scale to tell conservation managers whether their restoration efforts are successful, and how they might change their future river restoration efforts.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Höckendorff, S., Tonkin, J. D., Haase, P., Bunzel-Drüke, M., Zimball, O., Scharf, M. and Stoll, S. (2017), Characterizing fish responses to a river restoration over 21 years based on species’ traits. Conservation Biology, 31: 1098–1108. doi:10.1111/cobi.12908. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2017 by the Society for Conservation Biology. All rights reserved.

Seagrass scourge: when nutrient enrichment reaches the tipping point

October 24, 2017 by fredsingerecology

Sean Connell has watched as south Australia has lost vast expanses of kelp forest and seagrasses over the past years. One of the primary culprits associated with loss of seagrass meadows is excessive nutrients, particularly nitrogen, which enters the ecosystem with runoff, and causes an increase in algal epiphytes (epiphytes are small plants that grow on other plants). Epiphytes can negatively affect seagrass by blocking sunlight needed for photosynthesis, and indirectly, by increasing the rate of cellular respiration within the ecosystem, thus using up oxygen needed by seagrass for metabolic processes.

Two dolphins swim above a bed of seagrass off the south Australian coast.

Connell and his colleagues noticed that seagrass loss was often sudden; a large seagrass meadow would appear to be in good shape, and then it would abruptly disappear. They suggested that there might be a threshold effect in nutrient levels that seagrasses can tolerate; that these systems function well until a certain threshold in nutrient levels is crossed, above which there is an abrupt loss of seagrasses. They tested this hypothesis by subjecting plots of the seagrass Amphibolis antarctica to seven different concentrations of dissolved inorganic nitrogen (DIN) over a 10 month period, and monitored the abundance of epiphytes and seagrass over that timespan.

The meadows were about two km offshore from Lady Bay, Fleurieu Penninsula, Australia, in about 5 meters of water. Different amounts of nitrogen fertilizer were wrapped in nylon bags (for slow continuous release of DIN) and staked to the ocean floor. Amphibolis antarctica grows by producing new leaves at the top of each leaf cluster, but at the same time it drops old leaves. Leaf turnover, the researchers’ measure of growth, is simply new leaf production minus old leaf drop. The researchers tied on a small nylon cable at known locations on selected plants, noted how many leaves were above and below each tie at the beginning of the experiment, and recounted leaf number 10 months later. Finally, the researchers measured epiphyte growth by microscopically viewing a sample of seagrass leaves, and counting the number seagrass leaf cells that were covered by epiphytes.

Seagrass growth was relatively unaffected by all tested DIN levels.

Leaf production per day in relation to concentration of DIN.

However, leaf drop showed a strong threshold effect; leaf drop rates increased sharply between 0.13 – 0.15 mg/L of DIN.

Leaf drop per day in relation to concentration of DIN.

Putting these two graphs together, you can see (below) that leaf turnover switched from positive to negative at 0.13 – 0.15 mg/L of DIN. Negative leaf turnover translates to a sudden loss of seagrass at that threshold. At least in this system, at this location, 0.13 – 0.15 mg/L of DIN is the tipping point, beyond which the seagrass system suddenly goes into decline.

Leaf turnover per day (left y-axis and red data), and Epiphyte cover (% – right y-axis and green data), in relation to concentration of dissolved inorganic nitrogen.

The graph also shows that the tipping point coincides with an epiphyte cover of approximately 60%. It is possible that increased epiphyte cover may reduce seagrass photosynthetic rates (particularly in lower leaves), so that leaf turnover suddenly shifts into the negative zone, but the study was not designed to identify the underlying mechanism.

Seagrass meadows perform important ecosystem services, such as absorbing excess nutrients from the sediment, and providing habitat and food for a diverse group of grazers and indirectly, for their consumers. Thus seagrass conservation is vital. The danger here is that moderate levels of nutrients do not appear to have much effect on seagrass populations, but there is an abrupt shift to seagrass loss once the nutrient threshold is crossed. This makes the system very difficult to manage, because the loss occurs without warning. Australian ecologists have repeatedly failed to restore lost seagrass meadows, as simply reducing nutrient levels does not reverse the process. Thus anticipating seagrass loss before it happens is the most viable management solution for this critical ecosystem.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Connell, S. D., Fernandes, M., Burnell, O. W., Doubleday, Z. A., Griffin, K. J., Irving, A. D., Leung, J. Y.S., Owen, S., Russell, B. D. and Falkenberg, L. J. (2017), Testing for thresholds of ecosystem collapse in seagrass meadows. Conservation Biology, 31: 1196–1201. doi:10.1111/cobi.12951. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2017 by the Society for Conservation Biology. All rights reserved.

