The effect of soil moisture and ambient temperature on pupation depth for the imperiled Callophrys irus

doi:10.21203/rs.3.rs-2583789/v1

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The effect of soil moisture and ambient temperature on pupation depth for the imperiled Callophrys irus

https://doi.org/10.21203/rs.3.rs-2583789/v1

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published 01 Aug, 2023

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The frosted elfin Callophrys irus (Godart) (Lepidoptera: Lycaenidae), is an imperiled species endemic to fire-maintained habitats in eastern North America. C. irus spends the majority of the year as pupae that may be vulnerable to fires that occur during this life stage. One way C. irus survives fire is to burrow and pupate under the soil, but this behavior is variable between individuals. We ran an ex-situ test on the impact of two abiotic factors on the pupation depth of C.irus (n = 60): ambient temperature and soil moisture. We used two incubators at 18 ºC and 30 ºC in addition to two moisture conditions of 5 and 15%. The null model outperformed other models, suggesting the effects of soil moisture and temperature on depth were negligible. The number of caterpillars that burrowed was similar to previous work with nine caterpillars that burrowed fully beneath the soil surface. If in-situ burrowing rates reflect our findings high mortality rates can be expected from fire. Thus, small, isolated populations may require artificial interventions. Our results support previous recommendations on the importance of refugia and population/habitat-specific rotational burn schedules to ensure the long-term persistence of the species.

Lepidoptera

fire

management

burrowing

pupae

The frosted elfin (Callophrys irus Godart) is a rare Lycaenid butterfly currently in review for federal listing under the Endangered Species Act (USFWS 2018). The larval host plants of C. irus are early successional species in the Fabaceae family of lupine (Lupinus spp.) and wild indigo (Baptisia spp.; Schweitzer et al. 2011; Frye and Tangren). The frosted elfin inhabits disturbance-dependent communities such as sandhill and upland pine, oak savannas, and oak-pine barrens and once occurred in 32 states (Thom 2013). It is currently extirpated in Ontario (Canada), Illinois, Vermont, and the District of Columbia due to habitat loss, insecticides, and other factors (USFWS 2018). Fire suppression is one of the largest determinants of C. irus’s widespread habitat decline throughout North America (Motzkin et al. 1999; Wagner et al. 2003; Pfitsch and Williams 2009) but especially so in the southeastern US because it leads to encroachment of woody species that outcompete necessary host plants (Grigore and Tramer 1996; Anderson et al. 1999). Frequent prescribed fires, coupled with rotational burn schedules and refugia, are recommended for frosted elfin habitat management (Selfridge et al. 2019; Jue et al. 2022).

Ironically, fire may be a serious threat to frosted elfin survival. While C. irus requires short burn return intervals to maintain its habitat, it is vulnerable to fire for most of its life cycle as they exist at or close to the ground (Thom et al. 2015; Jue et al. 2022; Meyer et al. 2023). Subsurface pupation is a common adaptation used for protection from moisture loss, predators, and parasitoids in insects including Coleoptera, Diptera, Hymenoptera, Lepidoptera, and Thysanoptera (Varatharajan and Daniel 1984; Chapman 1998; Sprague 2013). Frosted elfins pupate at or near the soil surface or up to three centimeters deep, which could increase fire survival (Thom 2013; Selfridge et al. 2019). A recent study by Meyer et al. (2023) found that C. irus are more protected from prescribed fire when they burrow at least 1.75 cm below the soil surface. Regardless of the protection a burrowing strategy might provide, it is not consistently utilized by C. irus. Not all individuals burrow, nor do individuals burrow at consistent depths. Researchers to date have reported a 19.64% (n = 56) burrowing rate in C. irus (Thom et al. 2015; Mcelveen and Craig 2017; Selfridge et al. 2019; Meyer et al. 2023).

