From 26 to 28 June 2021, an unprecedented atmospheric heatwave coincided with the lowest low tides of the year in the Pacific Northwest (i.e., the region consisting of the northwestern corner of the contiguous United States and southwestern Canada). This event broke numerous all-time record high temperatures throughout the region and would have been virtually impossible without human-caused climate change (Philip et al., 2021). During and immediately following the event, many scientists, resource managers, and members of the public reported dead and dying marine organisms, including barnacles, mussels, clams, and oysters, on intertidal beaches throughout the region (Figure 1). These observations raised alarms among many stakeholders because these species support important commercial, subsistence, and recreational fisheries and are major constituents of nearshore ecosystems.

In response, we developed and deployed a semi-quantitative survey to a multiorganization network of collaborators to rapidly assess the postheatwave condition of nearshore invertebrates across the coastal Pacific Northwest and inland waters of Washington state and British Columbia known collectively as the Salish Sea (e.g., Strait of Juan de Fuca, Puget Sound, and the Strait of Georgia). Our goal was to inventory shellfish condition observations across a broad geographic scale to document the effects of the extreme heatwave and to serve as a starting point for future detailed quantitative research and monitoring. We asked local scientists (academic, tribal, and state and federal agencies) to rate shellfish condition in terms of the degree of postheatwave mortality (or, conversely, resilience) relative to what they would consider typical based on their prior experience with specific sites and species at the same time of year. We directed participants to only submit observations from locations where they possessed extensive local knowledge. In these situations, expert knowledge is a surrogate for empirical data collection because practitioners can develop quantitative information from the synthesis of their own observations, knowledge, and mental models of the system in question (Drescher et al., 2013). We used a five-point postheatwave rating (PHWR) system to evaluate the condition of organisms: 1 = much worse than normal, 2 = worse than normal, 3 = normal, 4 = better than normal, 5 = much better than normal. Further information on our survey methods and rationale is given in Appendix S1.

We collected 203 observations from 108 sites spanning the outer and inner coasts (Figure 2), covering 24 species. Here we focus our discussion on acorn barnacles (Balanus glandula), California and so-called bay mussels (Mytilus californianus, Mytilus spp.), butter clams (Saxidomus gigantea), cockles (Clinocardium nuttallii), native littleneck clams (Leukoma staminea), naturalized Manila clams (Ruditapes philippinarum), Olympia (Ostrea lurida) oysters, and naturalized Pacific oysters (Crassostrea gigas = Magallana gigas). We define bay mussels generally as Mytilus spp. due to difficulty differentiating M. trossulus, M. edulis, and M. galloprovincialis in the field and because of reports of hybridization between M. trossulus and M. galloprovincialis (E. Carrington, personal communication, July 26, 2021; C. A. Speck, unpublished). These species are conspicuous, well studied, and represent the majority of our observations (N = 171). They are also ecologically important, span a range of intertidal habitats, and support highly valued recreational, commercial, subsistence, and ceremonial harvest. All observations are reported in archived data (Raymond, 2022). We also note that we consider Manila clams and Pacific oysters as “naturalized” because they were introduced to the region ~100 years ago for aquaculture purposes but have established naturally reproducing populations.

Region-wide patterns of intertidal shellfish conditions reflect environmental gradients, the natural history of the species, and the intersection between them. A key factor that may contribute to these observed patterns is the difference in the timing of low tide over the days of the heatwave (Figure 3; Appendix S1: Figure S1). The outer coast of Washington state and British Columbia experienced low tide ~4 h before the inner coast sites of the Salish Sea, where low tide occurred very close to solar noon. Ambient air temperatures were also much higher at inner coast sites, potentially compounding the effects of a later low tide (Figure 3). Wave exposure, which is generally greater on the outer coast than the inner coast, may have moderated postheatwave ratings, along with the timing of low tide. The difference in the physical environment (tide timing and exposure) intersects the natural history of many of our focal species. For example, California mussels, which are almost exclusively found at outer coastal sites, largely avoided negative impacts (i.e., better condition) as opposed to congeneric bay mussels, which are found in more wave-protected inner coast sites and were more likely to suffer negative impacts (Figure 2c,d). Furthermore, species found higher in the intertidal zone, such as acorn barnacles, were generally found in worse condition than species found lower in the intertidal zone, such as clams and oysters (Figure 2).Though we are not able to separate species-specific effects here, this pattern highlights the range of thermal environments experienced by barnacles, mussels, clams, and oysters across the region. Thermal conditions at sites within the western Strait of Juan de Fuca (Figure 2) and along the outer coast are often buffered by winds, wave splash, or fog, and the only unusual barnacle mortality observed in this region was restricted to one less wave-exposed, southeast-facing shoreline (Figure 2b).