Crawling with caterpillars courtesy of climate change – and ants

October 6, 2017 by fredsingerecology

In the book of Exodus, Yahweh inflicts upon the Egyptians ten plagues, several of which have biological bases. Plagues two three, four and five are frogs, lice, wild animals and diseased livestock. But it is the eighth plague that is relevant to today’s tale – the locust explosion. As it turns out, insect populations have periodically exploded throughout recorded history (and no doubt before), and for many years ecologists have been trying to understand why insect populations are so variable. Rick Karban has taught a field course at Bodega Marine Reserve, California since 1985, and, as he describes “In some years, the bushes are dripping with caterpillars and in others they are very difficult to find. The wooly bears (Platyprepia virginalis) are so conspicuous and charismatic that I couldn’t help wondering what was responsible for their large swings in abundance (they are more than 1,000 times as abundant in big years than in lean ones).”

Wooly bear caterpillar density during annual surveys conducted in march of each year.

The early stage caterpillars are most common in wet marshy habitats, but as they develop, they move to dryer upland habitats where they pupate, metamorphose into moths and mate. Young caterpillars live in leaf litter, eating vegetation and decaying organic matter.

Late instar (close to pupation) wooly bear caterpillar feeding on bush lupine. Credit Rick Karban.

Karban and his colleagues recognized that insect populations are sensitive to climate, and wondered whether climate change may be playing a role in Platyprepia population explosions. But there’s much more to climate change than global warming; for example, many areas of the world expect much more variable precipitation patterns, with more big storms and more droughts. Karban and his colleagues wanted to know whether variable precipitation might affect wooly bear populations. So they examined rainfall records between 1983 and 2016, and found that numerous heavy rainfall events (over 5 cm) in the previous year were correlated with increases in caterpillar abundance.

Change in caterpillar abundance in relation to number of heavy rainfall events (over 5 cm) during the previous year. Note the y-axis is the natural logarithm of the change in abundance.

Karban and his students explored three hypotheses for why caterpillars increased following a year with numerous heavy rainfall events. First, perhaps more rain causes more plant growth and deeper litter, providing extra food for caterpillars. Second, heavy rains may reduce the number of predacious ground-nesting ants. Lastly, heavy rains may produce deeper denser litter providing refuge from predacious ants.

The researchers tested litter as food hypothesis by comparing caterpillar growth rates during the summer, which usually has very little rainfall. They weighed individual caterpillars, placed them into cages and supplied them with litter from either wet or dry sites. After 30 days, they reweighed the caterpillars and found that all of them had lost weight, and that there were no significant differences in weight change between wet and dry sites. Thus, at least during the summer, there was no evidence that wet sites had better food for caterpillars.

Karban and his colleagues turned their attention to ants.

KarbanFig6

If ants stayed away from wet sites, that would suggest that rainy years may benefit caterpillars by reducing the number of ants in their habitat. To measure ant abundance, the researchers set out bait stations supplied with a sugar-laced cotton ball and 1 cm³ of hot dog. They discovered many more ants, and in particular, many more Formica lasioides (a fearsome caterpillar-killer) ants were recruited to dry sites than wet sites. This suggested that years with numerous rainfall events might reduce ant abundance, at least in the wet areas preferred by young caterpillars.

The researchers tested the ant predation hypotheses by caging caterpillars in plastic deli containers that had either window screen bottoms that allowed ants to enter but prevented the caterpillars from leaving, or had spun polyester bottoms that prevented ant access. At each of 12 field sites, the caterpillars were caged with litter that matched the depth and wetness of litter found at that site. All caterpillars protected from ants survived, while 40% of the unprotected caterpillars from dry sites and 23% of the unprotected caterpillars from wet sites were killed by predators. So ants are clearly fearsome predators, but more so under dry conditions.

A Formica lasioides ant subdues an early install wooly bear caterpillar within the confines of a deli box. Credit Rick Karban.

