Crawling with caterpillars courtesy of climate change – and ants

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.


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.

Fires foster biological diversity on the African savanna

As an ecology student back in days of yore, I was introduced to the classic mutualism between ants and swollen-thorn acacia trees. In this mutually beneficial relationship, ants protect acacia trees by biting and projecting very smelly substances at hungry herbivores, and by pruning encroaching branches of plant competitors. In return for these services, acacia trees provide the ants with homes in the form of swollen thorns, and in some cases also provide food for their defenders.


Swollen thorns of Acacia drepanlobium occupied by C. nigriceps. Credit: Ryan L. Sensenig.

I always assumed there were limits to what these ants could do. I knew that elephants were a constant problem for trees trying to get established on the African savanna. I figured, wrongly, that ants could not do much to counter a determined thick-skinned elephant. But as Ryan Sensenig describes, ants will swarm any intruding elephant, rushing into the elephant’s very sensitive trunk and mouth, biting it and, in some cases, exuding a chemical compound that is very offensive to an elephant’s keen sense of smell. So don’t mess with these ants if you can help it!


The Laikipia Plateau has one of the few growing elephant populations in East Africa. Credit: Ryan L. Sensenig.

Fires play an important role in savanna ecosystems, killing many trees before they can get established, and creating a mosaic of burned and unburned areas which vary in grass quality and quantity, and in the abundance of acacia trees (and other species as well). Recently burned grasslands tend to be lower in grass abundance and higher in grass nutrient levels. In a previous study of controlled burns, Sensenig and his colleagues showed that larger animals, such as elephants, tended to graze in unburned areas, which had more grass – albeit of lower quality. Returning seven years after the burn, he was surprised to find that elephants, which eat both trees and grass, had shifted to the burned sites in preference to unburned sites. He thus wondered whether fire was having an impact on the ant-acacia mutualisms that defend acacias from elephants and other large herbivores.


Sunset strikes an Acacia xanthophloea on Mpala Research Centre in Laikipia, Kenya. Credit: Ryan L. Sensenig.

Ants do not share trees. In Mpala Research Centre in the Laikipia Plateau of Kenya, there are four mutually-exclusive species of ants that live in Acacia drepanolobium trees: Crematogaster sjostedti, C. mimosae, C. nigriceps, and Tetraponera penzigi.

Sensenig and his colleagues wanted to know whether the controlled burns had a long-lasting effect on ant species distribution on acacia trees. The researchers surveyed 12 plots that had been burned seven years previously and an equal number of unburned plots to see how burns affected which ant species were present.


Goshen College research students estimate ant densities on Acacia drepanolobium trees in the Kenya Longterm Exclosure Experiment. Credit: Ryan L. Sensenig.

They found that C. nigriceps was more common in acacias from burned areas while the other three species were more common in trees from unburned areas.


Why were there more C. nigriceps ants in previously burned areas? One explanation is that perhaps C. nigriceps is better at avoiding getting burned by fire, or else is better at recolonizing after a fire. To look for species difference in response to fire, the researchers simulated fires by burning elephant dung and dried grass in 3-gallon metal buckets, creating a small sustained smoke source. They stationed observers every 50 meters along a 500 meter transect for the first experiment, and a 1.8 km transect for the second experiment. They then measured ant-evacuation rate by counting the number of ants moving down the trunk. There were some very pronounced differences, with C. nigriceps having the highest evacuation rate, C. mimosae also showing a strong smoke response, and the other two species showing little evidence of any response.


Evacuation rate for each species in response to smoke.

C. mimosae generally prevails when it battles a colony of C. nigriceps. These results indicate that the subordinate C. nigriceps is able to maintain its presence in the community, in part, by taking advantage of its superior performance when it encounters a fire. The researchers also found some evidence that C. nigriceps is better at recolonizing after a fire than is C. mimosae. So despite being the subordinate species, C. nigriceps is abundant in this ecosystem.

Returning to those elephants, the researchers describe one final experiment in which some plots had a series of fences that excluded herbivores, while other plots were open to herbivores, including elephants.


In this experiment, as well, there were burned and unburned plots. In general, there were more ants present when herbivores were present, as the trees invested more in swollen thorns and in ant food (in the form of nectar) to attract protective ants. In addition, ants were more abundant in unburned plots than in plots that had been previously burned, with the exception of C. nigriceps when herbivores were excluded.

Ecologists have long known that fire maintains savanna ecosystems by preventing the grasslands from being overgrown by trees. This study shows that fires shift ant community structure in favor of the subordinate ant species (C. nigriceps), resulting in a higher diversity of ant species overall. The researchers suggest that if fires become more common in savannas, elephants may become more attracted to acacias that harbor a reduced (or nonexistent) cast of defenders, which could lead to a further reduction in the abundance of acacia trees and their mutualistic ants.

note: the paper that describes this research is from the journal Ecology. The reference is Sensenig, R. L., Kimuyu, D. K., Ruiz Guajardo, J. C., Veblen, K. E., Riginos, C., & Young, T. P. (2017). Fire disturbance disrupts an acacia ant–plant mutualism in favor of a subordinate ant species. Ecology, 98(5), 1455-1464.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.