Limited evidence for species‐specific sensitivity of temperature‐dependent fractionation of oxygen stable isotope in biominerals: A meta‐analysis

Responses of animals to individually experienced environmental conditions define the viability and distributions populations (Faillace et al., 2021). For aquatic ectotherms, water temperature is a key driver individual behaviour condition, due its direct indirect effects on physiological rates availability oxygen food (Rubalcaba 2020). Acquiring precise accurate data thermal experience organisms remains challenge. In mobile such as fish, by an may differ markedly from estimates derived fixed location loggers or remotely sensed (Collas 2019). Consequently, time-resolved records exposure histories are needed accurately assess responses variations in their environment, understand life-stage habitat partitioning predict vulnerability future climate change scenarios. Electronic recorders (e.g. tags) implanted into attached onto can provide high-resolution information temperatures (Block 2001). Most recorders, however, only be larger individuals have limited battery life. Data storage tags often require physical recovery download data, rate successful low (De Pontual 2012). Loggers also contribution reconstruct past earlier than 1980s, corresponding beginning widespread use. The associated costs mean that relatively few monitored/tagged, retrospective analysis impossible (Gallagher 2018). ratio stable isotopes (expressed δ18O values) biominerals, especially calcium carbonate biominerals mollusc shells, coral skeletons fish otoliths, acts natural proxy dependence equilibrium fractionation (18O 16O) during precipitation (Kim 2007; Urey 1951). oxygen-stable isotope ratios vary relation ambient isotopic modulated at time deposition. example, thermometry biomineral carbonates unicellular foraminifera used primary source for reconstruction deep ocean (Zachos 1994), underpinning models global sensitivity. As many grow continuously throughout individual's lifetime, variation composition studied structure represents chronological record this condition. Oxygen had been extensively (Dorval 2011; Godiksen 2012), cephalopods (Martino 2022) other taxa. absence full mechanistic model exchanges those taxa, use dependent statistical determination relationship between mineral. Isotopic dynamics abiotic, inorganic mineral growth determined through experimental experiments, providing linking This expressed negative linear with intercept describing separation slope sensitivity 2007). multicellular organisms, biomineralization typically occurs compartmentalized space, more less separated (Gilbert 2022), potential additional and/or kinetic influences ultimately biomineral. Such (often packaged ‘vital effects’) include, but not to, organisms' metabolism), transport across membrane boundaries mixing isotopically distinct sources within body. While consistent exists, date there consensus strength different sources. If does indeed consistently among taxa (or life stages), specific equations will calculations, deviation temperature-dependent hold organism physiology. Conversely, if essentially conserved application estimate simplified, cost metabolic signals. Here, we address problem drawing published relationships values, wide range context study, proposed two main equations: species biology conditions. biology, inherent should emerged multiple evolutive origins species' process. Hence, mechanisms could introduce variability equation variables (1) membranes, (2) differential crystal forms (3) First, vertebrates (primarily form dissolved oxygen, bicarbonate ions) must initially pass numerous barriers gill gut lining. blood plasma, exchanged products cellular respiration, influencing resulting values. case cephalopods, ions then exported saccular epithelium endolymph before finally being incorporated growing surface otolith statoliths (Campana, 1999; De & Geffen, 2003). Secondly, biomineralization, temperature-driven kinetics deposition follow predictions made thermodynamics 2007), unless physical–chemical factors strain imperfections significantly disrupt fractionation, which was potentially identified corals (Juillet-Leclerc, Finally, while most studies assume single (ambient water), body actually contains molecules three sources; water, diet released respiration. these present differing proportions depending physiology conditions, quantification respective influence better defined (Magozzi Experimental additionally apparent interspecific equations. Thus far, approaches type) dominated literature, rearing under controlled (Owen 2002), captive monitored situ mesocosm, cage aquaculture pens (Bugler 2009) capture wild specimens experiencing divergent—and preferably well-monitored—thermal (Aharon, 1983). likely replicate target studies, laboratory offer Other include investigated, analytical methods measure environment salinity) removal organic material (especially protein) carbonate. Organic removal, selected method heating peroxide digestion), has shown effect values (Key Jr 2020), no directionality identified. Diet another factor results, generally reported explicitly considered here. With work, aim identify systematic increase understanding biomineralization. Our study aims refine estimation equations, represent useful tool assessment impact ecosystems. We conducted review literature using ‘Web Science’ search engine (WOS) January 2022 (range 1950–2022). query