But does litter wetness help protect against predacious ants? To investigate this question, the researchers placed caterpillars in deli containers that permitted ant access. At each site, two containers were placed side-by-side; one contained a caterpillar + litter from a wet site, while the other contained a caterpillar + litter from a dry site. Both containers were completely filled with litter and left in the field for 48 hours. The researchers discovered that caterpillars were 26% more likely to avoid predation if they were in a container stuffed with litter from a wet site. This suggests that litter from wet sites acts as a refuge for caterpillars against predators.

Caterpillar survival rate in relation to litter wetness.

Unfortunately, no long-term data on ant abundance are available, so we don’t know the relationship between ant and caterpillar abundance over time. But when ants were excluded, caterpillars survived well, and when ants were present, caterpillars survived best in wet sites with deep litter. It is not clear why caterpillars survive ant predation better in wet litter. One possibility is that caterpillars are more active than ants at cooler temperatures, and may be more likely to avoid them in wet and cool conditions. A second possibility is that dry litter is structurally less complex than wet litter, and ants may be more likely to move efficiently to capture caterpillars in dry terrain.

Given the predictions for more rainfall variability in coming years, Karban and his colleagues expect caterpillar abundance to fluctuate even more dramatically from year to year. In this system, and presumably other insect populations as well, multiple factors interact to determine whether there will be a population outbreak reminiscent of Pharaoh’s experience early in recorded history.

note: the paper that describes this research is from the journal Ecology. The reference is Karban, Richard, Grof-Tisza, Patrick, and Holyoak, Marcel (2017), Wet years have more caterpillars: interacting roles of plant litter and predation by ants. Ecology, 98: 2370–2378. doi:10.1002/ecy.1917. 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.

Changing climate promotes prolific plants and satiated consumers

September 26, 2017 by fredsingerecology

Plants in Sweden can have a difficult life, but climate change has provided a more benign environment for some of them, including the white swallow-wort, Vincetoxicum hirundinaria. This perennial herb grows in patches in sun-exposed rocky areas, in forests located below cliffs, and along the edges of wooded areas. The plant forms clumps that are heavily laden with flowers in June and July, and creates pod-like fruits in July and August

Vincetoxicum hirundinaria growing in rocky outcrop (top photo). Vincetoxicum pods releasing their wind-dispersed seeds (bottom photo).

Christer Solbreck has had a lifelong interest in insect populations, and he has been following the insects that eat Vincetoxicum’s seeds for the past 40 years. As he described to me, surprisingly few population ecologists actually measure the amount of food available to insects. I should add that very few people have the resilience to study the same population of insects for 40 years, either. And interestingly, though this paper discusses the effect of a changing climate on seed production and seed predation, it was not Solbreck’s intent to consider climate change as a variable when he began, as climate change was not a concern of most scientists in the 1970s.

But climate change has happened in southeastern Sweden (and elsewhere), and has affected ecosystems in many different ways. Ecologists can quantify climate change by describing its effect on the vegetation period, or growing season (days above 5°C), which has increased by about 20 days since the mid 1990s.

Length of growing season (vegetation period) in southern Sweden.

During the same time period the abundance of Vincetoxicum has increased sharply.

Vincetoxicum abundance, measured as area of the research site covered, during the study.

You will note that “Vincetoxicum” has the word “toxic” in its midst; the seeds are toxic to most consumers, and are important food sources for only two insect species. Euphranta connexa females lay eggs in developing fruits of the host plant, with the emerging larva boring through the seeds and killing most of them. Lygaeus equestris is an all-purpose seed predator; both larvae and adults suck on flowers, on developing seeds within the fruits, and on dry seeds they find on the ground up to a year later.

Euphranta connexa female lays eggs in an immature seed pod.

Lygaeus equestra larva feeds on a fallen seed.

Solbreck teamed up with biostatistician Jonas Knape to analyze his data. From the beginning of the study, Solbreck suspected that annual variation in weather – particularly rainfall – might influence Vincetoxicum seed production, and consequent population growth of the two insect species. They discovered something quite unexpected; the dynamics of seed production shifted dramatically in the second half of the study, alternating annually from very high to very low production over that period. This dynamic shift coincides with the extension of the growth season as a result of climate change.

Seed pod abundance by year.

The researchers argue that there is a non-linear negative feedback relationship of the previous year’s seed production on the current year’s seed production. Negative feedback occurs when an increase in one factor or event causes a subsequent decrease in that same factor or event. In this case, an increase in seed production uses up plant resources, leading to a decrease in seed production the following year. But the effect is non-linear, and does not come into play unless Vincetoxicum produces a huge number of seeds, as shown by the graph below,

Seed production in the current year in relation to seed production in the previous year. Note that both axes are logarithmic. The curve represents the expected seed pod density generated by the statistical model, with the shaded area representing the 95% credible intervals. Open circles are data for 1977-1996, while closed circles are data for 1997-2016.

