Eelgrass ecosystem collapse and social-ecological regime shift driven by hydropower development and climate change

Domain: chemistry
Published: 2026-02-18
Editorial outcome: minor_revision

Abstract
Global declines in coastal habitats and wildlife have devastating consequences for Indigenous Peoples. In some places, hydropower development has environmental impacts that contribute significantly to coastal habitat loss. As development is rejuvenated for the carbon-neutral transition, mitigation of further coastal habitat impacts depends on assessing the relative and interactive effects of climate change and hydropower development. Here, we follow a detection and attribution framework to understand the collapse and limited recovery of a social-ecological system including eelgrass (Zostera marina, shikaapaashkw), geese (Branta spp., niskandiyiwaapuwaau), and Cree (Eeyou) in subarctic eastern James Bay, Canada (Eeyou Istchee). Informed by historical observations, Indigenous knowledge, and scientific research, we attribute the collapse of eelgrass and shifts in the associated social-ecological system to ecological effects of hydroelectric development (1978-1996), which degraded local environments causing eelgrass declines. Climate-driven extreme events (1998 onward) compounded losses and ecological feedbacks extended eelgrass declines all along the coast. Eelgrass recovery today appears limited by poor water clarity, altered sediments, hydrologic changes from development, and a new climate regime. Eeyou have adapted by shifting their relationships with the coastal habitat. Comprehensive assessments for hydropower developments should explicitly consider coastal social-ecological dynamics and the possible compounding impacts of climate change.

Introduction
Coastal habitats have supported human communities for hundreds of thousands of years. Coastlines provide food, shelter, and access to marine and freshwater environments that define the culture, livelihoods, and identities of Indigenous Peoples who have lived along marine shorelines for countless generations1. The destruction and loss of coastal habitats worldwide during the past century2 thus has gravely affected both social systems and ecosystems3. Coastal habitat protection, management and restoration can contribute to climate mitigation and adaptation4,5, biodiversity conservation6, and Indigenous self-determination. However, the interaction of local and global environmental change to cause habitat loss and prevent habitat recovery4 is a critical knowledge gap compromising current coastal restoration efforts and preventing true cost accounting of various development activities.

Seagrasses are foundation species in many coastal ecosystems. They provide critical habitat for marine and semi-aquatic wildlife, such as waterfowl, and the reliable, nearshore wildlife harvesting opportunities in seagrass ecosystems have been particularly important for many coastal Indigenous Peoples’ food security and cultural continuity (cf. 5–9). Recently, seagrass ecosystems have also gained attention because of their tendency to accumulate carbon (“blue carbon”), in addition to being biodiversity hotspots. Protecting and restoring degraded seagrass ecosystems may thus contribute to numerous benefits for both Indigenous and non-Indigenous coastal communities, as well as for the ecosystems themselves10–12.

Many seagrass populations around the globe have massively declined in the past century. Few have fully recovered to their historical depth and spatial extents, although North Atlantic eelgrass lost to widespread wasting disease in the 1930s is considered naturally recovered in many areas, and recovered as a result of active restoration in other areas13,14. Incomplete recovery of degraded seagrass ecosystems is often characterized by lower shoot density15, reduced depth extent16, and/or reduced spatial extent16–18 of meadows relative to historical observations, as well as reduced usage by wildlife and ecological functions such as carbon storage19. The reasons for failure to fully recover can be unclear, especially when proximate causes of declines and related environmental conditions have improved18–21.

Among the potential ultimate causes of ecological changes in seagrass ecosystems are local and regional land use and development activities in watersheds that alter riverine fluxes of freshwater, nutrients, and sediment, and cause localized deterioration of water quality and poor water column light conditions due to elevated concentrations of suspended sediments13,14. Sedimentation is a well-recognized stressor because it can disrupt the natural feedback loops that keep seagrass meadows healthy: i.e., excess sediment makes water more turbid, reducing light availability and consequently slowing seagrass growth22,23. Dams are well-know drivers of changes to downstream river flows, nutrient ratios, and sediment loads24–26. However, explicit consideration of how seagrass ecosystems may be impacted by dam construction and operation is lacking. Sixty-three percent of the world’s very long rivers are no longer free flowing27, and many of the remaining rivers are planned for impoundment28. Most studies on the ecological impacts of hydroelectric development focus on river and reservoir systems25–27, while impacts on coastal ecosystems remain unclear.

Here, we present a synthesis of recent evidence and transdisciplinary knowledge29 to reveal how a social-ecological system connecting eelgrass (Zostera marina, shikaapaashkw), geese (Branta spp., niskandiyiwaapuwaau), and Cree (Eeyou) in subarctic eastern James Bay, Canada (Eeyou Istchee) has been compromised by the effects of local hydroelectric development compounded by climate change. The evidence presented includes diverse forms of knowledge including Eeyou Indigenous Knowledge shared in interviews, long-term eelgrass monitoring data collected over 30 years, and recent research conducted in the region by the authors.

