Hot ants defend plants from elephants

I’ve lost a lot of sleep over ants.  As a spider researcher, I often placed ants on spiderwebs to lure my spiders out of their underground retreats and onto their webs. The problem was that these harvester ants (Pogonmyrmex species) were fierce, so to minimize damage to myself, I was forced to capture them in the very early morning, when they and (alas) I were very sluggish.

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Swollen thorn (domatia) that serves as living quarters for acacia ants. Credit: T. Palmer.

Todd Palmer has worked with ants for many years, including research on ant-plant mutualisms in which acacia trees provide domatia (swollen thorns) as ant living quarters and extrafloral nectaries as ant food, while ants provide protection from herbivores such as elephants, kudus and steenboks.

Similar to my efforts with ants and spiders, Palmer wanted to reduce ant-induced damage to himself and his colleagues, so he often took advantage of early morning ant sluggishness for purposes of manipulating acacia trees. On the other hand, if he wanted to study aggressive responses, he learned that mid-day was best. Recognizing the daily patterns of ant activity got Palmer, Ryan Tamashiro (Palmer’s undergraduate research student) and Patrick Milligan (Palmer’s graduate student) thinking about how these different levels of activity would influence herbivores, many of which tend to be most active during dawn and dusk when temperatures are low and ants are relatively sluggish.

Elephant side

Elephants are major herbivores that can cause enormous damage to acacia trees. Credit: T. Palmer.

Four species of ants live in domatia on branches of Acacia drepanolobium, the dominant tree species at Mpala Research Centre in Laikipia, Kenya.

Acdr habitat

A grove of Acacia drepanolobium. Credit: T. Palmer.

In order of relative abundance, the ant species are Crematogaster mimosae (52%), C. sjostedti (18%), Tetraponera penzigi (16%) and C. nigriceps (15%).  Previous research showed that C. mimosae and C. nigriceps are the two most effective acacia defenders.

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Crematogaster nigriceps on an acacia tree. Credit: T. Palmer.

Ants are poikilotherms, whose body temperature, and presumably their activity levels, fluctuate with environmental temperature.  As these ants live in acacia branches, the first order of business became to determine how branch temperature fluctuated with time of day during the 21 days of data collection.  Not surprisingly, branch temperature peaked at mid-day, and was lowest at dawn and dusk (temperatures were not measured during the night).

TamashiroFig S!

Variation in branch surface temperature with time of day. Horizontal bars are median values; boxes are first and third quartiles.

Tamashiro, Milligan and Palmer next asked how ant activity level related to branch temperature.  Different ant species don’t get along so well, so each tree hosted only one ant species.  For each tree surveyed, the researchers counted the number of ants that passed over a 5 cm branch segment during a 30 second time period (they did this twice for each tree),  The researchers discovered a strong correlation between branch surface temperature and baseline ant activity, with C. mimosae and C. nigriceps showing greatest activity levels at all temperatures, which increased sharply at higher temperatures.

TamashiroFig 1a

Ant activity levels in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

Do higher temperatures cause a stronger aggressive response to predators or other disturbances? Tamashiro and his colleagues tested this by rapidly sliding a gloved hand over a 15 cm segment of a branch three times and then resting the gloved hand on the branch for 30 s.  They then removed the glove and counted the number of ants that had swarmed onto the glove.  Again, C. mimosae and C. nigriceps showed the strongest aggressive response, which increased sharply with temperature

TamashiroFig 1b

Aggressive swarming by ants in relation to branch surface temperature. Shaded areas are 95% confidence intervals for each species.

While a gloved hand is a nice surrogate for predators, the researchers wanted to know how the ants would respond to a real predator, and whether the response was temperature dependent.  At the same time, they wanted to determine whether the predator would change its behavior in response to changes in ant defensive behavior at different temperatures.  They used eight somali goats (Capra aegagrus hircus) as their predators, and C. mimosae as the focal ant species for these trials.

Cpl. Paula M. Fitzgerald, USMC - United States Department of Defense

Somali goats in Ali Sabieh, Djibouti. Credit: Cpl. Paula M. Fitzgerald, USMC – United States Department of Defense.

The researchers chose eight trees of similar size for their experiment, and removed ants from four of the trees by spraying them with a short-lived insecticide, and preventing ant recolonization by spreading a layer of ultra-sticky solution (Tanglefoot) around the based of each treated tree.  Goats were allowed to feed for five minutes.

TamashiroFig2

Number of bites (top graph) and time spent feeding (bottom graph) by goats in relation to branch surface temperature. Shaded area is 95% confidence interval.

Tamashiro and his colleagues measured the number of bites taken (top graph) and the amount of time spent feeding (bottom graph) at different branch temperatures.  Both measures of goat feeding were not influenced by branch temperature if there were no ants on the trees (blue lines and points).  But if ants were present (red lines and points), goat feeding decreased sharply with increasing branch temperature, presumably reflecting more aggressive ant defense of the plants.