The researchers also found that high rainfall in June and July increased seed production.

So how do these wild fluctuations in seed production affect insects and the plant itself? One important finding is that in high seed production years, the proportion of seeds attacked by insects plummets because the sheer number of seeds overwhelms the seed-eating abilities of the insect consumers. Ecologists describe this phenomenon as predator satiation.

Seed predation rates in relation to seed pod density. Note that both axes are logarithmic. The curve represents the expected predation rate generated by the statistical model, with the shaded area representing the 95% credible intervals. Points are E. connexa predation rates while triangles are combined predation by both insect species.

As a result of predator satiation, there were, on average, seven times as many healthy (unattacked) seed pods in 1997-2016 than there were in 1977-1996. Presumably, this increased number of healthy seeds translates to an increase in new plants becoming established in the area. An important takehome message is that the entire dynamics of an ecosystem can change as a result of changes to the environment, in this case, climate change. More long-term studies are needed to evaluate how common these shifting dynamics are likely to become in the novel environmental conditions we humans are creating.

note: the paper that describes this research is from the journal Ecology. The reference is Solbreck, Christer and Knape, Jonas (2017), Seed production and predation in a changing climate: new roles for resource and seed predator feedback?. Ecology, 98: 2301–2311. doi:10.1002/ecy.1941. 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.

Powdery parasites pursue pedunculate oak

September 14, 2017 by fredsingerecology

Studying disease transmission is tricky for many reasons. Most humans frown on what might seem like the easiest experimental protocol – release a disease into the environment and watch to see how it spreads. For his doctoral dissertation in 2006, Ayco Tack settled on a different experimental protocol – bring the potential hosts to the disease. In this study, staged in Finland, the hosts were pedunculate oak trees, Quercus robur, and the disease was the powdery mildew parasite, Erysiphe alphitoides. Almost 10 years later, Adam Ekholm continued research on the same system, with Tack as his co-supervisor.

Trees on the move. Credit: Ayco Tack.

But before moving trees around, the researchers first needed to see how the disease moved around under field conditions. Within a tree stand, powdery mildew success will depend on how many trees it occupies, how many trees it colonizes in the future, and how many trees it disappears from (extinction rate). The researchers measured these rates over a four year period (2003 – 2006) on 1868 oak trees situated on the island of Wattkast in southwest Finland. They also measured spatial connectivity of each tree to others in the stand. In this case connectivity is a measure of the distance between a tree and other trees, weighted by the size of the other trees. So a tree that has many large neighbors nearby has high connectivity, while a tree with a few distant and mostly small neighbors has low connectivity. Results varied from year-to-year, but in general, the researchers found higher infection rates, lower extinction rates, and some evidence of higher colonization rates in trees with high connectivity.

Oak leaf infected with powdery mildew parasite. Credit: Adam Ekholm.

The importance of connectivity indicated that the parasites simply could not disperse efficiently to distant trees. But perhaps the environment might play a role in colonization rates as well. For example, fungi like powdery mildew tend to thrive in shady and humid environments. Thus a tree out in the open might resist colonization by powdery mildew more effectively than would a tree deep in the forest. To test this hypothesis, Tack and his colleagues placed 70 trees varying distances (up to 300 meters) from an infected oak stand. On one side of the oak stand was an open field, while the other side was closed forest. Thus two variables, distance and environment, could be investigated simultaneously.

Ayco Tack inspecting a potted tree_Tomas Roslin

Ayco Tack inspects an oak tree placed in an open field. Credit: Tomas Roslin.

The researchers collected infection data twice; once in the middle of the growing season (July) and a second time at the end of the growing season (September). Not surprisingly, infection rates were higher by the end of the growing season. In general, infection rates, and infection intensity (mildew abundance) were higher in the forest than in the field, indicating a strong environment effect. In the July survey, trees further from the oak stand had lower infection intensity, but as infection rates increased over the course of the season, the effects of distance diminished, particularly in the forest.

Upper two graphs show the impact of habitat type on (a) proportion of trees infected and (b) mildew abundance. The lower two graphs are the influence of distance from parasite source on mildew abundance of trees set in (c) a forest habitat and (d) an open field. Mildew abundance was scored on an ordinal scale with 0 = none and 4 = very abundant.