We apply a detection and attribution process30, increasingly emphasized in global change assessments31, to synthesize evidence and infer the causes of the eelgrass social-ecological system collapse in Eeyou Istchee (Fig. 1). This approach, centered on a causal model linking eelgrass health to environmental drivers, pressures, and biological feedbacks (Fig. 2), integrates scientific records, recent fieldwork, and Eeyou knowledge. To reflect the strength of inference and uncertainty, we use terms such as likely, very likely, and may have caused, depending on the weight of evidence. We present this case because large-scale ecological collapses—often linked to past development—are widespread, yet traditional scientific methods alone have struggled to explain or guide responses to them32. This study provides an example showing that attribution can be done even after significant time has passed and with limited quantitative data, especially when supported by partnerships between scientists and local knowledge holders.

Results
Components and collapse of an eelgrass-goose-Eeyou system
In northeast James Bay, a coastal marine social-ecological system was centered around eelgrass and the harvest of geese in the eelgrass habitat prior to and during the 1970s, when waterfowl was a vital source of food for north coast Eeyou, as it had been for time immemorial5,33,34. Tens of thousands of migrating Canada Geese (Branta canadensis) and Atlantic Brant (Branta bernicla horta) visited the eelgrass meadows each fall35. At the time, eastern James Bay supported the largest expanse of eelgrass Zostera marina meadows in North America36. Harvest surveys conducted in the 1970’s documented the annual harvest of more than 50,000 Canada Geese and 6000 Brant by Eeyou hunters living in the coastal communities37.

This eelgrass ecosystem collapsed in the late 1990s5,33,38,39. The collapse was rapidly observed and reported by land users from coastal traplines (i.e., land areas stewarded by a family, where they hold hunting and trapping rights) and by Cree First Nations of Eeyou Istchee. Coinciding with the eelgrass collapse, Eeyou observed a major reduction in the migratory visits of geese during fall, and a corresponding decline in hunting success33. The Eeyou formally reported the changes to Canadian Parliament in 2008, and the change was acknowledged by Fisheries and Oceans Canada32, but no scientific study of the change was initiated by government, academic or industry researchers for a 20-year period.

Coastal Eeyou in Chisasibi (formerly Fort George) associated the loss of eelgrass with hydroelectric development of the La Grande River (LGR)5,39,40. Environmental monitoring reports prepared for Hydro-Québec (the Crown corporation that owns and operates the hydroelectric complex) stated that the decline was most likely linked to natural causes such as wasting disease, climate change, and isostatic rebound33,38. Nevertheless, Eeyou continued to push for an investigation5,39. In 2017, a formal collaboration began between the Eeyou and a team of university-based researchers with a mandate to i) consider Indigenous and scientific knowledge as distinct but equal sources of information29 and ii) seek to identify what caused the eelgrass decline, including the role (if any) of putative drivers, including La Grande Complex hydroelectric power development (Fig. 1, inset).

Presently, with eelgrass meadows still sparse and discontinuous along the coast15, and coastal waters frequently murky15, the fall goose distribution is not predictable41,42. The Eeyou note a social-ecological regime shift marked by increasingly disordered and less productive hunts, leading to the erosion of traditional knowledge43.

Detection of eelgrass change
During the past 40 years, eelgrass underwent a massive decline along the east James Bay coast and failed to fully recover. Eeyou remember eelgrass as consistently widespread and abundant along the north coast of James Bay before the late 1990s5,39,40,44 (Fig. S1). During the 1980s, the Chisasibi First Nation coastal community noted localized eelgrass declines in some traplines near the LGR, but no changes were observed in other coastal communities located away from the influence of the LGR plume. Scientific observations in the 1970s44 and 199136 found eelgrass to be present between depths of 0.5 and 4.0 m, with shoots up to 2.5 m long, biomass in places >1000 g dw m−2, and an estimated areal coverage of ~250 km2. Eelgrass monitoring at six sites near LGR after 1981 noted localized eelgrass losses but no site-wide changes until 1999, when biomass measured at six monitoring sites decreased by about 90% (Fig. 3). Chisasibi Eeyou noted that eelgrass had ceased to be seen frozen in the ice or as beach wrack and deep eelgrass beds had disappeared completely. A survey of eelgrass cover across 87 sites distributed all along the coast, including areas not influenced by the LGR plume33,38, indicated an 88% decrease in the ‘dense’ eelgrass cover class (>50%) between 1996 and 1999 (Fig. 3, inset)15. During 2017–2021, shoot density and cover were still substantially lower than in the 1970s–early 1990s, with no shoots longer than 1.0 m and cover generally sparse or discontinuous (Fig. S2)15,45. Beds were generally patchy and limited to shallow areas (<2 m) (Fig. S3).