Observed postheatwave condition of bivalves, including butter clams, cockles, native littleneck clams, Manila clams, and Olympia and Pacific oysters, varied among species in accordance with aspects of their natural history (Figure 2e–j). Butter clams, which often burrow >15 cm deep in sediment and live at lower tidal elevations than other clam species (Dethier, 2006), were less affected by the heatwave than surface-dwelling cockles. Being buried deeper in the sediment, butter clams likely were buffered from high solar irradiance, high surface temperature, and high desiccation stress relative to animals such as cockles living on or near the surface. However, we did observe a range in butter clam condition among sites separated by ~30 km, indicating that local scale factors may also contribute to postheatwave clam condition. Manila and native littleneck clams varied in observed condition, but the low sample size for these species, owing to the opportunistic nature of our sampling or declining population size of native littleneck clams (J. Barber, unpublished), makes drawing broader conclusions difficult. Olympia oysters, which tend to be found lower in the intertidal zone (White et al., 2009), were less affected by the heatwave than Pacific oysters (Figure 2i,j). However, both oyster species experienced a range of observed conditions, again indicating the likely importance of local scale factors. Notably, more Pacific oysters were observed in poor condition in more southerly latitudes, which coincided with low tide and peak air temperatures. This may reflect the difference in air temperatures across the region, especially in southern Puget Sound, where air temperatures were greater than in northern Puget Sound (Figure 3). Pacific oyster observations near the Duckabush and Dosewallips estuaries were considered normal compared to other nearby locations in southern Hood Canal (Figure 2j). Observations by several contributing participants noted substantial increases to river flows associated with snow melt during the heatwave at these and other locations. Given these observations, it is possible that increased flow of surface water or groundwater could have provided thermal refuge for species at low tide; this requires further investigation.

Thermal stress is a common and well-studied factor in ecology, a major structuring force in intertidal and nearshore ecosystems (Connell, 1961; Harley & Helmuth, 2003), and can affect the recruitment and energetics of organisms and the prevalence of biotoxins and infectious agents (references below). For example, clam populations in the region exhibit population synchrony at relatively large spatial scales, and adult clam biomass likely reflects larval recruitment success 4 years prior (Barber et al., 2019). Given that all of the bivalve species discussed here were likely reproductive during the heatwave (Anderson et al., 1982), it is possible that high mortality in certain species (e.g., cockles) may manifest itself in reduced adult populations in ~4 years. Because clam recruitment is naturally episodic (Hunt & Scheibling, 1997), attributing this event to a loss in a year class will require multiple years of population monitoring. Sublethal, but extreme, ambient temperatures also have a direct effect on the metabolism of marine invertebrates (Hand & Hardewig, 1996). Therefore, it is reasonable to expect that many organisms were under increased metabolic stress during the heatwave, potentially leading to delayed mortality or reduced overall condition, as documented in Manila and related clams (Macho et al., 2016). Unmeasured biological factors, such as biotoxins or infections, also could have increased susceptibility to thermal stress-induced mortality in some species (Go et al., 2017; Green et al., 2019; King et al., 2021). For example, Pacific oysters with infections of the bacteria Vibrio sp. have reduced thermal tolerances compared to uninfected individuals (Wendling & Wegner, 2013).