While burrowing may increase an individual's chances of survival, little work has been done on C. irus to determine what factors contribute to this behavior. Selfridge et al. (2019) showed that preference for one of the two host plant species did not impact the final pupation site. But to date, no study has examined the abiotic factors that might lead C. irus caterpillars to pupate below the soil surface. Studies of Lepidopteran pests have shown that moisture is a critical factor in pupation site selection for overwintering insects (Qi et al. 2007). For example, larvae of Heortia vitessoides (Lepidoptera: Crambidae) avoid pupating in extremely dry or wet substrates (Wen et al. 2016). There is a negative correlation between moisture and compaction of the soil that may affect the amount of available oxygen (Eskafi and Fernandez 1990; Pielström and Roces 2014). In addition, soil compaction has been shown to lower the survival of overwintering pupae (Eger et al. 1983). Less moisture and correlated higher soil compaction may generally make it more difficult to burrow. Conversely, researchers have also shown that high moisture (30%) can also slow developmental progress from prepupae to pupae and decrease survival in Spodoptera exigua (Lepidoptera: Noctuidae; Zheng et al. 2013). Higher moisture in a banana-agar-yeast medium resulted in a larger proportion of two Drosophila spp. (Diptera: Drosophilidae) pupating on the walls of the vial (Sameoto and Miller 1968). Ambient temperature may also influence moisture levels, especially during drought events. In Florida specifically, soil surface temperatures in the spring and summer can exceed the lethal core limit of 50 ºC for animals (Thom 2013). Mensua (1967) observed an increase in Drosophila pupation height when temperatures increased from 13 to 35 ºC. However, at 29 ºC pupation height fell drastically.

It is important to understand the burrowing behavior of C. irus caterpillars due to the high rates of mortality at the surface especially as it relates to the frequent prescribed fire needed to maintain their habitat. We hypothesize that individuals within a certain habitat’s set of abiotic conditions lead to differences in burrowing behavior. This includes 1) the effect of soil moisture on soil compaction and aggregate stability where higher moisture could create a more conducive condition for excavating soil, 2) ambient temperature where a higher temperature could cause an individual to burrow to avoid desiccation or 3) a combination of both soil moisture and temperature could influence a caterpillar’s decision to bury. If the effects of these abiotic factors are known, land managers can take seasonal conditions into account and plan prescribed fires accordingly to lower mortality rates in vulnerable populations. In summary, we examine how ambient temperature and soil moisture under controlled conditions impact C. irus caterpillars’ burrowing behavior.

Mid- and late-instar frosted elfin caterpillars were collected from 41 unique host plant patches in the Apalachicola National Forest (ANF) of north Florida in March-May 2022 (permit #: WAK01192021). Caterpillars were randomly assigned to one of four treatments using two levels of 5% or 15% soil moisture and 18 ºC or 30 ºC temperatures (Fig. 1) and were added to the study in a staggered fashion as they were found in the wild. Each caterpillar was placed in a substrate-filled incubator in a cup with a ventilated lid and monitored daily at dawn and dusk until pupation.

The soil substrate was collected from the surface layer of a sandy, xeric site near the population of C. irus in the ANF. The substrate was sifted through a three-millimeter sieve to remove large particles, thoroughly mixed to ensure homogeneity, and dried at room temperature for a week. We filled transparent 132 ml plastic cups filled with 100 g of dried substrate then added distilled water using a spray bottle for even distribution to create the two soil moisture levels. Substrate moisture levels were determined with the equation: moisture content (%) = [weight of distilled water added into soil/(weight of saturated soil – weight of dried soil)] × 100. The substrate was compacted to match the average soil density (1.51 g/cm³) found in C. irus habitat in the ANF, resulting in a substrate height of 2.92 cm and 3.20 cm for low and high moisture treatments respectively.

The influence of temperature on burrowing was tested by placing cups containing one caterpillar each (given a soil moisture treatment) in one of two incubators. Each cup was buried to the rim in the substrate to reduce lateral absorption of heat and mimic the lower ground temperatures expected in situ. The temperature in the heated incubator (Hova-Bator model 1602N, Savannah, GA) was 30 ºC versus a room temperature of 18 ºC for the unheated control incubator. A full spectrum T6 light bulb was placed above each incubator and allowed light to enter the incubator without adding any additional heat from the bulb. To avoid overheating and possibly killing the pupa, the heated incubator and attached lights were put on a timer with a photoperiod of 13:11 h L:D. For one hour at dawn and dusk the heat and light cycled on and off in 15-minute intervals to mimic twilight hours. The unheated incubator was under the same light conditions. The position in the cup and the behavior of the caterpillars were recorded daily at dusk and dawn and each cup was moved to a new location in the incubator. Lupine (Lupinus perennis ssp. gracilis) leaves were replaced, and frass was removed from cups as needed until pupation. A wooden stick was placed in each cup at and perpendicular to the side of the cup to determine how often caterpillars use submerged material or plants as an aid to burrowing. Pupation depth was measured from the top of the soil to the closest point on the pupae.