Detection of environmental changes
Development of the “La Grande Complex” over three phases increased winter river flows ten-fold causing an enlarged freshwater plume and first increasing then decreasing sediment fluxes to the coastal habitat43,46,47. The complex consists of 11 power generating stations, 74 generating units, and nine reservoirs. During Phase I (1973–1985), four rivers, including the Eastmain River, were partially diverted into the La Grande River (LGR) watershed, increasing its flow. Peak LGR discharge shifted from spring to winter, with February flow rising from 520 m³ s−1 in 1975 to 1750 m³ s−1 in 1980, and 3000 m³ s-1 in 198446. Annual discharge from the Eastmain River after diversion dropped to about 10% of historical values. In Phase II (1987–1996), additional reservoirs and generation stations were added to the La Grande Complex, including La Grande-1 (LG1), <40 km from the bay, with a design flow of 5950 m3 s−143. In Phase III (2002–2013), partial diversion of the Rupert River further increased the average annual LGR discharge to 3782 m3 s−1, about double its pre-development discharge and nearly half the total discharge to James Bay48 (Fig. 4; Tables S1 and S2). In recent years, high winter discharges were sustained at ~4800 m3 s−1 continuously throughout the January–March period47.

Eeyou from coastal traplines near Chisasibi witnessed several environmental changes associated with LGR development including coastal freshening, riverbank erosion, and sediment release into the bay, the latter linked to murkier water and seabed hardening in the eelgrass habitat45. According to oceanographic studies, the ten-fold increase in winter LGR discharge also increased by ten-fold the size of the under-ice freshwater plume along the coast, as indicated by a salinity of 5 in Fig. 1. This increase in the freshwater plume from ~120 km2 to ~1200 km2 extended it into eelgrass habitat 30–40 km north and south of the river mouth46,47. The area of noticeable freshening of surface waters from winter LGR discharge, referred to as the LGR sector, stretched north to Hudson Bay (near Cape Jones)46,47. The winter LGR export of nitrate, the limiting nutrient in the bay’s oligotrophic marine waters, increased more than 10-fold, at the expense of nitrate delivery during spring and summer48,49. Reservoir flooding led to increased downstream fluxes of dissolved and particulate organic matter48,50,51 and, together with riverbank erosion, caused a four-fold increase in annual sediment exports from LGR during 1979–1991, including annual releases of ~1,000,000 t y−1 fine silt and clay50.

Discharge from the Eastmain River after diversion dropped to about 10%, which weakened its influence along the coast. The diversion limited the Eastmain watershed to the coastal plain near the bay dominated by marine clays, silts, and peat bogs. Suspended particulate matter (SPM), colored dissolved organic matter (CDOM), and nutrients increased in Eastmain River water but because of reduced flow, the overall influence of the river decreased43. The Eastmain estuary experienced higher surface salinity, weaker stratification, and altered circulation after the diversion51.

The marine climate in northeast James Bay changed abruptly in the late 1990s. Coastal Eeyou have remarked on the way climate change is transforming coastal ecosystems and mention, in particular, loss of sea ice45. Climate scientists detect a transition in the mid-1990s after 1996 from a relatively stable regime of seasonal ice and surface-water temperature extremes in the broader Hudson Bay region to much greater fluctuations from year to year52. In northeast James Bay, due in part to a strong El Niño, the winter of 1997/1998 was exceptionally warm with low snow cover. Warm air temperatures continued into spring and the regional sea ice broke up in mid-May of 1998 about one month earlier than the mean breakup date during 1982–1997 (Fig. 4B). With ice clearing from northeast James Bay in late May, a spring storm (Figure S4) produced a sediment-rich LGR freshwater plume that was transported northward (Figure S5). Rapid warming of ice-free surface waters led to unseasonably high sea surface temperatures (SSTs) throughout June-October 1998 (Fig. 4C). In total, five high-SST events lasting a total of 79 days occurred during that period that meet the definition of a marine heat wave (MHW; SST exceeding 90th percentile of the baseline for five consecutive days or more (Fig. 4D))53. Prior to the five 1998 MHWs, there were only two MHWs in Eeyou Istchee coastal waters for the entire 1982–1997 period.

Although an exceptional year individually, 1998 is even more notable as a change-point year, meaning that the northeast James Bay system has not returned to pre-1998 conditions in the subsequent 25+ years. Using a Pettitt change-point test, 1998 is a clear change point for sea ice breakup, MHW frequency, and May-July 10-m wind speeds. For June-October SSTs, 1996 is the stronger change-point year; like the other three parameters, there is no significant trend before or after the change point. Thus, since the late 1990s, James Bay has experienced windier springs, earlier sea ice breakup, and hotter, longer, and more frequent MHWs53. Furthermore, what used to be extreme is now the norm: for example, in the warmest year prior to 1996 (1984), the median June–October SST in northeast James Bay was only 4.2°C, whereas an average year now (post-1996) has a median June-October SST of 5.4°C (Fig. 4C). Notably, climate change is not the primary driver for change in river discharge in northeast James Bay. LGR development resulted in a change-point year of 1985 for discharge. Significantly higher discharge since 1998 (130 km3 y−1) compared to 1951–1985 and 1986–1997 (Fig. 4A) may be a function of regulation combined with (inter)decadal variability within the climate system.

