Cat and fox: agents of Australian extinctions

Australia’s drylands are famous for their assemblage of ultra-cool mammals. As one example, it is difficult for us non-Australians to imagine a more endearing creature than the rock-wallaby pictured below.

Black-foted Rock-wallaby

Black-footed rock wallaby. Credit: Peter McDonald.

Unfortunately, numerous species of Australia’s dryland mammals are going extinct. Many of these extinct species weigh between 35 and 5500 grams – a weight range that researchers have described as the critical weight range (CWR). Peter McDonald and his colleagues wanted to know what was causing these extinctions, and why were they most prevalent in the CWR. They considered two hypotheses. First, perhaps the land was becoming less productive, either from habitat destruction by humans, or as a result of changing climate. Reduced plant abundance could cause herbivorous mammals to go extinct. An alternative hypothesis is that perhaps newly introduced predators, notably feral cats and red foxes, were killing the native mammals so effectively, that they were disappearing from the Ausralian drylands.

Previous research indicated that extinction rates were lower in areas that had more species living in trees and around rocks, leading McDonald to think that maybe habitat was influencing extinctions in important ways. In particular, he realized that rugged mountainous areas might have fewer predacious cats and foxes, and secondly that these two predators tend to go for prey within the CWR. Putting these ideas together, perhaps mountainous areas are refuges for Australia’s dryland CWR species, protecting them from predator-driven extinction. If so, mammal species richness would be highest in rugged, protected areas, and lowest in more open areas. If, on the other hand, mammals are going extinct because overall productivity is declining, we would expect overall species richness to be greatest in the most productive areas.
McDonald and his colleagues tested these two competing hypotheses by censusing mammals in four different types of habitats in Tjoritja National Park within the MacDonnell Range of central Australia. These were (1) mountain areas dominated by a sparse assemblage of shrubs and clumps of spinifex grass, (2) spinifex grasslands (with a more abundant cover of spinifex than found in the mountains), (3) Acacia shrublands, and (4) alluvial woodlands, which were most productive with richest soils.

 

 

Mountain refuge habitat_PeterMcDonald

Mountains. Credit: Peter McDonald

 

spinifex

Spinifex grasslands

acacia

Acacia shrubland

alluvial

Alluvial woodland

The researchers set up a variety of different mammal traps in 90 different sites representing these four habitats to capture and identify small mammals, and they detected larger mammals by searching for fresh scat at each site. The researchers estimated productivity with the normalized difference vegetation index (NDVI), which uses satellite imagery to measure the green-ness, and hence productivity, of a site or region.

In support of the predation hypothesis, more mammal species were found in the most rugged terrain.

McDonaldFig1A

Number of mammal species per site in relation to ruggedness of terrain. The curve is the fitted value of the regression equation.  The shaded area represents the 95% confidence interval.

In contrast to the productivity hypotheses, fewer mammal species were found in the most productive sites

McDonaldFig1c

Number of mammal species per site in relation to productivity of terrain as measured by the NDVI. The curve is the fitted value of the regression equation.  The shaded area represents the 95% confidence interval.

While it’s useful to evaluate both hypotheses by measuring current species richness, the researchers also needed to know how many species were actually driven to extinction in the time since cats and foxes invaded. They reconstructed historic species richness for each habitat based on subfossil remains (remains of organisms that are only partially fossilized), from indigenous knowledge supplied by aboriginal Australians, and from historical accounts in the early literature.

They discovered that CWR extinctions were most prevalent in alluvial (12/12 species) and acacia (7/7 species) habitats. Spinifex habitas lost 5/6 CWR species, while mountainous habitats only lost 2/6 CWR species. Importantly, species outside of the CWR have survived relatively well in all habitats, further implicating cats and foxes as the agents of extinctions.

McDonaldFig2

Current (extant) and historic (pre-invasion by cats and foxes) mammalian species richness in the four habitats. The dots are the mean weight, and the lines are the weight ranges for each species.  The shaded area represents the critical weight range (CWR)

More support for the the predation-habitat link comes from recent research that indicates that red foxes are absent from the mountain habitat, while feral cats are substantially less abundant. Even when present, cats are much less efficient hunters in the mountain habitat because the complex rock structure affords more refuges to prey items.

Feral cat with fat-tailed antechinus_NTG

Feral cat captured on camera with a fat-tailed Antechinus. Credit Tony Griffiths.

Across Australia, many CWR species have gone extinct in regions colonized by cats and foxes. McDonald and his colleagues provide solid evidence that these introduced predators are responsible for these extinctions. They urge researchers to explore other mountainous regions in Australia to see if they too are acting as refuges for CWR mammals.

note: the paper that describes this research is from the journal Conservation Biology. The reference is McDonald, P. J., Nano, C. E. M., Ward, S. J., Stewart, A., Pavey, C. R., Luck, G. W. and Dickman, C. R. (2017), Habitat as a mediator of mesopredator-driven mammal extinction. Conservation Biology, 31: 1183–1191. doi:10.1111/cobi.12905. 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.

Changing climate promotes prolific plants and satiated consumers

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

Solbreck1AB

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.

Solbreck2B

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

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

Solbreck2Ayes

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.

solbreck1c.png

Euphranta connexa female lays eggs in an immature seed pod.

Solbreck1D

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.

Solbreck2Cyes

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,

Solbreck3yes

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.

Solbreck4yes

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.

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.