Pine savannas in the Southeastern United States are subject to an historical regime of periodic fire, with many and varied ecological consequences. Insectivorous plants of the genus Sarracenia (L.) (Sarraceniaceae) often entirely lose their aboveground leaves to these periodic fires. During the growing season, these tubular leaves, which act as pitfall traps for insects, are host to pitcher plant moths, Exyra (Grote) (Noctuidae), which live their entire life cycle within the plant. This study tested the effect of smoke on a small sample of Exyra semicrocea in pitchers, and demonstrated that they respond quickly by flight.
Pine savannas of the Southeastern United States are dominated by the large southern yellow pines, which include Pinus palustris (Mill.), Pinus taeda (L.), and Pinus elliottii (Engelm.). These forests do not have a dense canopy, which allows for the growth of a rich understory (Harrington et al. 2013), including in scattered suitable microenvironments pitcher plant savannas (Wells 1928, Walker & Peet 1983). Hydric pine savannas have wet, sandy soil that is nutrient poor, and contain several species of carnivorous plants, including several species of pitcher plant (Folkerts & Folkerts 1993). Such savannas and bogs, the pitcher plants they contain, and a rich associated biota are of high conservation concern because of the biological diversity of the areas and their greatly reduced modern extent (Stephens et al. 2011).
Longleaf pine forests are subject to frequent fire (Komarek 1974, Platt et al. 1991) and contain plant and animal species that are fire adapted, and which are the subject of a rich literature reviewed by Van Lear et al. (2005). Historically, fires in pine savannas of the coastal plain occurred at intervals of one to ten years (Komarek 1974, Platt et al. 1991), and the US Forest Service manages such sites with controlled burns every 3 years (USDA National Forest Service 2002). The insectivorous pitcher plants, Sarracenia flava (L.) and Sarracenia leucophylla (Raf.) are adapted to these frequent fires (Brewer 1999). The plants have subterranean rhizomes, which allow them to quickly replace their above-ground parts and avoid competition with other plants (Barker et al. 1988).
Pitcher plants have no less than 17 arthropod symbionts, given relatively little study compared to the pitcher plants themselves (Stephens et al. 2011), among which are pitcher plant moths, Exyra (Grote) (Noctuidae) (Stephens & Folkerts 2012). Two of the three species of Exyra, the pitcher plant mining moth, E. semicrocea (Guenée) and Riding's pitcherplant looper moth, E. ridingsii (Riley) are prevalent in the pitcher plant savannas of the Southeast where they inhabit the pitcher plant savannas (Stephens & Folkerts 2012). The moths live out the majority of their life inside pitcher plants (Jones 1921), only emerging at night (Stephens & Folkerts 2012). The adults lay one egg in a plant. The larvae pupate after five larval instars and the adults shelter in the plants, only flying out at night.
Given that these savannas burn frequently, and that pitcher plant moths are found in pitchers that have grown since recent fires (Ricci 2015), we would expect pitcher plant moths to be adapted to frequent fires. Prior to this study, it was unknown if the adult moths flee fires and survive, or if they fail to avoid fire and risk death. We hypothesized that the moths would leave the pitchers when fire approached, despite our experience that Exyra strongly resist physical efforts to force them to leave pitchers during the day. Furthermore, our experience was that when physically forced to depart pitchers, we rarely observed them to fly more than 20 meters during the daytime (McPhail and Meier pers. obs.). This distance is unlikely to be sufficient to avoid fires.
Methods
Fire Experiment 1. On October 17, 2015, between 0700 hours and 0800 hours, at 30° 41.138′N, 88° 3.879′W within Mobile, Alabama, we placed two Sarracenia leucophylla pitchers in separate jars full of dry pine needles and grass. One pitcher at a time, we then set the pine needles and grass ablaze. We recorded the number of moths that left their pitcher as well as the time in which it took them to leave. No moths were killed while conducting this experiment.
Fire Experiment 2. On October 18, 2015, in the Sumatra Pine Savanna within the Apalachicola National Forest between 1300 hours and 1400 hours, we found six Pitcher Plant Mining Moths in five tubular leaves of S. flava. Their coordinates were 30° 2.407′N, 84° 57.684′W.
