Temperature-driven outbreak cycles in the Japanese tea pest



Figure 2 Moth dynamics at the Kagoshima tea station. (A and B) Adult densities. (Right) Years with relatively low amplitude (C) and high amplitude (D) outbreak cycles.


Figure 1 Adult moth of the smaller tea tortrix, Adoxophyes honmai.

A number of insect species show large-amplitude outbreak cycles that are roughly one generation in duration, particularly during warmer summer months. The predominant view is that these cycles occur because insect stages are synchronized by the environment, such as cold winters. While this can account for the occurrence of one or two cycles at the start of a season, it doesn’t explain how some insects can show sustained multiple cycles throughout a season because there isn’t a mechanism to prevent cohorts from smearing into each other. An alternative explanation is that generation cycles are large-amplitude population cycles where temperature can impacts system stability through the action it has on moth life history.

Working with Ottar Bjornstad (Penn State, USA) and Takehiko Yamanaka (National Institute for Agro-Environmental Science, Japan), Bill Nelson is working on a project to understand the impact that temperature has on population dynamics. Owing to the passion that one of us has for green tea, and all of us have for remarkably detailed time-series (Figure 2), we are working with the smaller tea tortrix Adoxophyes honmai. This moth is a nasty pest of Japanese tea plantations that shows sustained outbreak cycles each year. Since temperature influences dynamics through it’s effect on individual life-history traits, we approached the problem by developing physiologically structured population models from laboratory life-history data and comparing their predicted dynamics with the observed time-series. Our work has shown that the cycles are the result in intraspecific competition rather than interactions with the food web (Yamanaka et al. 2012 Am. Nat.) and that  seasonal changes in the outbreak cycles occur because the system crosses a HOPF bifurcation and becomes destabilized during warm parts of the season (Nelson et al. 2013 Science; Figure 3).


Figure 3 Predicted temperature-driven changes in stability. (A) The system is stable at cool temperatures (black), but undergoes outbreak cycles at high temperatures (blue). Mean monthly temperature for the tea station is shown in red. (B) Sample of predicted moth densities.


Figure 4 Experimental apparatus for temperature control experiments (a: water chiller, b: insulated aquaria with heaters) and images of a tea tortrix egg mass (c), adult (d), and larva (e).

We are now embarking on the next phase of the project, which is to understand the ecological and evolutionary mechanisms that give rise to outbreak cycles. To do this, we are conducting experiments at both the individual-scale and population-scale (Figure 4). Combined with physiologically-structured models that scale from life-history traits to population dynamics, this approach provides a nice synergy between experiments and theory because the models are fully parameterized by individual-scale data, and the resulting theoretical predictions at the population-scale can be tested experimentally.

Castration and gigantism in Daphnia


When Daphnia magna individuals are infected by the bacterium Pasteuria ramosa, they are reproductively castrated and can grow to twice their normal biomass. The two animals here were born in the same clutch, but the animal on the left was infected and the animal on the right was not. You can see the lack of eggs in the brood pouch, the large size, and the cloud of parasite spores filling the hemolymph of the animal on the left. My interest in this system has been to understand the role of energy acquisition and allocation in influencing the within-host dynamics of Pasteuria.

Diversity maintenance in Daphnia over fine spatial scales

Migration Figure
The System

Ariel Gittens, as part of her recent graduate work in the Nelson lab, has identified three distinct phenotypes of Daphnia pulicaria that seem to coexist seasonally in Round Lake while undergoing distinct migration behaviours.  The most obvious distinction between the phenotypes is a difference in the up-regulation of hemoglobin that causes the animals to be differently coloured where “Pales” do not up-regulate hemoglobin, “Reds” substantially up-regulate and “Pinks” lie somewhere in between.  Additionally, Figure 5 shows the varied migration behaviours of the phenotypes. “Pales” occupy the cold and food-rich hypolimnion during the day and migrate upwards to occupy the warm epilimnion at night. Conversely, “Reds” do not appear to undergo any migration whatsoever, preferring to remain in the hypolimnion indefinitely. “Pinks” undergo a more moderate migration behavior of smaller amplitude but on a similar schedule to Reds. There is strong evidence in the literature and in Ariel’s thesis work to suggest that variation in the up-regulation of hemoglobin is the result of varying time spent in the oxygen poor hypolimnion, however the mechanism behind the maintenance of these multiple migration strategies, as well as the relative importance of the many environmental factors at play in this system, remains unclear.


Analyzing population structure in Daphnia pulicaria.

Based on observations in the field, lab and in the literature. CP - cyclic parthenogen, OP - obligate parthenogen

Life cycle based on observations in the field, lab, and in the literature. CP – cyclic parthenogens, OP – obligate parthenogens, apomixis – asexual reproduction without meiosis. Neonates (1st instar) typically go through 20 -25 instar stages in their life cycle (Lynch, 1989).
Note: In some cases CP females do not seem capable of producing males even though they can reproduce sexually.

A year long time series of size, fecundity, hemoglobin, and food availability, is being investigated for changes in genotype and phenotype from summer 2014 to August 2015.  This snapshot of Daphnia pulicaria will enable us to assess their local adaptive capabilities and determine the extent to which they can overwinter successfully in Round Lake.  The overwintering genotypes will be ready to exploit the phytoplankton available in late winter and early spring at which time they can start to increase by reproducing sexually and asexually.

Background genetics on D. pulicaria.

summ table Ldh

Microsatellite work by Cristecu et al. (2012) have shown a clear genetic divegence in the nuclear genome of D. pulex and D. pulicaria.  The two species are typically either “pond” species D. pulex or “lake” species D. pulicaria. . Preliminary electrophoresis runs for the allozyme lactate dehydrogenase indicated that in Round Lake we had Daphnia pulex and a D. pulex/pulicaria hybrid (the latter making up ~11% of the population).  A reference cloneline of D. pulex was obtained from Clay Prater (phD candidate at Trent University).  It was shown that in Round Lake we in fact have D. pulicaria and the ‘hybrid’ is actually thought to be D. schodlerii. All three species are morphologically similar.  D. schodlerii is a little smaller than the two other species and has one more mid-pectel tooth.


The role direct versus indirect ecological interactions have on evolution in simple food webs

food web interactions

Highlighting the various direct and indirect interactions in a host-parasitoid food web, where two competitors share the same resource and predator.