built concepts; biogenic carbonates, isotopes, estimation, following string: (otolith OR bone shell aragonite) AND (‘oxygen isotope*’ d18O ‘oxygen 18’) (thermal* temperature). provided 989 records, 12 articles were added based cross-referencing, consisted examination list references citing (‘cited by’ section publisher's website article's Google Scholar record). A study's suitability inclusion/exclusion meta-analysis evaluated predetermined criteria (Figure 1) preferred reporting items reviews meta-analyses (PRISMA) best practices statement (Moher 2009). Of 1001 first articles' title abstract, where whether included estimating (896 excluded). remaining (105) retrieved assessed text level confirm objectives stated abstract concordant described (53 excluded), minimally required expression equation. texts read entirely (52 articles) final selection pre-determined eligibility criteria; formulation: calculation (either Equation 1 3) fractionation: formulation merely response (19 explicit consideration critical subsequent meta-analytical models, comparison coefficients formulations, nature regression strongly diverts polynomial equations), risks inducing errors conclusions. total 37 (27 original WOS search, 6 cross-referencing 4 suggested reviewers) retained extraction analyses 1). Details extracted materials results sections each article. Specifically, stage (larvae, juveniles adults), type analysed shell, otolith, statolith), (aragonite calcite), approach (wild sampling, rearing), procedure matter matrix none, heating, peroxide), number (study size), maximum minimum temperature, experiment (freshwater saltwater). Temperature-dependent slopes, intercepts, standard error (both Equations 3, when available) results. 3 estimated Patterson (1998) raw article reported. Additionally, four (Burbank 2020; Kastelle 2022; Storm-Suke Willmes 2019) corrected version, linked divergent 3. Those both relative same (Vienna Peedee Belemnite, VPDB), rather VSMOW samples commonly conducted. resulted large difference intercepts compared rest dataset. correction intercepts—which influenced error—and all presented (14 studies). (bcorrected = b * −0.044 + 2.53, R2 0.69) convert biased post-hoc approximation similar intercept. computation any they published. Phylogenetic distances COI sequences Genebank repository. species-specific gene sequence since divergence, test evolutionary accounting process Sequences aligned msa R package (Bodenhofer 2015) squared root pairwise identity seqinr (Charif Lobry, distance transformed continuous metric axis nonmetric multidimensional scaling (NMDS), computed function metaMDS vegan (Oksanen 2017). Six either slopes (meta-analysis 2), 4) correlation 5 6). assessing (1,3 5) mixed fitted via restricted maximum-likelihood moderators high-level name (i.e. coral, crustacean, mollusc, sponge), binary categorical variable [<2] saltwater [>30]) larva, juvenile adult). unique identifier random consider non-independence generated study. (2, 6) (laboratory capture), (numeric, 3.8–27.1) sample pre-treatment (no yes) along sizes unbiased (Olkin Pratt, 1958). Effect log-transformed size (Nakagawa missing sampling variance terms (vi, n 24 missing) imputed vi (8.71*10−4, 19) divided (Ne) (Koricheva 2013). coefficients' calculated Fisher's r-to-z coefficient Pearson's R2. Two carried out subset dataset, fishes (n 18 studies), finer-scale moderators; phylogenetic distance, (larval, adult) 7) 8). Sampling 8 19). Meta-analyses 7 meta-analytic models. All calculations metafor (Viechtbauer, 2010). After extraction, 53 2). frequently teleost (‘fish’, molluscs (including cuttlefish, 14 (12 equations) (6 equations). Comparatively groups sponges (two spicules). statocysts Cyprideis torosa (Bodergat 2014) included, representing ‘crustacea’. experiments (43 freshwater (10 No brackish (see Supporting Information S1). Slightly half wild-sampled (28 25 one combined dataset average size—which isotopes—was 54 (SD 22.2, ranging 10 470). ranged −0.17 0.16, (mean −0.12), crustacean 0.04), 0.06), sponge 0.09) 0.15) ordered NMSD axis. checked artefacts first. correlated publication (F1,49 1.14, p 0.29), 1.30, 0.526), (F1,47 0.31, 0.58), suggesting temporal trends bias). Observation funnel plots did show sign pronounced asymmetry bias, precluding necessity imputing sizes. Meta-analysis 2 (effect slopes) showed significant moderators, groups, (freshwater/saltwater) 3). among-studies (σ2) 0.0, residual heterogeneity (Cochran's QE39 2.42, 1.00). Similarly, neither (laboratory/captive rearing, carbonate, content slopes. Life stage, adult specimens, small positive When (ANOVA, F1,38 28.86, < 0.0001). Unlike 4). Experiment wild-capture having higher small, yet coefficients, our accuracy 5). However, affected 6), reduction (compared lower predictive power (Supporting S2). 