Multiple factors and organismal traits can enhance or mitigate thermal stress in intertidal species, including morphology (body size and shell color), behavior (aspect), and environment (substrate, wind, and proximity to shade or freshwater runoff). Water quality factors, including pH, turbidity, and salinity, may also contribute to bivalve stress and mortality (Dethier et al., 2019). These unmeasured factors may have influenced observed postheatwave condition and may have delayed mortality for many species. Thus, further investigation into these factors and how they may have modulated thermal stress during this and future heatwaves will be critical for increasing our understanding of the effect of extreme heat events on intertidal organisms in the region. Moreover, the information could prove useful for identifying local climate refugia and incorporating climate adaptation into shellfish management. Long-term population and environmental monitoring data will be particularly useful in separating heatwave effects from normal population fluctuations.

Our observations, though coarse, demonstrate the widespread negative impacts post heatwave to intertidal species across the waters of the Pacific Northwest and Salish Sea. Our broad survey suggests that the June 2021 heatwave may have far-reaching and potentially multiyear effects on nearshore ecology, cultural connections, and fisheries. These observations represent just the beginning of our understanding of how the heatwave may have affected intertidal species and may serve as a bellwether for future extreme temperature events, which are predicted to become more frequent and more severe in a warmer climate (IPCC, 2021). The present work highlights heatwave responses by naturally occurring or enhanced sessile marine invertebrates; yet some of these species support a robust aquaculture industry in the Pacific Northwest. Identifying impacts on farmed shellfish was beyond the scope of this effort, and such impacts have yet to be examined. Continued population, recruitment, disease, and environmental monitoring and research will be needed to accurately assess species, community, and ecosystem responses, as well as impacts on human use. This project may also serve as a model for the power of research across a broad coalition of partners and as a method to rapidly assess unique or short-lived weather events. The range of expertise, perspectives, and geographic location of project partners enabled a research product that will serve many user groups and has laid the groundwork for future collaborations.

2021年6月26日至28日，前所未有的大气热浪与西北太平洋地区（即美国西北角和加拿大西南部组成的地区）发生了全年最低的低潮。这一事件打破了整个地区的多项历史高温记录，如果没有人为造成的气候变化，这一事件几乎是不可能发生的（Philip et al., 2021 ）。事件期间和事件发生后不久，许多科学家、资源管理者和公众报告称，整个地区的潮间带海滩上出现了死亡和垂死的海洋生物，包括藤壶、贻贝、蛤和牡蛎（图 1）。这些观察结果引起了许多利益相关者的警惕，因为这些物种支持重要的商业、自给和休闲渔业，并且是近岸生态系统的主要组成部分。

作为回应，我们开发并向多组织合作者网络部署了一项半定量调查，以快速评估太平洋西北沿海以及华盛顿州和不列颠哥伦比亚省内陆水域（统称为萨利希海）的近岸无脊椎动物的热浪后状况（例如，胡安德富卡海峡、普吉特海湾和乔治亚海峡）。我们的目标是在广泛的地理范围内清查贝类状况观察结果，以记录极​​端热浪的影响，并作为未来详细定量研究和监测的起点。我们要求当地科学家（学术、部落、州和联邦机构）根据热浪后的死亡率（或者相反，复原力）相对于他们根据他们之前在特定地点和地区的经验所认为的典型情况，对贝类状况进行评级。一年中同一时间的物种。我们指示参与者仅提交来自他们拥有丰富当地知识的地点的观察结果。在这些情况下，专家知识可以替代经验数据收集，因为从业者可以通过综合自己的观察、知识和相关系统的心智模型来开发定量信息（Drescher 等， 2013 ）。我们使用五点热浪后评级（PHWR）系统来评估生物体的状况：1 = 比正常情况差得多，2 = 比正常情况差，3 = 正常，4 = 比正常情况好，5 = 比正常情况好得多。有关我们调查方法和理由的更多信息，请参阅附录 S1。

