Experimental simulation of environmental warming selects against pigmented morphs of land snails

Abstract

In terrestrial snails, thermal selection acts on shell coloration. However, the biological relevance of small differences in the intensity of shell pigmentation and the associated thermodynamic, physiological, and evolutionary consequences for snail diversity within the course of environmental warming are still insufficiently understood. To relate temperature‐driven internal heating, protein and membrane integrity impairment, escape behavior, place of residence selection, water loss, and mortality, we used experimentally warmed open‐top chambers and field observations with a total of >11,000 naturally or experimentally colored individuals of the highly polymorphic species Theba pisana (O.F. MÜLLER, 1774). We show that solar radiation in their natural Mediterranean habitat in Southern France poses intensifying thermal stress on increasingly pigmented snails that cannot be compensated for by behavioral responses. Individuals of all morphs acted neither jointly nor actively competed in climbing behavior, but acted similarly regardless of neighbor pigmentation intensity. Consequently, dark morphs progressively suffered from high internal temperatures, oxidative stress, and a breakdown of the chaperone system. Concomitant with increasing water loss, mortality increased with more intense pigmentation under simulated global warming conditions. In parallel with an increase in mean ambient temperature of 1.34°C over the past 30 years, the mortality rate of pigmented individuals in the field is, currently, about 50% higher than that of white morphs. A further increase of 1.12°C, as experimentally simulated in our study, would elevate this rate by another 26%. For 34 T. pisana populations from locations that are up to 2.7°C warmer than our experimental site, we show that both the frequency of pigmented morphs and overall pigmentation intensity decrease with an increase in average summer temperatures. We therefore predict a continuing strong decline in the frequency of pigmented morphs and a decrease in overall pigmentation intensity with ongoing global change in areas with strong solar radiation.

Multiple Introductions of the Pestiferous Land Snail Theba pisana (Müller, 1774) (Gastropoda: Helicidae) in Southern California

“…Highly variable banding patterns and shell pigmentation in T. pisana were observed herein but not analyzed between or within sites. For a detailed treatment and discussion of shell banding, see Cain [98], Cowie [99], and Köhler et al [89]. Radular morphology was consistent with illustrations and descriptions by other authors [66,67] and was not significantly different between T. pisana from Los Angeles and San Diego sites.…”

“…Such studies also highlight the phenomenon of biotic homogenization [80], identify anthropogenic pathways of introduction [81], may improve protocols for species interception and quarantine, and inform strategies for invasive species eradication or control [81]. Likewise, the distinct parentage of T. pisana in Southern California could be an important component of studies focused on diversification in the genus Theba [82] and varied investigations of genetic drift [83] and the founder effect [84], resource use [85], niche partitioning [86] and adaptation [87][88][89] in introduced gastropods. We anticipate that the CO1 barcodes and 16S and ITS2 sequences from T. pisana specimens generated for this study will be useful in assessing the provenance of new populations and interceptions of T. pisana in California, elsewhere in North America, and worldwide.…”

Thermobiological effects of temperature‐induced color variations inAglais urticae(Lepidoptera, Nymphalidae)

“…After placing the arrangement with the four butterflies in the lighting cabinet, they were illuminated for 5 or 15 min. After these times, thermographic images were taken with a Micro‐Epsilon thermo Imager TIM 400 thermocamera, and the surface temperature of the dorsal side was then determined using the corresponding TIM software (Figure 3 ) following the methodology of Köhler et al ( 2021 ). For this purpose, 10 individual measurements were taken per animal at different but specific locations on the wings, from which an individual‐based mean value was calculated.…”

Morph-dependent nematode infection and its association with host movement in the land snail Cepaea nemoralis (Mollusca, Gastropoda)

“…This possible association between immunity and pigment-related pathways could have further ecological relevance in land snails. Indeed, many species exhibit shell colour polymorphism (Williams, 2017), which affects behavioural and physiological thermal responses (Jones, Leith & Rawlings, 1977; Schweizer, Triebskorn & Köhler, 2019; Köhler et al ., 2021) or vulnerability to predators (Jones et al ., 1977; Rosin et al ., 2011; Rosin et al ., 2013; Surmacki, Ożarowska-Nowicka & Rosin, 2013).…”