Water clarity decreased along the Eeyou Istchee coast both at local and regional scales during recent decades. Eeyou report that coastal marine water changed from transparent blue to murky brown in Chisasibi between 1986 and the early 1990s and a decade later in Wemindji45. Eeyou from both these communities historically could see the bottom (seabed) at depths of 6 m or more, while the southernmost coast around Eastmain and Waskaganish was traditionally marked by colored and turbid water. During 2017–2021, Secchi disc depths along the coast were typically 2 m or less (Fig. S6) and photosynthetically active radiation (PAR) at the seabed (2–4 m) was very low due to light attenuation by a combination of turbidity and CDOM. Four factors are suspected of contributing at various scales to the decreased water clarity in Eeyou Istchee (Fig. 5):

Browning of James Bay waters likely has occurred, based on satellite images that show an increase in absorption by CDOM (a g(440 nm)), between 1998 and 2021 throughout eastern James Bay surface waters, particularly during the month of June after 2010 (Fig. S7). Thus, the increase in CDOM on a coast-wide scale likely explains in part the increased murkiness witnessed by Eeyou in all Eeyou coastal communities over the past 20 years45. The observed coastal browning is likely related to a general increase in river discharge into the bay since the late-1980s54 and rising concentrations of dissolved organic carbon (DOC) and CDOM in river water, coherent with regional trends of increasing DOC and CDOM over the past three decades that have been reported for inland waters across northern Canadian landscapes55. Earlier sea ice melt and retreat may also play a role.

Excess sediment and organic matter released from LGR during the four phases of development likely dispersed with the river plume and deposited at and beyond the plume fringes, where current velocities decrease and salinity increases, while another part may have been trapped in eelgrass beds. Both Eeyou and monitoring teams got the impression of increased turbidity along the coastline in 1985, compared to previous years when the water was clearly transparent, even in windy weather. Sediment core data obtained in the LGR sector show high inventories of a watershed soil erosion tracer, 137Cs56, and buried organic matter that could represent a source of nutrients for algal mats (e.g., Cladophora sericea and a host of epiphytic microalgae) that seem to have become more abundant in the shallow bays. Presently, the LGR as it emerges from the last reservoir LG1 is characterized by lower concentrations of nutrients, DOC, and SPM, and lower fluxes of these constituents during the growing season compared to before development; this is due mostly to the retention of particulates within the upstream reservoirs and the shifting of discharge into winter48,49. However, there is an additional, unquantified but potentially significant SPM flux due to bank erosion in the lowest reach of the river43,57 that could result in events of high riverine delivery of suspended materials, likely at times of peak river discharge during winter. Nutrient release from sediments due to degradation of previously buried organic matter has not been quantified.

Sediment destabilized after loss of eelgrass meadows, exacerbated by more extreme weather and longer open-water season, likely is being recycled in the nearshore area, contributing to a coastal turbid fringe. Eeyou use the word “aayoshtinuukticj” to describe how large eelgrass meadows with long shoots that reached the surface at low tide historically calmed the waters in the bays5. With today’s shorter shoots and lower shoot density (Fig. 3) comes a decrease in the calming effect. Sediment core geochemical profiles show that previously stored sediment was destabilized and eroded after loss of the eelgrass meadows, releasing carbon, nitrogen, and other elements; furthermore, surviving eelgrass beds are not trapping much sediment on an ongoing basis, leading to increased water turbidity23,58. Sediment nutrients that go unused by eelgrass may stimulate increased presence of algal mats, as seen in Danish coastal waters59. Wave-driven sediment resuspension may be exacerbated by increased spring wind velocities and the lengthening of the ice-free season. High-resolution satellite imagery shows that turbid waters with SPM concentrations up to 30 mg L−1 can be pervasive in the nearshore waters along the coastline (Fig. S8).

Attribution of changes in eelgrass to changes in drivers
We use the causal model (Fig. 2) to synthesize evidence for strong relationships between changes in eelgrass health and environmental conditions. We structure the analysis around four time periods related to the eelgrass crash, recognizing the evolution of the role of the Eelgrass-sediment-light (ESL) feedback as eelgrass declined. We do not attribute any large-scale changes in eelgrass to the Eastmain diversion because of the small spatial scale of the known environmental effects (Fig. 5).

Low salinity (<5), which adversely affects the ability of eelgrass to maintain a positive carbon balance (i.e., net primary production)60,61, likely started affecting eelgrass growth in the LGR sector when the winter plume enlarged in the 1980s. Negative effects on carbon balance may particularly jeopardize eelgrasses in high-latitude environments, which require substantial carbohydrate reserves to survive long light-limited winters62,63. The tolerance of eelgrass to low salinity varies across populations but salinity ≤5 consistently reduces eelgrass productivity and survival60,61. Thus, it is very likely that expansion of the LGR winter plume from ~120 km2 to ~1200 km2 reduced eelgrass winter survival and early spring growth in the affected area.

