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.

Climate changes a bird’s life in shrinking grasslands

Back in graduate school, a couple of my grad student buddies and I would get together to fish for brown trout in the Kinnickinnic River in western Wisconsin.  We were students at the University of Minnesota (Twin Cities), but the Kinni was the closest trout stream.  Tired of catching small brown trout, we consulted a trout fishing map and discovered that the headwaters of the Kinni were rich in brook trout. So early one morning, map in hand, we followed strange paths and found our sacred brook trout haven. Alas, the only thing it was rich in was corn, now about two feet high – though there was a modest depression where trout waters once had flowed. Our personal depression was perhaps more than modest – having been robbed of brook trout, and the opportunity to experience some pristine waters flowing through a beautiful grassland.

Grasslands, one of the biomes native to parts of Wisconsin and Minnesota, are globally one of the most endangered biomes, because they usually are relatively easy to convert into farmland and suburban developments. Native grasslands harbor a wide biological diversity; consequently conservation biologists are concerned about their continued loss.

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Cool-season grassland in southwest Wisconsin. Credit: John Dadisman.

Ben Zuckerberg, Christine Ribic and Lisa McCauley wanted to know how environmental factors influenced the nesting success of grassland birds, in particular, because as obligate ground nesters, they might be susceptible to changing  weather conditions that will be affecting the climate in coming decades.  A nest built on the ground is much less insulated from the environment than one built in or on a tree or even a ledge.

Bobolink 7 days (Carolyn Byers)

Seven day old bobolink chicks in a ground nest. Credit: Carolyn Byers.

Zuckerberg and his colleagues used Google Scholar and the ISI Web of Science to comb the literature (1982-2015) for studies that explored the nest success of obligate grassland birds in the United States. They identified 12 bird species from 81 individual studies of 21,000 nests. Based on their experience and the literature, both precipitation and temperature were likely to influence nest success, which is the proportion of nests that fledge at least one young. They considered three precipitation time periods: (1) Bioyear – previous July through April of the breeding season, (2) May of the breeding season, (3) June – August of the breeding season. They considered breeding season temperatures during May, and during the period from June-August. The researchers were also interested in the size of the grassland (grassland patch size), reasoning that a larger grassland might provide more diverse microclimates, so, for example, a bird might be able to find a dry microhabitat for nesting in a large grassland, even in a wet breeding season.

ZuckFig1

Map of the identity and location of species considered for this study.

The researchers discovered that both temperature and precipitation were important.  Nest success increased steadily with bioyear precipitation (Figure (a) below).  Presumably, more rain led to more plant growth and more insect survival, which would help feed the young.  Taller plants could also help shade or hide the nests. In contrast, nest success declined sharply with precipitation during spring and summer of the breeding season (Figure (b) and (c)). Heavy rains during the breeding season can flood nests, and also decrease the foraging efficiency of parents who might need to spend more time incubating nests during rainstorms. Lastly, extreme (low or high) May temperatures depressed nest success, which was highest at intermediate temperatures (Figure (d)). Egg viability depends on maintaining a constant temperature, and the parents may be more challenged to thermoregulate at extreme temperatures.  Temperatures later in the breeding season did not affect nest success.

ZuckFig2

Effects of (a) bioyear precipitation (previous July – April of the breeding season), (b) May precipitation during the breeding season, (c) June – August precipitation during the breeding season, and (d) May temperature on nest success. Shaded area represents 95% confidence interval.

But all is not straightforward in the grassland nest success world. These main findings about precipitation and temperature interacted with grassland size in interesting ways.  For example high bioyear precipitation, which overall increased nest success, only did so for smaller grassland patches (dashed line in top graph below), but not for larger patches (solid line).  Extreme May temperatures had different effects on nest success in relation to grassland patch size.  Low May temperatures were associated with high nest success in small patches (dashed line in bottom graph) and with low nest success in large patches (solid line).  High May temperatures were associated with high nest success in large patches, and with low nest success in small patches.

ZuckFig3

Predicted nest success of grassland birds in relation to bioyear precipitation (top graph) and May temperature (bottom graph) in relation to grassland patch size.  Solid lines represent large grasslands, while dashed lines represent small grasslands.  Shaded area is 95% confidence interval.

The researchers were surprised to discover that patch size affected how weather influenced grassland bird nesting success. Some of the patterns seem intuitively logical; for example, in unusually hot breeding seasons birds had higher nest success in larger grasslands than in smaller grasslands.  Presumably, birds were more likely to find a cooler microclimate for their nests in a large grassland.  However it is puzzling why in unusually cold breeding seasons birds had higher nest success in smaller grasslands. The researchers are planning a follow-up study to better document and measure the existence of microclimates in grasslands of different sizes, and explore how different microclimates influence the nesting success of vulnerable grassland birds.  Finding that warmer temperatures and drought generally reduce nest success to the greatest extent in small grassland patches is strong incentive for conservation mangers to establish large core grasslands as a tool to maintain bird populations in the wake of present and future changes to the climate.

note: the paper that describes this research is from the journal Conservation Biology. The reference is Zuckerberg, B. , Ribic, C. A. and McCauley, L. A. (2018), Effects of temperature and precipitation on grassland bird nesting success as mediated by patch size. Conservation Biology, 32: 872-882. doi:10.1111/cobi.13089. Thanks to the Society for Conservation Biology for allowing me to use figures from the paper. Copyright © 2018 by the Society for Conservation Biology. All rights reserved.