Ten years later, Adam Ekholm, as part of his PhD dissertation that studies the effect of climate on the insect community on oak trees, added a third element to the mix – the influence of genes on disease resistance. He wondered whether certain genotypes were more resistant to powdery mildew infection. The researchers grafted twigs from 12 large “mother” trees, creating 12 groups of trees, with between 2 – 27 trees per group (depending on grafting success). Each tree in a given group was thus genetically identical to all other trees within that group.

Oak tree placed in the forest. Credit: Ayco Tack.

The researchers chose a site that contained a dense stand of infected oaks, but was surrounded by a grassy matrix that contained only an occasional tree. To study the impact of early season exposure, Ekholm and his colleagues divided the trees into two groups; 128 trees were placed in the matrix at varying distances from the infected stand, while 58 trees were placed directly in the midst of the stand for about 50 days, and then moved varying distances away. The researchers scored trees for infection at the end of the growing season (mid-September).

Trees that spent 50 days within the oak stand had much higher infection frequency and intensity than trees that were initially placed in the matrix. Some genotypes (for example genotype I in graphs C and D below) were much more resistant to infection than others (such as genotypes D and J). Finally trees further from the source of infection were less susceptible to become colonized over the course of the summer (data not shown).

Proportion of trees infected (A) and proportion of leaves infected (B) in response to early season exposure to stand of oaks infected with the powdery mildew parasite (oak stand) or no early season exposure (matrix). Proportion of trees infected (C) and proportion of leaves infected (D) in relation to tree genotype. Genotypes are labeled A – L; numbers in parenthesis are sample size for each group.

These findings illustrate how dispersal, host genotype and the environment influence the spread of a parasite under natural conditions. The parasite exists as a metapopulation – a group of local populations inhabiting networks of somewhat discrete habitat patches. Some populations go extinct while others successfully colonize each year, depending on distance from a source, tree genotype and environment. Ekholm and his colleagues encourage researchers to use similar experimental approaches in other host-parasite systems to evaluate how general these findings are, and to explore how multiple factors interact to shape the dynamics of disease transmission.

note: the paper that describes this research is from the journal Ecology. The reference is Ekholm, Adam; Roslin, Tomas; Pulkkinen, Pertti and Tack, Ayco. J. M. (2017). Dispersal, host genotype and environment shape the spatial dynamics of a parasite in the wild. Ecology. doi:10.1002/ecy.1949. The paper should come out in print very soon. Meanwhile you can also link to Dr. Tack’s website at www.plantmicrobeinsect.com 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.

Is your goose cooked? Climate change and phenological mismatch.

September 6, 2017 by fredsingerecology

As an undergraduate at the University of Manitoba, Megan Ross investigated nutrient reserves stored up by Lesser Snow Geese before reproduction in southern Manitoba. These reserves of fat and protein are critical to female geese, who then fly thousands of kilometers north to breeding grounds above the Arctic Circle, where they lay eggs and raise their young. For her Master’s thesis (this study), Ross investigated how nutrient levels influence adult reproductive success and recruitment of new goslings into the population.

Lesser Snow Goose on its nest. Credit: Megan Ross

As climates become warmer and more variable, there is a danger that goose reproduction may fall out of synchrony with the availability of high quality food in the feeding grounds – a phenomenon called phenological mismatch. If eggs don’t hatch until substantially after the grass is well-established, then grass nutritive value may not be high enough to raise a goose family. The problem is that even if geese had the ability to adjust the timing of their migration, it would be very difficult for them to know what feeding conditions are like thousands of kilometers away. Ross and her colleagues explored several questions regarding phenological mismatch and how successfully Snow Geese and Ross’s Geese (a smaller relative of Snow Geese – not named after our senior author) raise their broods.

Ross’s Goose paddling about. Credit: DickDaniels (http://carolinabirds.org/)

Those of you who hang out near ponds, golf courses, or farms probably know that goose populations are thriving. Over the past few decades, geese at Karrak Lake in Nunavut, Canada, have increased sharply in population, though the growth rate has leveled off in recent years (see graph below).

Combined estimate of Ross’s Goose and Lesser Snow Goose population size at Karrak Lake. Credit: Megan Ross.