Reduced water clarity during the growing season likely started affecting eelgrass growth in the LGR sector when reservoir flooding and bank collapse increased sediment and organic matter releases in the 1980s. High sediment and organic matter loads can directly reduce water clarity or indirectly (via the ESL feedback) reduce water clarity by smothering eelgrass shoots or causing problems associated with decaying organic matter that impact eelgrass growth. Eelgrass needs clear waters for growth because it has a higher light requirement than both macroalgae and phytoplankton, with an average minimum light requirement of ~20–30% of surface irradiance60. We suspect that light started to decrease in parts of the LGR sector when hydroelectrical development started, due to a combination of excess sediment and organic matter releases from LGR and reduced flocculation from the additional freshwater. Local eelgrass losses would have released previously stored sediments and nitrogen64, likely exacerbating the poor water clarity and starting to shift the eelgrass ecosystem toward a regime shift (Fig. 6E).

Eelgrass growth all along the coast was likely affected by the climate shift and extreme events starting in 1998. The early ice breakup, unseasonably high SSTs and prolonged MHWs in the early part of the 1998 growing season (May, June, and July) may have caused eelgrass to experience extreme negative carbon balance leading to poor growth and/or high mortality. Experimental studies have shown that unusually warm winter-to-spring conditions when light is still limited can have severe effects on eelgrass by accelerating the consumption of energy reserves, which are low following winter, and by triggering early spring flowering65.

Eelgrass recovery likely has been limited by suboptimal water column light levels, partly due to browning and partly from turbidity, combined with a new, more variable, climate regime. An experiment that determined ex situ production-irradiance curves for eelgrass from two Eeyou meadows and collected in situ light data during summer 2021 (continuous measurements of PAR) found suboptimal light conditions for eelgrass growth66. The growing season in James Bay is short, and eelgrass plants need to build up substantial carbon stores during that period to survive the long under-ice period. Because suboptimal water column light levels threaten the ability of eelgrass to build up these stores, we suspect that light limitation has limited eelgrass recovery in the region.

Methods
Statistics and reproducibility
This study was co-designed with Indigenous Cree (Eeyou) First Nation partners through processes developed under research agreements with Niskamoon and the project steering committee29. Eeyou land users conducted fieldwork along the coast between January 2016 and August 2021 and participated in several iterations of data analysis, interpretation, and review. Details on the interweaving of Eeyou knowledge and science through informal channels are given in Fink-Mercier et al.29 and the project’s final report82, which is published online at https://doi.org/10.34992/4K4Z-TF96. Through formal interviews, Eeyou participated in recording their knowledge between July 2019 and June 2022 including 27 coastal traplines and 66 semi-structured and participatory mapping interviews. The study engaged 95 Eeyou land users, including tallymen and elders. Thus, Indigenous knowledge was central to this study, influencing planning, data collection, analysis, synthesis, result presentations, and final reports, alongside Western science.

Statistical analyses of scientific data were conducted in accordance with standards in each field. For eelgrass shoot density, sample size reflected availability of past monitoring data (1982 to 2009). Using generalized additive mixed models (GAMMs; R-package gamm4), we tested for temporal trends in eelgrass shoot density assuming a negative binomial error distribution. No data were excluded from the analyses15. The Investigators were not blinded to allocation during experiments and outcome assessment. For analysis of environmental times series, a Pettitt test (a non-parametric test for change points) and two-tailed Mann–Whitney test (assessing difference in medians) around the best change point year of 1998 were applied. The null hypothesis was no step change (p<0.05 comparing before/after 1998 for all variables). Experiments were used to test the nutrient and light limitation hypotheses. In the former, we experimentally manipulated plot-level water column nutrient concentration in situ at two sites and compared eelgrass growth in manipulated and control quadrats66. At each site, we set up 3 parallel transects at least 5 m from the edge of the meadow using SCUBA and randomly assigned experimental treatments to 25×25 cm quadrats every 5 m along each transect. To assess the ability of eelgrass to grow under low light conditions, we used 8 whole, randomly selected shoots collected from within the experimental array at each site to construct production–irradiance (PI) curves66.

Ethics and inclusion statement
The knowledge of the Eeyou is well suited to detecting change as their harvesting activities rely on observations of their environment at multiple scales40,42,45. The Indigenous knowledge component of this study was community-driven, with input from Eeyou land users, eelgrass ecologists, waterfowl experts, and the project’s steering committee29. Eeyou engagement in every step of the research was specified in the formal research agreements between the Eeyou organizations and the universities, and these terms were adhered to by the university researchers. These agreements specified protocols for returning all data to the communities and respecting privacy of material in interviews, consistent with established FAIR and CARE principles. The Behavioral Research Ethics Board of the University of British Columbia approved the components of this research that relied on formal interviews with Eeyou people (H20-02942)45. This work fully complies with the Tri-Council Policy Statement: Ethical Conduct for Research Involving Humans (TCPS 2 2018). The ethical obligations surrounding informed consent in research involving Indigenous Peoples align with Article 9.1 of the TCPS. Additionally, this study adhered to the principles outlined in individual Research and Information Sharing Agreements executed between the principal investigator and the respective First Nations Governments.