我们从横跨外海岸和内海岸的 108 个地点收集了 203 个观测值（图 2），涵盖 24 个物种。在这里，我们重点讨论橡子藤壶 ( Balanus mudula )、加利福尼亚州和所谓的海湾贻贝 ( Mytilus californianus , Mytilus spp.)、黄油蛤 ( Saxidomus gigantea )、鸟蛤 ( Clinocardium nuttallii )、本地小颈蛤 ( Leukoma staminea )、归化马尼拉蛤 ( Ruditapes philippinarum )、奥林匹亚 ( Ostrea lurida ) 牡蛎和归化太平洋牡蛎 ( Crassostrea gigas = Magallana gigas )。我们通常将海湾贻贝定义为贻贝属（ Mytilus spp）。由于在现场区分M. trossulus 、 M. edulis和M. galloprovincialis存在困难，并且有报道称M. trossulus和M. galloprovincialis之间存在杂交（E. Carrington，个人通讯，2021 年 7 月 26 日；CA Speck，未发表） ）。这些物种很引人注目，经过充分研究，代表了我们的大部分观察结果 ( N = 171)。它们在生态上也很重要，跨越一系列潮间带栖息地，并支持高价值的娱乐、商业、生存和仪式收获。所有观察结果均在存档数据中报告（Raymond， 2022 ）。我们还注意到，我们认为马尼拉蛤和太平洋牡蛎是“归化的”，因为它们在大约 100 年前被引入该地区用于水产养殖目的，但已经建立了自然繁殖的种群。

全区域潮间带贝类状况的模式反映了环境梯度、物种的自然历史以及它们之间的交叉。可能导致这些观察到的模式的一个关键因素是热浪期间低潮时间的差异（图 3；附录 S1：图 S1）。华盛顿州和不列颠哥伦比亚省的外海岸比萨利希海的内海岸地点经历了大约4小时的低潮，那里的低潮发生在非常接近太阳正午的时候。内海岸地区的环境气温也高得多，可能会加剧后来退潮的影响（图 3）。外海岸的波浪暴露程度通常高于内海岸，这可能会影响热浪后的评级以及低潮的时间。物理环境（潮汐时间和暴露）的差异与我们许多焦点物种的自然历史相交叉。例如，加州贻贝几乎只出现在外海岸地区，与同属海湾贻贝相比，它们在很大程度上避免了负面影响（即更好的条件），而同类海湾贻贝则出现在受波浪保护的内海岸地区，并且更有可能受到影响。负面影响（图2c、d）。此外，在潮间带较高处发现的物种（例如橡子藤壶）通常比在潮间带较低处发现的物种（例如蛤和牡蛎）状况更差（图 2）。尽管我们无法区分特定物种这种模式突出了该地区藤壶、贻贝、蛤和牡蛎所经历的热环境范围。 胡安德富卡海峡西部（图 2）和外海岸的热条件经常受到风、浪花或雾的缓冲，在该地区观察到的唯一不寻常的藤壶死亡仅限于少一波——暴露的、面向东南的海岸线（图2b）。

观察到的双壳类动物的热浪后状况，包括黄油蛤、鸟蛤、本地小颈蛤、马尼拉蛤、奥林匹亚牡蛎和太平洋牡蛎，根据其自然史的各个方面，物种之间存在差异（图2e-j）。黄油蛤通常在沉积物中挖 >15 厘米深，生活在比其他蛤类物种更低的潮汐高度（Dethier， 2006 ），与表层蛤相比，受热浪的影响较小。黄油蛤被埋在沉积物中较深的地方，相对于生活在地表或附近的动物（如鸟蛤），它们可能会免受高太阳辐照度、高表面温度和高干燥压力的影响。然而，我们确实观察到相距约 30 公里的地点之间的黄油蛤状况存在一定范围，这表明局部尺度因素也可能对热浪后蛤状况产生影响。马尼拉和本地小颈蛤的观察条件有所不同，但由于我们采样的机会主义性质或本地小颈蛤种群规模的下降（J. Barber，未发表），这些物种的样本量较小（J. Barber，未发表），使得得出更广泛的结论变得困难。奥林匹亚牡蛎往往位于潮间带较低的位置（White 等人， 2009 年），与太平洋牡蛎相比，受热浪的影响较小（图 2i，j）。然而，这两种牡蛎物种都经历了一系列观察到的条件，再次表明当地规模因素的可能重要性。值得注意的是，在更南纬地区观察到更多状况不佳的太平洋牡蛎，这些地区恰逢低潮和最高气温。这可能反映了整个地区气温的差异，特别是在普吉特海湾南部，那里的气温高于普吉特海湾北部（图 3）。 与胡德运河南部其他附近地点相比，Duckabush 和 Dosewallips 河口附近的太平洋牡蛎观测结果被认为是正常的（图 2j）。几位贡献参与者的观察指出，在这些和其他地点的热浪期间，与融雪相关的河流流量大幅增加。鉴于这些观察结果，地表水或地下水流量的增加可能为低潮时的物种提供了热避难所；这需要进一步调查。

