Near-Daily Reconstruction of Tropical Intertidal Limpet Life-History Using Secondary-Ion Mass Spectrometry ✉ Anthony Mau 1 , Erik C
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ARTICLE https://doi.org/10.1038/s43247-021-00251-2 OPEN Near-daily reconstruction of tropical intertidal limpet life-history using secondary-ion mass spectrometry ✉ Anthony Mau 1 , Erik C. Franklin 2, Kazu Nagashima 3, Gary R. Huss3, Angelica R. Valdez1, Philippe N. Nicodemus1 & Jon-Paul Bingham1 Measurements of life-history traits can reflect an organism’s response to environment. In wave-dominated rocky intertidal ecosystems, obtaining in-situ measurements of key grazing invertebrates are constrained by extreme conditions. Recent research demonstrates mollusc 1234567890():,; shells to be high-resolution sea-surface temperature proxies, as well as archival growth records. However, no prior molluscan climate proxy or life-history reconstruction has been demonstrated for the tropical rocky intertidal environment—a zone influenced by warmer waters, mixed tides, trade-wind patterns, and wave-action. Here, we show near-daily, spa- tiotemporal oxygen isotope signatures from the tropical rocky intertidal environment by coupling secondary ion mass spectrometry analysis of oxygen isotopes with the scler- ochronology of an endemic Hawaiian intertidal limpet Cellana sandwicensis, that is a sig- nificant biocultural resource harvested for consumption. We also develop a method for reliable interpretation of seasonal growth patterns and longevity in limpets. This study pro- vides a robust approach to explore tropical intertidal climatology and molluscan life-history. 1 College of Tropical Agriculture and Human Resources, University of Hawai’iatMānoa, Honolulu, HI, USA. 2 Hawai’i Institute of Marine Biology, School of Ocean and Earth Science and Technology, University of Hawai’iatMānoa, Kāne’ohe, HI, USA. 3 Hawai’i Institute of Geophysics and Planetology, University of ✉ Hawai’iatMānoa, Honolulu, HI, USA. email: [email protected] COMMUNICATIONS EARTH & ENVIRONMENT | (2021) 2:171 | https://doi.org/10.1038/s43247-021-00251-2 | www.nature.com/commsenv 1 ARTICLE COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-021-00251-2 nderstanding the phenotypic plasticity of marine species To reliably reconstruct Hawaiian limpet growth patterns, we Uto environmental change is crucial to understand the applied measurements of oxygen isotopes from secondary ion dynamics of coastal populations. Recent responses across mass spectrometry (SIMS) from shell line and increment features multiple marine taxa to extreme sea surface temperature (SST) formed during growth cessation (with represented time periods in anomalies highlight the need for intertidal research focusing on parentheses): major growth line (annual cycle), minor growth thermal tolerance and habitat shifts1,2. For rocky intertidal ecol- lines (lunar cycle), and minor growth increments (tidal cycle). For ogy, however, monitoring climate responses in-situ presents sig- these culturally and commercially important molluscan shellfish, nificant challenges under adverse tide-, wave-, and wind-exposed resolving growth patterns and longevity has critical implications conditions; and sub-annually resolved oceanographic climate for aquaculture, conservation, and fisheries. Here we recon- proxies have only recently been identified for this semi-terrestrial structed the life-history of the yellowfoot limpet Cellana sand- environment3–7. Similar to other oceanographic climate proxies wicensis from three shells, two modern and one historical, by (1) (i.e., coral skeletons, fish otoliths, foraminifera), most mollusc investigating oxygen isotope variation in the tropical intertidal shell are precipitated in isotopic equilibrium with seawater8.In environment using near-daily spatial scale SIMS analysis, and (2) these accretionary hard-tissues, oxygen isotope ratio (δ18O) determining seasonal growth and longevity. This study provides a measurements can be aligned with physiochemical features to robust approach to explore tropical intertidal temperature cli- infer seasonality with more negative values reflecting warmer matology and molluscan life-history. climate and more positive values reflecting cooler climate3,7,9–12. To date, robust reconstruction of seasonal to millennial sea- Results surface temperature (SST) from mollusc shells are numerous in Within each of the three shells of C. sandwicensis, five carbonate mid-to-high latitudes—where δ18O is strongly correlated with 9,13–15 mineralogical microstructure layers were revealed by SEM and seawater temperature . In contrast, SST proxies in low Raman microscopy in accordance with MacClintock, C. (1967). latitudes are limited to subtidal organisms (primarily corals), as fl With reference to the myostracum or muscle attachment layer hydrological processes (i.e., rainfall, estuarian mixing) in uencing (M), we observed one interior layer—aragonitic, radial crossed- δ18 16 sea surface salinity (SSS) can confound drivers of O . lamella layer (M−1)—and two exterior layers—aragonitic, con- Therefore, while corals are established long-term proxies of mean + 17–20 centric crossed-lamellar layer (M 1) and calcite, concentric annual SST , a high-resolution proxy for tropical intertidal crossed-foliated layer (M + 2), the latter being suitable for isotope climate is missing entirely. measurements (Fig. 1). The carbonate polymorph was uni- Mollusc limpet shells are an excellent candidate for tropical dentifiable for the shell’s outermost layer—a radial crossed- intertidal climate proxy records due to their archeological pre- foliated layer (M + 3). servation, wide distribution, and sequential growth (Twadle et al., 18 The observed VPDB corrected δ Ocalcite values from SIMS of 2016). With absolute temporal alignment of growth, ecologists can three shells ranged from −5.04‰ to −7.74‰ (modern specimen interpret species’ responses to physiological (i.e., ontogeny, repro- − ‰ − ‰ 21–25 CW1), 4.38 to 7.83 (modern specimen CW2), and duction) and environmental (i.e., extreme climate, tide) factors . −0.57‰ to −5.02‰ (historical specimen BPBM) (see Fig. 2, Within the Hawaiian Archipelago, endemic intertidal limpets Supplementary Fig. 5, Supplementary Table 1, Supplementary (Cellana spp.) are a significant biocultural resource declining in 26 Table 2). Across four annual isotope cycles, the BPBM oxygen abundance and experiencing contracting population distributions . isotope profile follows a sinusoidal pattern indicative of seasonal Due to complex and extreme rocky intertidal conditions, research 27,28 changes in the shell records of C. sandwicensis. Based on analy- on growth patterns of Cellana is limited . tical precision (2 standard deviations) and measurement precision Fig. 1 Shell specimen and microstructures. Shells were sectioned from anterior to posterior end. a White lines represent parallel cuts for thick-section preparation from historical specimen BPBM 250851-200492. b Cross-sections show the true direction of growth for limpets. c SEM exposed shell microstructures for area denoted in b. Oxygen isotope measurements were performed along the direction of growth in the crossed-foliated, calcite layer M + 2. 2 COMMUNICATIONS EARTH & ENVIRONMENT | (2021) 2:171 | https://doi.org/10.1038/s43247-021-00251-2 | www.nature.com/commsenv COMMUNICATIONS EARTH & ENVIRONMENT | https://doi.org/10.1038/s43247-021-00251-2 ARTICLE Fig. 2 Oxygen isotope profile of historical shell specimen. A shell cross-section and the associated oxygen isotope profile (δ18O) of a Hawaiian limpet (C. sandwicensis), reported in permille (‰) relative to the international VPDB standard, were measured sequentially along the growth axis—starting at the shell margin. This pattern in the δ18O profile of the historical shell (BPBM—green line) reflects the recorded seasonality in intertidal SST. The positive δ18O measurements (red squares) were taken along and correspond with major bands (red circles) in the shell cross-section. Error bars represent measurement error 2 sigma (2σ), which reflects both precision (2 standard error) and reproducibility (2 standard deviation). δ18 + (2 standard errors), the maximum uncertainty for Ocalcite was were pronounced and spanned the width of M 2 layer, usually 0.51 ‰. intersecting visible notches on the external surface of the shell. δ18 The correlation between measured and calculated Ocalcite Minor-growth lines were observed in varying intervals of micro- were strong and significant for both modern specimens growth increments (circalunidian); and micro-growth increments (R2 = 0.71; p < 0.0001 and R2 = 0.69; p < 0.0001 for CW1 and were subdivided by observed micro-growth lines (circatidal). The CW2, respectively) (Fig. 3). In the linear regression model, slopes micro-growth increment widths ranged from 6.32 µm to were 0.39 and 0.37 for CW1 and CW2, respectively. The variance 61.74 µm, but were typically less pronounced and wider for neap δ18 δ18 in Ocalcite is likely a combined signal of Oseawater and SST. tides in comparison to spring tides, which were very pronounced We modeled reconstructed SST profiles for the historical shell and narrow. The average micro-growth increment widths for across a range of ecologically relevant salinity values and found an each specimen were 22.54 µm (CW1), 20.67 µm (CW2), and 18 effect of evaporation on δ Ocalcite (Fig. 4). The reconstructed SST 13.69 µm (BPBM). The estimated age for modern and historical values changed by 0.84 ± 0.04 °C psu−1. Temperature thresholds specimens was 2 years (CW1 and CW2) and 5 years (BPBM), (Tmin and Tmax) were most biologically relevant at salinity of 42 respectively. These age estimates were based on the number