Eelgrass abundance, nutrient content and depth delineation
To compile information on eelgrass biomass and density in Eeyou Istchee, Hydro-Québec monitoring reports were reviewed and all raw observations were compiled15. Eelgrass biomass monitoring was a main method of monitoring. Six eelgrass beds within the LGR sector were monitored for shoot density and biomass by Hydro-Québec between 1982 and 2009 to assess the impacts of La Grande development. Eelgrass biomass was assessed at a larger number of locations along the coast in 2019. Eelgrass cover monitoring was the second method employed between 1999 and 201915. Cover classes were assigned according to four abundance classes (Fig. S2).

To assess eelgrass beds depth range, we conducted side-scan sonar surveys using an autonomous underwater vehicle (AUV) at seven coastal locations in 2019. The AUV was equipped with a Klein side-scan sonar, a conductivity and temperature sensor, and a 10-beam Doppler velocity logger (DVL) for underwater navigation and AUV to the seafloor distance measurement81. A square grid of 20×20 m was overlaid on the side-scan sonar imagery and each grid cell classified by eye as one of: bare seabed, patchy eelgrass, or continuous eelgrass. Water depths along the survey lines were retrieved and sorted into depth bins for each of the classified areas to produce histograms of the water depth distribution of the eelgrass.

To assess energy reserves and nutrient limitation, we measured eelgrass C content in the roots and N in leaves in 2019, respectively. To assess contribution of water column and sediment nutrient sources, we also analyzed the N isotopic ratio (δ15N) in eelgrass shoots83.

To test if light and nutrient levels in the water limit eelgrass growth, we conducted experiments on eelgrass from two beds south of Chisasibi. For nutrient limitation, we manipulated water column nutrient concentrations and compared eelgrass growth in high-nutrient (manipulated) and ambient-nutrient (controlled) conditions at each site66. SCUBA divers measured eelgrass growth rates using a standard protocol. For light limitation, we collected shoots from each eelgrass bed, brought them to a field laboratory, and manipulated light levels. Evidence of light limitation was obtained by comparing eelgrass light requirements with light records from sampling sites.

Remote sensing of ice breakup and sea surface temperature
To compare with eelgrass metrics, time series of environmental variables were compiled and examined15. Mean daily sea surface temperatures of June (°C) for James Bay were obtained from the Group for High Resolution Sea Surface Temperature (GHRSST) product ‘AVHRR_OI-NCEI-L4-GLOB-v2.1’, which provides continuous daily record of SST on a 0.25° spatial grid from 1982 to 2019. The regional annual ice breakup dates were determined from regional ice charts produced by the Canadian Ice Service. Regional sea-level pressure and wind fields at hourly temporal resolution and 0.25° spatial resolution were acquired from the fifth-generation reanalysis (ERA5) of the European Center of Medium-Range Weather Forecasts84,85. Annual freshwater discharge was estimated for the large watershed sectors of the JB from 1951 to 202186. Marine heat wave (MHW) frequency, duration, and intensity for 1982 to 2021 for eastern James Bay were described using the SST dataset from the Operational Sea Surface Temperature and Sea Ice Analysis (OSTIA) system53. This system generates high-resolution (1/20° grid), daily, global, gap-filled SST fields derived from satellite and in situ data. MHW events were defined by five days of sustained warming above the 90th percentile for a 40-year baseline period (1982-2021) for at least five consecutive days87.

Ocean color remote sensing
Concentrations of optically active biogeochemical compounds, i.e., colored dissolved organic matter (CDOM) and suspended particulate matter (SPM) in the bay were assessed through satellite remote sensing. Regionally tuned empirical algorithms were used to compute CDOM absorbance (a g(400 nm)) and SPM concentrations based on in situ reflectance, CDOM, and SPM data collected in 2018 and 2019 within the scope of the CHCRP88. For the analysis of long-term changes to CDOM, data from the Moderate-resolution Imaging Spectroradiometer onboard the Aqua satellite (MODIS-Aqua) were atmospherically corrected using a modified version of SeaDAS v889. For the estimation of SPM concentrations, data from the Multi Spectral Imager (MSI) onboard Sentinel-2 (atmospherically corrected using ACOLITE90) was used. Log-transformed values for satellite derived SPM concentrations were mapped to evaluate the spatial variability along the coast as observed by Sentinel-2A MSI on August 8, 2016.

In situ water parameters
To compare the extent of the La Grande River plume to pre-development extent, we carried out a detailed study of the plume when the LGR discharge averaged 4800 m3 s−1 in the winters of 2016 and 201747. Salinity was measured using a conductivity-temperature-depth probe (CTD) and recorded continuously from January to April using ice-deployed moorings. Additionally, discrete CTD profiles were taken all along the coast in all four seasons from 2017 to 2021, and water samples were collected and analyzed for salinity49,91.