Measuring recruitment of goslings into a population of a million birds is not the easiest task. The researchers used helicopters to herd the birds into portable geese corrals, and then simply calculated the proportion of juveniles as their measure of recruitment. They also weighed, measured and banded all of the captured birds before releasing them, unharmed back into the environment. For each year of the study, they calculated phenological mismatch as the difference between the mean annual hatch date and the NDVI₅₀ date (which stands for the date of 50% annual maximum Normalized Difference Vegetation Index). To calculate NDVI₅₀, researchers use satellite images to estimate the date at which the environment achieved 50% of maximum green-up for the year.

Small portion of the goose population near Karrak Lake. Credit: Megan Ross

Several factors were related to recruitment. For both species, recruitment was very low in years with considerable phenological mismatch (Graph a). High recruitment was associated with high levels of protein in both species (Graph b), and high levels of fat in snow geese (Graph d). Recruitment was also greatest if nests were initiated early in the year (Graph c).

Mean annual values for Ross’s Geese (gray circles) and Lesser Snow Geese (black circles) in relation to (a) phenological mismatch, (b) female body protein index, (c) ELI (early late index) – a measure of nest initiation date (for example, ELI = -5 means that nests were initiated 5 days earlier than average on that particular year), and (d) female body fat index.

The number of eggs per clutch, and the number of nests that produced at least one gosling (nest success) were highest when geese initiated their nests earlier in the year. Snow Geese laid, on average, more eggs, than did Ross’s Geese, but Ross’s Geese had somewhat higher nesting success than did Snow Geese. But nutrients also figure into this increasingly complex picture. In years when females stored up more protein, they tended to lay more eggs.

Three Lesser Snow Goose goslings huddle together. Credit: Megan Ross.

Not surprisingly, the researchers also demonstrated that warmer springs were associated with earlier vegetation growth (NDVI₅₀). The geese were able to adjust somewhat to earlier NDVI₅₀ by initiating nests earlier in the year. However, these adjustments were only partial at best, so that phenological mismatch was very high in years that greened-up early (the distance along the x-axis between the data points and the bold dotted line in the graph below).

Mean annual hatch date for Ross’s Geese (gray circles) and Lesser Snow Geese (black circles) in relation to the date of the year that NDVI₅₀ is reached. The bold dotted line is the expected value if there were no phenological mismatch.

From these data, you might ask why don’t the geese migrate earlier in the spring? One problem is that they need enough protein and fat to migrate, to produce eggs and to incubate the eggs during the cool Arctic spring. Another part of the problem is that gonadal development is determined by day length – not temperature – so there is a limit to how early in the year the geese are able to begin courtship and breeding activities. The concern is that if, as expected, environmental warming continues, phenological mismatch could become more extreme, further reducing juvenile recruitment, and putting a seemingly robust population at risk.

note: the paper that describes this research is from the journal Ecology. The reference is Ross, Megan V., Alisauskas, Ray T., Douglas, David C. and Kellett, Dana K. (2017), Decadal declines in avian herbivore reproduction: density-dependent nutrition and phenological mismatch in the Arctic. Ecology, 98: 1869–1883. doi:10.1002/ecy.1856. 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.

Subsidized Shorelines: where pelagic meets benthic

August 29, 2017 by fredsingerecology

Chris Harrod met his wife, Christina Dorador, while both were working at the Max Planck Institute for Limnology in Germany. Subsequently Dorador began a postdoctoral position in her native Chile, and Harrod went for a visit over Christmas, 2007. He was impressed by the beautiful rocky inshore habitat that was dominated by kelp forests and many species of invertebrates and fish.

Rocky shoreline near Tocopilla, Chile. Credit: Chris Harrod.

As a fisheries biologist, Harrod soon immersed himself in the inshore kelp forest-dominated ocean, and was stunned by the sheer volume of stuff floating around. The water was green rather than blue, and filled with decaying phytoplankton and zooplankton. Where did all this stuff come from? Harrod knew that off the Peruvian and north Chilean coasts, prevailing winds move surface waters away from the shoreline, inducing upwelling of deeper nutrient-rich waters to the surface. This nutrient flux is the basis of a huge anchoveta fishery, which feeds humans, fish, marine invertebrates and marine mammals. He wondered whether the mass of floating debris in the inshore habitat might originate from offshore waters brought in from upwelling, and if the debris actually fueled some of the larger fish and molluscs that dominate inshore kelp forests. The prevailing opinion was that the energy for these fish and molluscs originated from the inshore photosynthetic kelp, rather than from photosynthetic phytoplankton further offshore that get their nutrients from upwelling.