热应力是生态学中一个常见且经过充分研究的因素，是潮间带和近岸生态系统的主要结构力（Connell， 1961 ；Harley＆Helmuth， 2003 ），并且可以影响生物体的补充和能量以及生物毒素和传染性病原体的流行。代理（参考下文）。例如，该地区的蛤种群在相对较大的空间尺度上表现出种群同步性，成年蛤生物量可能反映了 4 年前幼虫招募的成功（Barber 等， 2019 ）。鉴于这里讨论的所有双壳类物种都可能在热浪期间繁殖（Anderson 等人， 1982 ），某些物种（例如鸟蛤）的高死亡率可能会在大约 4 年内表现为成虫数量的减少。由于蛤的招募自然是偶发性的（Hunt & Scheibling， 1997 ），因此将此事件归因于一年级的损失将需要多年的种群监测。亚致死但极端的环境温度也对海洋无脊椎动物的新陈代谢有直接影响（Hand＆Hardewig， 1996 ）。因此，可以合理地预期，许多生物体在热浪期间承受着更大的代谢压力，可能导致死亡延迟或整体状况下降，正如马尼拉和相关蛤中所记录的那样（Macho等人， 2016年）。未测量的生物因素，例如生物毒素或感染，也可能增加某些物种对热应激引起的死亡的敏感性（Go 等人， 2017 年；Green 等人， 2019 年；King 等人， 2021 年）。 例如，太平洋牡蛎感染了弧菌属细菌。与未感染个体相比，热耐受性降低（Wendling & Wegner， 2013 ）。

多种因素和生物特征可以增强或减轻潮间带物种的热应激，包括形态（体型和外壳颜色）、行为（方面）和环境（底质、风以及接近阴影或淡水径流）。水质因素，包括 pH 值、浊度和盐度，也可能导致双壳类应激和死亡（Dethier 等， 2019 ）。这些未测量的因素可能影响了观察到的热浪后的状况，并可能延迟了许多物种的死亡。因此，进一步研究这些因素以及它们如何在这次和未来的热浪期间调节热应力对于加深我们对极端高温事件对该地区潮间带生物影响的了解至关重要。此外，这些信息对于识别当地气候保护区并将气候适应纳入贝类管理很有用。长期人口和环境监测数据对于区分热浪影响和正常人口波动特别有用。

我们的观察虽然粗略，但表明热浪过后对西北太平洋和萨利什海水域的潮间带物种产生了广泛的负面影响。我们的广泛调查表明，2021 年 6 月的热浪可能会对近岸生态、文化联系和渔业产生深远且可能多年的影响。这些观测结果只是我们了解热浪如何影响潮间带物种的开始，并可能作为未来极端温度事件的风向标，预计在气候变暖的情况下，这些事件将变得更加频繁和更加严重（IPCC， 2021 ）。目前的工作强调了自然发生或增强的固着海洋无脊椎动物的热浪反应；然而，其中一些物种支持了太平洋西北地区强劲的水产养殖业。确定对养殖贝类的影响超出了这项工作的范围，而且此类影响还有待研究。需要持续进行人口、补充、疾病和环境监测和研究，以准确评估物种、群落和生态系统的反应以及对人类使用的影响。该项目还可以作为广泛合作伙伴联盟研究力量的模型，并作为快速评估独特或短暂天气事件的方法。项目合作伙伴的专业知识、观点和地理位置的范围使得研究产品能够服务于许多用户群体，并为未来的合作奠定了基础。