To assess the seasonal availability of nutrients in coastal surface waters, nitrate and phosphate were measured in water samples from the LGR sector during early winter, late winter, and summer (2016 and 2017)49, and from sites distributed all along the eastern coast of James Bay during winter (2018, 2019 and 2020), spring (2018 and 2019), summer (2018, 2019 and 2021), and fall (2017 and 2018)91. Sampling stations were located within 25 km of the shore.

Sediment cores
To assess whether erosion had occurred, sediment cores up to 58 cm in length were collected across six Chisasibi traplines between 2017 and 2021 using a gravity corer and push corer as described previously56. The sediment cores were sectioned immediately and subsections analyzed to obtain profiles of the natural radioisotope 210Pb and the artificial radionuclide 137Cs, which is expected to be present in coastal sediments continuously deposited since ca. 195456.

Reporting summary
Further information on research design is available in the Nature Portfolio Reporting Summary linked to this article.

Peer review rounds
[{"round": 1, "reviewer_comments": {"reviewer_1": "This paper presents an admirable and clearly written synthesis of a quest to understand the large-scale loss of eelgrass, the foundation of a coastal ecosystem in James Bay, Canada, and its impact on that ecosystem and the people of the indigenous nation that historically relied heavily on this system. The paper seems to me a strong example of the approach and value of combining multiple kinds of knowledge, both among disciplines of traditional western science and in bridging them to the knowledge of people that have lived with the ecosystem for a long time. It shows pretty convincingly that the widespread collapse of the eelgrass ecosystem in James Bay was ultimately forced by major river flow rerouting and change in hydrological conditions as a result of hydropower development, coupled with a strong shift in the climate regime.\nI appreciate the detection-attribution framework and the approach using weight of evidence - it is frustratingly common in the scientific literature to see papers reporting a \"significant difference\" without even mentioning the direction of change, much less how much variance is explained! I like the \"assertion-evidence\" format, breaking the text into statements followed by the evidence supporting each.\nSo the paper aims to provide an example of both integration of different knowledge sources and the application of a detection-and-attribution framework. We need such examples.\nI have a few questions and comments:\nPage 9: Climate-driven browning of James Bay Waters. Test states that satellite images show an increase in absorption by CDOM between 1998 and 2010 throughout the region. I am definitely not seeing this in figure S7. At several sites an increase *after* 2010 seems clear, but I can't imagine any statistical test of these data finding a net change between 1998 and 2010.\nPage 9: Excess LGR fine sediment releases. The radiotracer data seem convincing, but I'm confused by the statement that the LGR has relatively low suspended particular matter now. Does this mean it is or is not a threat to eelgrass?\nP 13. Discussion Par 1 states that throughout nearly 2 decades of development, most eelgrass meadows resisted or recovered from salinity and low light stress because of their initial healthy condition, resilience due to stabilizing ESL feedback loop, and stable, regional marine climate. This is an entirely plausible conclusion to draw, but given the emphasis on detection and attribution in the Intro, this assertive language seems a bit loose. Yes, eelgrass meadows appear to have been relatively stable during that initial time period. But what is the evidence that it was because of their initial healthy condition, stabilizing ESL feedback, and a stable marine climate? These did not jump out to me from the foregoing account so a reader could use a reminder here, as well as qualification with confidence statements such as used earlier. Similarly, the next sentence on multiple stressors pushing the system past its tipping point cites two general papers on tipping points whereas, to me at least, the wording seems to imply that they are supporting the conclusion of this particular system's flip past its tipping point. To be clear, I find the authors' argument pretty convincing, I just find the logic of this paragraph a bit loose.\nFinally, I am not intimately familiar with the quite impressive body of work that this group has done, but there are a number of published papers on seemingly similar themes. So it's not entirely clear to me how novel this one is.\nFig 2: what are the red vs black arrows?\nFig 5: Label for red rectangle in legend is missing\nFig S3: Counts of what? what is a trapline? Not defined in text.\nFig S6: Color symbols in legend are too small to read.", "reviewer_2": "General Comments\nInitially I was highly intrigued by the premise of eelgrass decline in association with these massive hydroelectric developments in the Hudson Bay region. I remain convinced that the declines occurred and that they were influenced by these developments so I think it is a very worthwhile story. However, I can only describe the case made in the present manuscript as woefully inadequate. Naturally, climate change must be invoked, clearly non significant patterns and weather events become a ‘step change’ in the climate. Many misinterpretations of climate science that one might expect in the nightly news occur here. I would also add that this is a very northerly location, eelgrass grows down to florida and so has a very reasonable tolerance for warmth so it is difficult to find a credible linkage with temperature. Discussion of primary productivity in February! At this time the plant is dormant, mostly underground, convinced me that there are no seagrass scientists on this work. While I would strongly suspect that light is a factor, because it almost always is, the data presented is just inadequate to establish this. I find the indigenous observations to be the most credible part of what is presented and give them higher weight than much of the data presented. The bits and pieces of data, very often inadequately presented, do not help in assigning causality. There are a lot of fancy words about a ‘detection and attribution process’ etc.. But you still can’t make a silk purse out of a sows ear. The premise of the authors that traditional approaches as stated (not maligning indigenous science, which I consider to be no different than any other empirical science such as ecology that was founded on observation and deductive reasoning) when accompanied by good data, have been outstanding at assigning causality and providing solutions to mitigation even when events occurred decades in the past. The lack of action to mitigate is a societal decision, not a function of our ability to characterize change and its cause.