7, saltwater) nor There non-significant QE12 0.33, 1.00) 8), closely related marine benthic predators Atlantic Cod, Gadus morhua), diadromous salmonids, e.g. Arctic Char, Salvelinus alpinus, cyprinids). significant, S3). intercept; adults larvae Using framework, observed parameters aimed water. Thermal sensitivities (equation highly variation. sampling) regressions. overall, subject except effect, lower-than-average Analyses well saltwater), These insights wider taxonomic spectrum. various observations help knowledge gaps thermometry. equation) aspects biology—including environment—and (consistent hypothesis H1). highlights weaknesses term effects’ explain differences median (−0.209‰*T) indistinguishable synthetic aragonite (−0.21‰*T; Kim 2007) given uncertainties (−0.288‰*T; Beck 2005), dominate dependency biological disequilibrium sensitivity, suggest probably negligible, least practical implication result individuals) confidence that, equation, deviating caution. Any strong indicate unknown hidden play, condition marked Notably, like rate, IRMS facilities micro-milling, sectioning others), acid digestion reaction CO2 inconsistently Variations (accuracy), coefficient. widely variety difficult cases, details missing, partially very precision, lack detail precludes clear factors. 80% otoliths specified pair sagitta, lapillus asteriscus) used. sagitta usually largest pairs, specified, it assumed analysed, exceptions Morissette choice implications pairs composed aragonite, vaterite calcite) exhibit chemical affinity trace elements (Budnik Campana, Macdonald Missing details, found responsible substantial proportion unexplained coefficients. According exerted laboratory-based wild-caught specimens. H3 emphasizes offers finer control monitoring variability, uncertainty. Better further large-scale reviews. variation, experimental, remain beyond analysis, because constraints noted above. It important note authors applied erroneous conversion VPDB reference (δ18OVPDB 0.99978* δ18OVSMOW − 0.22, incorrect attributed Friedman O'Neil (1977). (1977) δ18OVPDB 0.970068 – 29.94. appears propagated typographical Høie al. (2004) subsequently reused studies. Unfortunately, tested equation(s) used, any, 56% analysis. International Union Pure Applied Chemistry (IUPAC) guideline 0.97001 29.99 (Brand 2014; recently adopted accordance suite IUPAC science. frequent (VSMOW vs. addressed post hoc possible Section Use appropriate standards critical, analysing calcite NBS19 standard, reaction-temperature dependencies Future fully describe material, phosphoric acid, without factor, corrections made. emerging secondary ion mass spectrometry (SIMS) addition (IRMS) surface-based SIMS unavoidably contained carbonate-bound contributing offset δ18O-derived (Hane Rollion-Bard Marin-Carbonne, 2011). over acquisition (Shirai 2018; 2019), choice, association H2. exceeded 3‰, equivalent inferred c.12°C common although seems support dynamics. Corals, particular, groups. shallow-water striking δ13C autotrophic heterotrophic 2022). Biomineralization undoubtedly evolved independently occasions, conclusions group others. Isotope processes well-studied 1983; Bohm 2000) recent work implies primarily arise occurring calcification (the calcifying fluid fractionation) organism) per se. (lower temperature), within-organism photosynthesis (increasing microstructural scale Since predictors investigated corals. considering fishes, still 1‰ (equivalent c. 4°C al.'s (2007), showing long thermometry, routinely referred (Darnaude Kozdon overall spacing controlling part reducing species, case, fish. Both (but slopes), H4. (phylogeny environment) partly correlated, index corresponded mostly species. interpretation marine) origin diverging osmotic state exchange (Knezovich, 1992; Loewen 2016). Marine ingest seawater, leading flux water—which value 0 ± 0.6‰—and, thus internal pool would By contrast, hypertonic limit ingestion freshwater. (−6.1 4.2‰; Pfister seawater (~0‰ 0.6‰), greater flux. expected constant −3.5‰ (Kreuzer-Martin 2005; Li 2016), predicted intercept, position continuum, clear, available Variation stages environments. Experiments salinity treatments shed light phenomenon clarify We, therefore, argue balance osmoregulation, principal inter-specific fractionation. conservation broad generalized formulated about coral) Based draw realistic term. (Table reasonable substitute species- taxon-specific lacking. produces unrealistic estimations temperature. term, produced laboratory/captive summary, find argument statistically taxon-related differences. Among functional traits osmoregulation fishes. terms. robust, consistency systems therefore changes experimentally. focussed here explore animal physiology, particularly osmoregulation. is, knowledge, attempt generalize unrelated meta-analyses, remained extract descriptions non-negligible originated design choices contribute formulae, errors, spectrometer protocol. demonstrates importance implementing practices, scientific media (articles talks), promote sharing accurate, open conceived ideas designed methodology; Olivier realized review, data; conceptualized coded them led writing manuscript. contributed critically drafts gave approval publication. want thanks colleagues insightful discussions project, notably Peter Grønkjær, David Deslauriers Pascal Sirois. OM grateful Émilie Champagne her guidance conducting meta-analysis. Salary contributions AMS UKRI Leaders Fellowship [MR/V023578/1]. acknowledge anonymous reviewers Aaron Ellison comments previous version. program Ressources Aquatiques Québec. None conflict interest declare. peer history https://www.webofscience.com/api/gateway/wos/peer-review/10.1111/2041-210X.14122. codes, datasets figures freely accessible Borealis repository, link: https://doi.org/10.5683/SP3/JRSOO8. Table S1. meta-analysis, listing name, latin structures, types, dependant S2. Outputs general (meta-analyses 1, 2, moderators’ size, (SE), z interval (CI) bounds S3. 8) Please note: publisher functionality supporting supplied authors. queries (other content) directed author