These findings have important implications for acacia trees, which are a critical species in the sub-Saharan ecosystem.  Previous research has shown that elephant damage is strongly influenced by the number of swarming ants on a particular tree; a greater number of swarming ants are associated with less elephant damage. Many vertebrate browsers feed throughout the day, but may feed preferentially at dawn and dusk, when temperatures are cooler and ant-defense is weakest. Browsing is particularly problematic for acacia saplings, which are usually attacked by small-bodied vertebrates such as steenbok, which forage primarily at night when ants are least active.  Thus the effectiveness of ant defense may be compromised by mismatches between vertebrate activity periods and ant activity periods.

note: the paper that describes this research is from the journal Ecology. The reference is Tamashiro, R. A., P. D. Milligan, and T. M. Palmer. 2019. Left out in the cold: temperature-dependence of defense in an African ant–plant mutualism. Ecology 100(6): e02712. 10.1002/ecy.2712 . Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2019 by the Ecological Society of America. All rights reserved.

 

 

Sweltering ants seek salt

Like humans, ants need salt and sugar.  Salt is critical for a functioning nervous system and for maintaining muscle activity, while sugar is a ready energy source. In ectotherms such as ants, body temperature is influenced primarily by the external environment, with higher environmental temperatures leading to higher body temperatures.  When ants get hot their metabolic rates rise, so they can go out and do energetically demanding activities such as foraging for essential resources like salt and sugar. On the down side, hot ants excrete more salt and burn up more sugar.  In addition, like humans, very high body temperature can be lethal, so ants are forced to seek shelter during extreme heat.   As a beginning graduate student, Rebecca Prather wanted to know whether ants adjust their foraging rates on salt and sugar in response to the conflicting demands of elevated temperatures on ants’ physiological systems.

Prather at field site

Rebecca Prather at her field site in Oklahoma, USA. Credit: Rebecca Prather.

Prather and her colleagues studied two different field sites: Centennial Prairie is home to 16 ant species, while Pigtail Alley Prairie has nine species.  For their first experiment, the researchers established three transects with 100 stations baited with vials containing cotton balls and either 0.5% salt (NaCl) or 1% sucrose.  The bait stations were 1 meter apart.  After 1 hour, they collected the vials (with or without ants), and counted and identified each ant in each vial.  The researchers measured soil temperature at the surface and at a depth of 10 cm. The researchers repeated these experiments at 9 AM, 1 PM and 5 PM, April – October, 4 times each month.

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Ants recruited to vials with 0.5% salt solution.  Credit: Rebecca Prather.

Sugar is easily stored in the body, so while sugar consumption increases with temperature, due to increased ant metabolic rate, sugar excretion is relatively stable with temperature.  In contrast, salt cannot be stored effectively, so salt excretion increases at high body temperature.  Consequently, Prather and her colleagues expected that ant salt-demand would increase with temperature more rapidly than would ant sugar-demand.

PratherFig1

Ant behavior in response to vials with 0.5% salt (dark circles) and 1% sucrose (white circles) at varying soil temperatures at 9AM, 1 PM (13:00) and 5PM (17:00). The three left graphs show the number of vials discovered (containing at least one ant), while the three right graphs show the number of ants recruited per vial.  The Q10 value  = the rate of discovery or recruitment at 30 deg. C divided by the rate of discovery or recruitment at 20 deg. C. * indicates that the two curves have statistically significantly different slopes.

The researchers discovered that ants foraged more at high temperatures. However, when surface temperatures were too high (most commonly at 1 PM during summer months), ants could not forage and remained in their nests.  At all three times of day, ants discovered more salt vials at higher soil temperatures. Ants also discovered more sugar vials at higher temperatures in the morning and evening, but not during the 1 PM surveys. Most interesting, the slope of the curve was much steeper for salt discovery than it was for sugar discovery, indicating that higher temperature increased salt discovery rate more than it increased sugar discovery rate (three graphs on left).

When ants discover a high quality resource, they will recruit other nestmates to the resource to help with the harvest.  Ant recruitment rates increased with temperature to salt, but not sugar, indicating that ant demand for 0.5% salt increased more rapidly than ant demand for 1% sugar (three graphs above on right).

The researchers were concerned that the sugar concentrations were too low to excite much recruitment, so they replicated the experiments the following year using four different sugar concentrations.  Ant recruitment was substantially greater to higher sugar concentrations, but was still two to three times lower than it was to 0.5% salt.

PratherFig2

Ant recruitment (y-axis) to different sugar concentrations at a range of soil temperatures (X-axis). Q10 values are to the left of each line of best fit.

Three of the four most common ant species showed the salt and sugar preferences that we described above, but the other common species, Formica pallidefulva, actually decreased foraging at higher temperatures.  The researchers suggest that this species is outcompeted by the other more dominant species at high temperatures, and are forced to forage at lower temperatures when fewer competitors are present.

In a warming world, ant performance will increase as temperatures increase up to ants’ thermal maximum, at which point ant performance will crash.  Ants are critical to ecosystems, playing important roles as consumers and as seed dispersers. Thus many ecosystems in which ants are common (and there are many such ecosystems!) may function more or less efficiently depending on how changing temperatures influence ants’ abilities to consume and conserve essential nutrients such as salt.

note: the paper that describes this research is from the journal Ecology. The reference is Prather, R. M., Roeder, K. A., Sanders, N. J. and Kaspari, M. (2018), Using metabolic and thermal ecology to predict temperature dependent ecosystem activity: a test with prairie ants. Ecology, 99: 2113-2121. doi:10.1002/ecy.2445Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

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).”

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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.

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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.

KarbanFig4

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.

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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.

KarbanFig7A

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.

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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!

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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.

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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.

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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.

SensenigFig2

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.

SensenigFig4

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.

SensenigFig6

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.