All statistics were done using program R statistical software (R Core Team 2022). We used the lme4 package to perform a generalized linear model (logit link) with whether or not a caterpillar attempted to dig as a binomial response variable with soil moisture, temperature, and an interaction term between the two as independent variables. We then used Akaike’s information criterion corrected for small sample sizes (AIC_c) to compare subsets of this global model (five models total including the null model). The top model was selected based on the most parsimonious model with the lowest ΔAIC_c and highest model weight that was not a subset of other models (Arnold 2010). Summary statistics are provided on all other attributes of pupation with 95% confidence intervals when appropriate. Significance was established at α = 0.05.

Sixty of the 65 frosted elfin caterpillars that entered the study survived to pupation. One individual was killed by a parasitoid fly larva (Diptera: Tachinidae) before pupation that likely infected the caterpillar before it entered the study. The cause of mortality for the remaining four individuals is unknown but included those in both soil moisture and temperature treatments. The other 60 individuals were approximately evenly distributed between treatments (Table 1). Forty-one caterpillars made their pupation site “choice” (stopped moving) during the night as opposed to the 19 individuals that stopped during the daytime. Caterpillars wandered around their containers for a mean of 5.06 days (counted in half-days, range: 0.5–10.5 days) without eating before selecting a pupation location. Caterpillars spent a mean of 2.58 days in a sedentary pre-pupal phase after wandering (counted in half-days, range: 1–4 days).

Table 1

Results of a lab study on frosted elfin (*Callophrys irus*; n = 60) pupation depth (attempted burrowing/no burrowing) given differing soil moisture and ambient temperature.
	Soil Moisture
Temperature	5%	15%	Total
18 ºC	5/9	1/14	29
30 ºC	3/13	4/11	31
Total	30	30	60

The top performing model was the null model (ΔAIC_c = 0, w = 0.42, Table 2), and estimated the probability that a caterpillar pupated within the soil was 0.22 (95% CI: 0.14–0.33; P < 0.01). Since the null model was the top performing model, we combined soil moisture and temperature groups for most summary statistics. A total of 13 (21.67%) caterpillars pupated within the soil (below the soil surface to some degree), 23 (38.33%) pupated at the soil surface, and 24 (40%) pupated above the soil. The pupation site of 15 C. irus was on the side or lid of the plastic cup. Twelve individuals pupated on the wooden stick, of which, two used it to burrow within the soil. When caterpillars pupated within the soil, four individuals did not fully burrow and instead pupated in a shallow depression that left most of their body exposed at the soil surface. Nine (15%) burrowed fully beneath the soil an average of 7.5 mm (n = 4; 95% CI: 0.44–14.56 mm) and 3.8 mm (n = 5; 95% CI: 1.38–6.22 mm) below the surface for room temperature and heat-treatment respectively. Two individuals from the control group, one in each soil moisture level, burrowed 1.1 cm and 1.6 cm below the ground, a depth that may not be affected by some low-severity fires (Robichaud and Waldrop 2007; Thom et al. 2015).

Table 2

Generalized linear model results for factors affecting frosted elfin (*Callophrys irus*) pupation above or within the soil surface. Models included categorical variables of soil moisture (5 or 15%; ‘m’), temperature (18 ºC or 30 ºC; ‘t’) and the interaction between the two (noted by ‘x’). The number of model parameters (‘K’) is given to indicate model complexity. Models were compared using Akaike’s information criterion corrected for small sample sizes (AIC_c), and model weight (w).
	K	AICc	ΔAICc	w
Null	1	64.79	0	0.42
m	2	66.04	1.25	0.22
t	2	66.9	2.11	0.15
m x t	4	67.16	2.38	0.13
m + t	3	68.23	3.45	0.08

Overall, we failed to reject the null hypothesis, meaning there was no relationship found between the burrowing of frosted elfin caterpillars and temperature or soil moisture. However, our results corroborate previous work and contribute to the overall knowledge of burrowing depth for this species. The proportion of individuals that pupated below the surface in our study (15%) is comparable to the 19.64% of preceding research. Based on data provided by Thom et al. (2015) and Meyer et al. (2023) it is unlikely C. irus can survive fire unless they burrow much deeper beneath the surface. Only two caterpillars out of 60 (~ 3%) burrowed at a level deep enough (~ 1.5 cm) to survive the expected lethal temperatures of a typical prescribed fire in north Florida. If our findings mimic natural propensities to burrow, high mortality can be expected when prescribed fires are applied to management units containing elfin pupae. Meyer et al. (2023) observed a higher rate of natural burrowing with four out of 10 burrowing to depths of 1, 1.5, 2.5, and 5 cm. While the sample was small, data suggest chances of survival could be as high as 30%. Future laboratory investigations on the rate of burrowing in frosted elfins could test more extreme variables using more common Lycaenid species that exhibit comparable burrowing behavior.

