“Notes from Underground” – cicadas as living rain gauges

Given recent discussions between Donald Trump and Kim Jong-un about whose button is bigger, many of us with entomological leanings have revisited the question of what insects are most likely to dominate a post-nuclear world. Cicadas have a developmental life history that predisposes them to survival in the long term because some species in the eastern United States spend many subterranean years as juveniles (nymphs), feeding on the xylem sap within plants’ root systems. Magicicada nymphs live underground for 13 or 17 years, depending on the species, before digging out en masse, undergoing one final molt, and then going about the adult business of reproduction. This life history of spending many years underground followed by a mass emergence has not evolved to avoid nuclear holocausts while underground, but rather to synchronize emergence of billions of animals. Mass emergence causes predator satiation, an anti-predator adaptation in which predators are gastronomically overwhelmed by the number of prey items, so even if they eat only cicadas and nothing else, they still are able to consume only a small fraction of the cicada population.


Mass Magicicada emergence picturing recently-emerged winged adults, and the smaller lighter-colored exuviae (exoskeletons) that are shed during emergence. Credit: Arthur D. Guilani.

Less well-known are the protoperiodical cicadas (subfamily Tettigadinae) of the western United States that are abundant in some years, and may be entirely absent in others. Jeffrey Cole has studied cicada courtship songs for many years, and during his 2003 field season noted that localities that had previously been devoid of cicadas now (in 2003) hosted huge numbers of six or seven different species. He returned to those sites every year and high diversity and abundance reappeared in 2008 and 2014. This flexible periodicity contrasted with their eastern Magicicada cousins, and he wanted to know what stimulated mass emergence.



Protoperiodical cicadas studied by Chatfield-Taylor and Cole.  Okanagana cruentifera (top) and Clidophleps wrighti (bottom). Credit Jeffrey A. Cole.

Cole and his graduate student, Will Chatfield-Taylor, considered two hypotheses that might explain protoperiodicity in southern California (where they focused their efforts). The first hypothesis is that cicada emergence is triggered by heavy rains generated by El Niño Southern Oscillation (ENSO), a large-scale atmospheric system characterized by high sea temperature and low barometric pressure over the eastern Pacific Ocean. ENSO has a variable periodicity of 4.9 years, which roughly corresponds to the timing Cole observed while doing fieldwork. The second hypothesis recognized that nymphs must accumulate a set amount of xylem sap from their host plants to complete development. Sap availability depends on precipitation, and this accumulation takes several years in arid habitats. So while ENSO may hasten the process, the key to emergence is a threshold amount of precipitation over a several year timespan.

Working together, the researchers were able to identify seven protoperiodical species by downloading museum specimen data (including where and when each individual was collected) from two databases (iDigBio and SCAN). They also used data from several large museum collections, which gave them evidence of protoperiodical cicada emergences back to 1909. Based on these data, Chatfield-Taylor and Cole constructed a map of where these protoperiodical cicadas emerge.


Maps of five emergence localities discussed in this study.

The researchers tested the hypothesis that protoperiodical cicada emergences follow heavy rains triggered by ENSO by going through their dataset to see if there was a correlation between ENSO years and mass cicada emergences. Of 20 mass cicada emergences since 1918, only five coincided with ENSO events, which is approximately what would be expected with a random association between mass emergences and ENSO. Scratch hypothesis 1.

Let’s look at the second hypothesis. The researchers needed reliable precipitation data between years for which they had good evidence that there were mass emergences of their seven species. Using a statistical model, they discovered that 1181 mm was a threshold for mass emergences, and that three years was the minimum emergence interval regardless of precipitation. Only after 1181 mm of rain fell since the last mass emergence, summed over at least three years, would a new mass emergence be triggered.


Cumulative precipitation over seven time periods preceding cicada emergence.

The nice feature of this model is that it makes predictions about the future. For example, the last emergence occurred in the Devil’s punchbowl vicinity in 2014. Since then that area has averaged 182.2 mm of precipitation per year. If those drought conditions continue, the next mass emergence will occur in 2021 at that locality, which is longer than its historical average. Only time will tell. Hopefully Mr. Trump and Mr. Jong-un will be able to keep their fingers off of their respective buttons until then.

note: the paper that describes this research is from the journal Ecology. The reference is Chatfield-Taylor, W. and Cole, J. A. (2017), Living rain gauges: cumulative precipitation explains the emergence schedules of California protoperiodical cicadas. Ecology, 98: 2521–2527. doi:10.1002/ecy.1980. 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.


