Successful scavengers

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

Turner1

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.

TurnerFieldSite

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.

Turner5

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.

EcologyFig1Turner

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.

EcologyFig3Turner

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.

vultures_pigcarcass

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.

Life and death in a diminutive ecosystem

Ecosystems are big things, as they encompass an entire community of organisms and the nonliving factors (such as nutrients and water) that interact with the community. So we’re accustomed to thinking about the Serengeti as an ecosystem, as it includes (among many things) the large animals, such as lions, wildebeest and buffalo that live there, the animals and plants they eat, and the soils and nutrients that feed these plants.

But ecosystems can also be tiny. Let’s think about an individual tank bromeliad, Quesnelia arvensis, which can hold up to 3 liters of water in tanks formed where individual leaves come together. Gustavo Romero has identified over 140 species of invertebrates that live within these natural tanks, including large predators such as damselfly and tabanid larvae, and many species of smaller predators (mesopredators) including a diverse group of chironomid midges. The larger predators eat the smaller predators, while predators of both sizes eat a very diverse group of detritivores – animals that feed on the remains of dead organisms. The terrestrial fauna in the immediate vicinity are spiders. Visitors from the surrounding forest ecosystem include 12 bird species and 6 frog species, which forage on larvae within the bromeliads.

Cantorchilus longirostris on bromeliad (Quesnelia arvensis) leaf

Long-billed marsh wren perches on the tip of bromeliad leaf.  This bird can use its long beak to probe for invertebrates living within the bromeliad tank. Credit: Crasso Paulo Bosco Breviglieri

Crasso Paulo Bosco Breviglieri and his colleagues had previously done research demonstrating how insectivorous birds hanging out near bromeliads inhibited dragonflies from ovipositing (laying eggs) within the bromeliad tank. As these birds were much larger than the animals living within the tanks, Breviglieri and Romero hypothesized that the birds would focus on eating the largest items offered to them by this ecosystem. By removing the largest items (the top predators), birds increase the biomass of the prey of these top predators, including detritivores. Thus bird predation should indirectly increase decomposition rate and nutrient availability.

Breviglieri food web

Effects of birds and frogs on bromeliad trophic cascades. Solid arrows are direct effects and dashed arrows are indirect effects (for example frogs eat top predators, thereby indirectly increasing mesopredators).  Wider arrows are stronger effects.

Trophic cascades, a process in which the effects of consumption within an ecosystem cascade down from higher to lower feeding levels, can be difficult to study. The problem is that one favorite approach is to remove predators (the top trophic level) and see if prey abundance increases while the food of these prey decreases, and so on. This is extremely challenging when top predators are lions or wolves and ecosystem area encompasses thousands of kilometers, but much easier when predators are birds or frogs, and each ecosystem is a tank bromeliad. Simply put a cage over a tank bromeliad and presto!, no birds or frogs can get in.

Dr. Crasso Paulo B. Breviglieri building the cages that isolated the bromeliads

Breviglieri with a caged bromeliad. Credit: Jennifer Tezuka

Breviglieri and Romero collected 30 tank bromeliads from the forest, and meticulously cleaned each plant to remove all organisms and organic matter. They filtered and homogenized the water from the bromeliads, and returned 1 liter of water to each plant so that each plant began the experiment with the same quantity of water and microorganisms. The researchers then added equal numbers of organisms to each bromeliad from all of the trophic levels, ranging from apex predators such as damselflies down to detritivores, such as shredders, which eat dead plant leaves and begin the break down process. They also added 10 leaves to each tank for detritivore consumption and further decomposition.

For their experiment, Breviglieri and Romero had three different treatments, with 10 bromeliads per treatment: (1) caged, with each bromeliad enclosed within a steel mesh that allowed insects through but restricted birds and frogs, (2) open-cage control, with each bromeliad only partially enclosed so predators had free access, (3) uncaged control. They returned these to the field at 40 meter intervals, and allowed 155 days to pass.

Larva of zygoptera on bromeliad (Quesnelia arvensis)leaf

Bromeliad with a damselfly larva (top predator) that for unknown reasons has climbed out of the tank onto a leaf.  A bird flew to a nearby perch, but the alert damselfly dove back down into the tank, earning a 9.6 from the judges. Credit: Crasso Paulo Bosco Breviglieri

After 155 days, Breviglieri and Romero collected all of the bromeliads, and identified, counted and weighed (dry weight) all of the organisms. They discovered that the dry mass of invertebrates was much greater in the caged treatments than either control (Figure A). The abundance of apex predators (damselflies and tabanids) did not increase; but the size of individuals increased dramatically (Figure B). Mesopredators increased in abundance (Figure C), while shredder abundance declined sharply (Figure D). Shredder larvae forage on sediment and are a favorite damselfly food item, so it is not surprising that shredders declined, given the sharp increase in damselfly size, and presumably appetite.

BreviglieriFig3ABCD

Lower shredder abundance in the caged bromeliads led to a sharp decline in decomposition rates (left graph below). In theory, this should make fewer nutrients available to the bromeliads and reduce bromeliad growth. In contrast to expectations, caged bromeliads actually grew more leaves (right graph below), despite the reduction in decomposition rates. Breviglieri and Romero remind us that the greater mass of larvae were producing a much greater mass of fecal matter and prey carcasses, both of which are very nutrient rich. Also, higher predation rates can cause some insects to mature and leave their tank at a smaller size, consuming fewer nutrients while in the larval form, and leaving more nutrients for each plant to use for its own growth.

BreviglieriFig3EF

Decomposition rate measured as detrital mass lost (left graph), and growth rate measured as new leaves grown by the bromeliads (right graph), for caged, open-caged and uncaged controls.

Clearly, there are many unanswered questions about this trophic cascade. For example, why don’t the number of top predators increase in abundance when birds and frogs are excluded? When I asked him this question, Breviglieri suggested that two processes could explain this finding. First, top predators eat smaller larvae of their own species. Second, female insects can chemically sense the presence of predators in these bromeliads, and refrain from ovipositing in plants hosting large predators.

Perhaps most important, can we extend the conclusions from these small ecosystems to larger ecosystems? In nature there are many analogous ecosystems in which predators have strategies for crossing boundaries and influencing ecosystem processes. For example, many birds dive into lakes searching for fish and invertebrates. Moving in the opposite direction, banded-archerfish spit out water jets to dislodge invertebrates from adjacent vegetation into the water, and crocodiles leave rivers to grab and consume convenient gnus. In these systems, as in bromeliads, predators cross ecosystem borders to feed, and it is important for us to understand if there are any general patterns in how these visitors from the outside affect ecosystem functioning.

note: the paper that describes this research is from the journal Ecology. The reference is Breviglieri, Crasso Paulo Bosco, and Gustavo Q. Romero. 2017. Terrestrial vertebrate predators drive the structure and functioning of aquatic food webs. Ecology. doi:10.1002/ecy.1881.  It was published online on June 12, and should appear shortly in print. 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.