While there was no significant difference in pupae burrowing across temperature or soil moisture conditions, there are other potential influences on burrowing behavior. We believe that the caterpillars may dig opportunistically when they encounter a micro-pocket of low compaction during wandering. This may have been a factor with two individuals that dug near the stick and one that used a space between the sand and cup that originated when the stick was placed. It is possible that the energetic cost of digging does not outweigh the probability of being burned. The variation in pupation behavior observed in this species may be controlled by inherited traits while burrowing likelihood is further influenced by energy, conditions, or the ability to find a suitable location. For example, genetics, environmental factors, and sex influence larval behavioral phenotypes which are linked and heritable in individuals of Drosophila melanogaster. Phenotypes that travel further to forage for food pupated higher or burrowed deeper in containers (Sokolowski and Hansell 1983; Riedl et al. 2007).

Additionally, C. irus may burrow to escape predation. For example, insect predators can have different thermal tolerances than their prey, which may limit interactions (Huey and Kingsolver 1989; Chown and Nicolson 2004). Formica lasioides (Hymenoptera: Formicidae) predation of Platyprepia virginalis (Boisduval) (Lepidoptera: Arctiidae) decreased when larvae took refuge in cool, wet leaf litter (Karban et al. 2015). Potentially, C. irus’ burrowing behavior protects individuals from their most common predators. Callophrys irus may be less likely to burrow in the absence of predators, which it could detect from olfactory stimuli from the environment and was not present in our study. Regardless of the evolutionary influences on this behavior, the frequency of burrowing could be critical information for the successful stewardship of vulnerable populations.

Historically, fires in southeastern pine savannas primarily occurred during the lightning season in May to mid-July and were low-intensity, fast-moving fires (White and Harley 2016). When considering the tradeoff between burrowing and conserving energy, spatial and temporal heterogeneity of prescribed fires (i.e. ‘pyrodiversity’) in this habitat may have made energy conservation more favorable for the frosted elfin over evolutionary time. For example, in north Florida sandhill pine ecosystems, researchers recommend burning in 2–4 year intervals. In this climate, burning before February and after April protects frosted elfins during their most vulnerable life stages as eggs or caterpillars (McElveen pers. comm.; Jue et al. 2022). Burning outside this recommended time frame may also affect the successional stages of the host plant and the ability of adults to recolonize a hostplant patch from neighboring populations within their flight time of 2–5 weeks (Thom 2013). Fire affects vegetation structure across 40% of the world’s land surface and across many different ecosystems (Chapin et al. 2011). The best time to burn for C. irus is specific to the site and habitat type being managed. Seasonality along with local coevolution with fire should be considered.

Our results support previous recommendations of refugia and rotational burn schedules throughout occupied C. irus habitat. Pyrodiversity has been recommended for the benefit of avian, invertebrate, and plant species of longleaf pine habitats (Hanula and Wade 2003; Knight and Holt 2005; Chitwood et al. 2017; Robertson et al. 2019; Weber et al. 2022). Land managers should assess fire return intervals, ignition techniques, and weather conditions when applying fires to small, isolated populations of this imperiled butterfly. Importantly, artificial intervention may be required to ensure population survival post-burn.

Author Contributions

Rob Meyer fulfilled the supervision role, funding acquisition, material preparation, and preformed the formal analysis and investigation. The conceptualizations and the original draft were written by Emma Jonas and Rob Meyer. All authors contributed to the methodology, the review and editing of each draft, and read and approved the final manuscript.

Acknowledgments

We would like to thank Jessica Valdez and Apalachicola National Forest staff for allowing us to conduct work within the forest. Their overall support of the project has made this possible. We would also like to thank Dave McElveen and Jim Cox (Tall Timbers Research Station) for their edits and comments on the early manuscript and support of the project.

This project was made possible through funding from the FWFF (CWT 21- 13) and the Fish and Wildlife Services At- risk Species Program through the Wildlife Management Institute (SA 2020-04). Author Robert Meyer receives a salary from Tall Timbers Research Station.

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The effect of soil moisture and ambient temperature on pupation depth for the imperiled Callophrys irus

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