Languishing Leatherbacks

Leatherback turtles, Dermochelys coriacea, are the largest of all sea turtles, tipping the scales at up to 900 kg. Unlike other sea turtles, the leatherback lacks a carapace covered with scutes; instead its carapace is covered by thick leathery skin that is embedded with small bones forming seven ridges running along its back. This turtle has a wonderful set of anatomical and physiological adaptations, such as huge flippers and an efficient circulatory system, that make it a powerful swimmer and deep ocean diver. Males spend their entire lives at sea, while females usually return to their birthplace along sandy beaches to dig nests and lay eggs.


Leatherback female on the beach at Las Baulas National Park. Credit: Karla Hernández.

Unfortunately, from the perspective of conserving awesome animals in our world, some populations of leatherbacks are declining rapidly, and many are now listed as critically endangered by the IUCN Red List. Pilar Santidrian Tomillo wanted to know why leatherback populations in the Eastern Pacific Ocean have declined so much in recent years. Working at Las Baulas National Park in northwestern Costa Rica since 1993, Tomillo and her colleagues have tagged 1927 nesting females so they could measure survival and return rates to the nesting shoreline. They discovered an alarming trend of sharp decline as described by the graph below.

TomilloFig1Tomillo and her colleagues knew that many leatherbacks were killed every year as a consequence of bycatch – capture by fishing nets or lines cast by fishermen who are targeting other species. But leatherback bycatch is very difficult to monitor accurately, as few fishermen keep accurate records of dead turtles, and turtles may die after being entangled and subsequently freed. The researchers also suspected that climate variability could influence leatherback population size. El Niño Southern Oscillation (ENSO) is a large-scale atmospheric system that affects global climate. In leatherback foraging areas, El Niño years are associated with high atmospheric pressure and warm sea temperatures, while La Niña years are associated with low atmospheric pressure and cool sea temperatures. Importantly, cool sea temperatures stimulate upwelling of nutrient-rich water to the surface, increasing production of phytoplankton, thereby increasing the abundance of  jellyfish and other favored leatherback food items. So the researchers hypothesized that the leatherbacks might do better in La Niña years than in El Niño years.

But what do they mean by doing better? There are two important factors influencing population growth: survival and reproduction. Either one could be affected by climate. By recapturing marked individuals, Tomillo and her colleagues were able to measure both survival and one important aspect of reproduction, which is how often females return to lay eggs. Reproduction is a very energetically demanding process for leatherback females, as they must migrate long distances (often thousands of kilometers) from their feeding grounds, and their eggs are large and plentiful, so females require a huge investment in resources to reproduce. Consequently, at Tomillo’s field site, only 4.5% of females reproduced in consecutive years, while the average interval between reproductive events was 3.65 years.

Let’s consider leatherback survival. As you can see from the data below, annual survival probability is very variable from year to year, ranging from about 30% in 2012 to near 100% in several years. Disturbingly, the long-term trend is downward, and the overall mean adult survival rate of 0.78 is very low in comparison to viable populations of sea turtles. If survival rates do not increase, the future is very bleak for this population.

Tomillo Fig4

Annual survival probability of adult females tagged at Las Baulas National Park. Vertical bars indicate 95% confidence intervals.

How does climate variation influence survival and reproduction? The Multivariate ENSO Index (MEI) measures ENSO strength, with positive numbers (X-axis on graphs below) indicating El Niño years (with poor food availability), and negative numbers indicating La Niña years (with good food availability). The researchers found no climate effect on survival (top graph below), but a high reproductive rate associated with La Niña events (bottom graph below).


The question remains, why is survival so low? Climate does not appear to affect survival, so that brings us back to human impact. Tomillo and her colleagues recommend reducing bycatch levels and implementing beach conservation measures to eradicate egg poaching. They also warn us that increases in global temperatures reduce egg hatching success, and pose a severe stress to this and other critically endangered leatherback populations throughout the world.

note: the paper that describes this research is from the journal Ecology. The reference is Santidrian Tomillo, P., N. J. Robinson, A. SanzAguilar, J. R. Spotila, F. V. Paladino, and G. Tavecchia. 2017. High and variable mortality of leatherback turtles reveal possible anthropogenic impacts.  Ecology 98: 2170–2179. 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.