The first treatment was to observe the moths in the pitchers for two minutes to determine if they would leave the pitcher without disturbance. We recorded the number of moths that left their pitcher plants as well as the time in which it took them to leave. In the second treatment, a group member exposed the moths to two minutes of gently blowing air with a bee smoker that had not been ignited at ca. 10cm from the opening of the pitcher. We recorded the number of moths that left their pitcher plants as well as the time in which it took them to leave. In the third and final treatment for this second experiment, a group member flicked, squeezed, and shook the pitchers to provoke the moth into leaving. We recorded the number of moths that left their pitcher plants as well as the time in which it took them to leave. For the experimental trial, we exposed each of these moths to smoke from burning dry pine needles and grass within the smoker. A group member subjected each plant to smoking while holding the bee smoker 10cm away from the pitcher. It was intended that smoking of the pitcher should continue for up to two minutes if the moths remained in the pitchers. We recorded the number of moths that left their pitcher plants as well as the time which it took them to leave. Once the moths left their pitchers, we attempted to follow two of the moths to determine the distance that they would fly. No moths were killed while conducting this experiment.
Temperature of the Smoke. A bee smoker was filled with pine needles and lit. We held the smoker at 10cm from the opening into the pitcher and applied smoke to three pitchers from S. leucophylla in a fashion similar to that used by us in the field. We used a Fluke Hydra Series II thermocouple, set on channel 1, to read in degrees C., in the J temperature range. We took six sequential readings from each pitcher at 5 second intervals at 10 cm deep inside the pitcher, this being the minimum depth in the pitcher where moths were located. We took two readings before wafting smoke towards the pitcher, and four after the pitchers began receiving smoke.
Statistical Analysis.We used the VasserStats Online Program to perform a Chi-Square independence test comparing the frequency of departure within two minutes for each of the trials.
Results
Fire Experiment 1. When we started the fire underneath two of the pitcher plants, both moths emerged. The first flew out 13 seconds after the pine needles were lit, and the other flew out 17 seconds after the needles were lit. It is interesting to note that the needles began smoking profusely a short period of time after being lit. If the time that they began to smoke is set as the reference point, then it took the first moth 4 seconds to leave the pitcher, and the second moth 7 seconds to leave the pitcher.
Fire Experiment 2. The three control trials caused no moths to leave their plants. None of the moths even moved when left alone or blown on. When the pitchers were vigorously shaken and flicked with our fingers, the moths moved around the inside of their pitchers and ultimately moved deeper into them. When smoked, every moth almost immediately left its plant (n = 6; mean = 6.5 seconds; s = 2.7). A chi-square test comparing experimental and control was highly significant (χ2 = 12, df = 2, p = 0.0025).
A group member followed two of the moths after they fled their pitcher plant. Both moths flew over 200 meters before entering another pitcher plant.
Influence of the smoke on temperature. Wafting smoke past the openings of S. leucophylla in a fashion similar to that used on the moths in the field yielded a maximum temperature change of 0.1 degrees C among all 3 pitchers tested.
Discussion
We hypothesized that the moths would leave their pitchers and take flight in the presence of smoke as a means of escape before being consumed by fire. This hypothesis suggests that existing populations of pitcher plant moths can emigrate to survive fires; thus inviting comparisons to the shifting mosaics and metapopulation dynamics described by Harrison et al. (1988), Hanski et al. (1994), and Hanski et al. (1995) for butterflies. Given past personal experiences with the moths' reluctance to leave pitchers during the daytime, we were not certain that they would do so under the influence of smoke (Pers. Obs. McPhail and Meier). Fire might severely reduce a local population of pitcher plant moths if they fail to respond, and assuming that they do not employ a life cycle approach to survival (for example, pupating underground). In order to successfully employ a metapopulation strategy, Exyra moths must be able to successfully recolonized areas that are burned. Until recently there was no research on this subject. Ricci (2015) suggested that Riding's pitcherplant looper moths may employ a metapopulation strategy despite showing low mobility. We found in a small sample of six pitcher plant mining moth that even a few seconds exposure to smoke caused moths to leave the pitchers and fly. The results of this study support the additional hypothesis that smoke, not temperature is the stimulus that triggers the emigration of the moth from one habitat to another. Temperature differences inside the pitchers were minimal, 0.1 C, when the moths were exposed to smoke.
Despite our previous observations of daytime movements limited to 20 meters, when confronted with smoke, the moths were observed traveling much longer distances (200 meters). This ability to flee longer distances increases the opportunities for pitcher plant moths to survive fires, and relocate if necessary.
Acknowledgements
The authors would like to thank the following for their contribution to the above experiment. Western Kentucky University's Honor's College and the Western Kentucky University Green River Preserve for funding this work. We thank Dr. John Andersland and Barrett Rogers, for field work contribution and photography. Amelia Smith for extra-experimental field work. Robert Choate for thermocouple equipment and expertise. We would like to thank Debbie Folkerts for confirming the identification of a pitcher plant mining moth from the population. Finally, we would like to thank Eric Metzler and an anonymous reviewer for reviewing this paper.