Two bilagay, Cheilodactylus variegatus, swim among green algae in a debris-laden inshore habitat off the coast of Chile. Credit: Chris Harrod.

While you can ask a fish or mollusc what they had for dinner, it is very difficult to get them to respond. Fortunately, ecologists can use stable isotope ratios – the ratio of a rare (and nonradioactive) isotope of an element to its standard common isotope – to help get the answers they need. Harrod collaborated with several researchers in this study, including his Master’s student, Felipe Docmac, who collected and analyzed much of the data and was the first author of the paper. Docmac and his colleagues used the ratio of heavy and light isotopes of carbon (C) and nitrogen (N) to calculate d¹³C (the ratio of ¹³C to ¹²C) and d¹⁵N (the ratio of ¹⁵N to ¹⁴N) to infer where inshore fish were getting their energy.

The basic question was whether the nutrients supporting the food web were primarily from pelagic or benthic sources. In this case, the pelagic source refers to phytoplankton from the offshore areas of upwelling, while the benthic source refers to kelp and green algae that grow on the bottom (benthos) of the inshore habitat. Docmac and his colleagues collected invertebrates and large fish from five different sites along the north Chilean Coast, and calculated ¹³C and ¹⁵N values from tissue samples. Invertebrates were divided into two groups: filter-feeders were represented by mussels, which fed on suspended materials (such as the prolific floating debris), while benthic grazers were gastropods (snails) that fed on benthic kelp and green algae.

Five collection sites along the northern coast of Chile.

I’m going to skip the precise details of how stable isotope analysis actually works; I’ll provide enough information so you can understand the findings. There are two important facts to keep in mind. First an animal’s stable isotope ratio is influenced by the stable isotope ratio of its food source. So an animal feeding on prey with high d¹³C and d¹⁵N will itself have higher stable isotope ratios than will an animal feeding on prey with lower d¹³C and d¹⁵N. Second, the stable isotope ratio increases as we go up the food chain in a predictable manner, because the lighter isotopes of carbon and nitrogen tend to be more readily excreted than are the heavier isotopes.

We are now ready to look at the data. First, notice that while there is some variation from location to location, the (Pelagic) mussels tend to have consistently lower d¹³C values than do the (Benthic) gastropods (X-axis of graph), but fairly equivalent d¹⁵N values (Y-axis of graph). The benthivorous fish have, as we would expect from animals higher up the food chain, much higher d¹⁵N values than either of the invertebrates. But here is the key. The benthivorous fish have a much lower d¹³C value than do the benthic invertebrates (gastropods). If gastropods (and presumably other grazers) were in the benthivorous fish food chain, then we would expect the fish to have a higher d¹³C value than do the benthic gastropods. The researchers thus conclude that these fish are deriving most of their energy from the pelagic debris that is washing in from ocean currents.

d¹³C (X-axis) and d¹⁵N (Y-axis) stable isotope values in benthivorous fish (black circles). Bars emanating from each point indicate 95% confidence intervals (CI). Numbers inside symbols indicate the site of origin for each sample (see map above), Also shown are values for filter-feeding mussels (red up-pointing triangles) and grazing gastropods (blue down-pointing triangles). Gray lines indicated predicted values of diets that were based solely (100%) on pelagic or benthic sources.

The researchers were stunned by these findings. Going into the study, Harrod did not know what he would find, but would not have been surprised by a 15% contribution from pelagic sources, or maybe even 30%. But he was blown away that the data indicated estimates of greater than 90% pelagic contribution at most of the sites. Ecologists have long known that one ecosystem may subsidize a second ecosystem with resources. For example, salmon carcasses can provide nutrient subsidies to trees near riverways, or even deeper into the forest after being transported by bears. But the extent of the subsidy in this study is unprecedented. Docmac and his colleagues urge researchers to explore exactly how the pelagic materials get into the food web, and to see whether such subsidies are common near other upwelling zones worldwide so that coastal resources can be managed more effectively.

note: the paper that describes this research is from the journal Ecology. The reference is Docmac, Felipe, Miguel Araya, Ivan A. Hinojosa, Cristina Dorador, and Chris Harrod. 2017. Habitat coupling writ large: pelagic‐derived materials fuel benthivorous macroalgal reef fishes in an upwelling zone. Ecology doi:10.1002/ecy.1936. It was published online on Aug. 2, 2017, and should appear in print very soon. 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.

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