\nSpecific comments\nIntroduction general. Nowhere in the introduction or the subsequent result is there any chronology of the hydroelectric development and the reader is left trying to interpret that from what is presented.\nL43, the sentence is true for all peoples, not sure why it would focus on indigenous people. Replace indigenous peoples with ‘humans’.\nL62 This statement is untrue, seagrasses were devastated by wasting disease in the last century on a spectacular scale and recovered entirely on a scale that probably rivals any know plant species recovery. There are many examples of recovery on a smaller scale documented more recently. The plant shows an enormous and rapid propensity for recovery once the stressor is removed. This argument is very one-sided and the authors need some further research.\nL63 I fail to see what is transdisciplinary about the present study, remove this.\nL93 I fail to see how indigenous and scientific knowledge are in any way distinct. Epistemology would define knowledge as being the intersection of truth and belief, and this is shared among all humans as is deductive reasoning (despite Descartes erroneous belief that it was divine).\nL96 This statement is incorrect, and I note not substantiated by any human knowledge or reference. For the time period in question, global CO2 levels have been on a fairly linear upward trajectory. Regionalization typically refers to the regionalization of global climate models, and as such are unlikely to predict ‘intensification’. This appears to be both an exaggerated and unsubstantiated statement.\nL98 The last paragraph comes out as being more of an advertisement than a brief summary of the study that would typically occur in an introduction. It seems to be a bit more methodological than I would expect, suggest shortening considerably and incorporating into the previous paragraph.\nFigure 2. It is unclear where the eelgrass limits for salinity and temperature came from. From both extensively looking at literature, and empirical observations, eelgrass can be highly abundant when temperatures are above 25 degrees C. It may in fact be necessary to stimulate flowering shifting from clonal to sexual reproduction, I am unsure where this came from. Secondly >5 psu (ppt is generally unused now as it refers to direct ion measurements not usually conducted)75% of the time seems to be a really odd way to represent this. I have found the experimental literature value of 10 PSU corresponds really well to the distribution in estuaries using the mean salinity.\nFigure 3. The figure needs to clarify that in years with no or zero data, data was not in fact collected. The reader cannot distinguish between a zero value and the absence of data at present.\nL162 This is a very poor description of the hydrology. What is a ‘natural discharge’. Is that the mean annual discharge? And why is this number, whatever it is, being compared to a single month of February in the text? Why focus on February when the plant is pretty much absent. Eelgrass can disappear totally from areas in winter and reemerge in May. So why focus this on February? The mean annual discharge is shown in the figure, which establishes that this increased in LGR due to rerouting another river. However, this graph does nothing to show changes in the annual pattern of flow, which may very well be critical here and is essential for interpretation.\nL167 There would seem to be little need to italicize annual here.\nThere are a variety of descriptions here, flow regime, overall discharge, salinity that are mixed together in such a form as to be entirely uninterpretable. Flow timing and quantity should be shown in a before and after hydrograph with daily average discharges as obviously things are happening in months other than February. If sediment changed, annual loads for a number of years before and after should be tabulated.\nLine 181 I find the title of this section to be entirely unsubstantiated. No doubt there was an El Nino. This is weather, not climate. Sea surface temperature deviation seems increasingly variable but there is certainly no upward or downward trend. Excluding the strong El Nino year a trend is questionable. MHW is pretty arbitrary statistical definition and it is unclear that this in any way causes exceedances of the physiological range of temperature relevant to the plant. Overall though, while global change is occurring gradually, there is little evidence here of a ‘step change’ in ‘climate’, and the period examined is at the minimum for examining climate. There is a 3000 year reconstruction of climate in the area Vallerand 2024 that suggest temperature of 2 degrees higher than now on average, so the argument of this influencing zostera (which does very well in much warmer areas) is exceedingly weak.\nLine 203, eelgrass declines are almost always due to light, so I have no doubt that the altered hydrology and salinity in conjunction with increased sediment has something to do with this. However, there seems to a paucity of information here. The authors are clearly aware of the irradiance required for eelgrass, yet compare the light attenuation to a single number in the Wadden sea despite a huge amount of literature on the subject. There is also no connection between the stated single value for light attenuation and the growth potential. FYI a value of 1.2 allows eelgrass to grow deeper than two meters and 1.79 does allow eelgrass to grow at depths of 1 to 2 meters, so does not entirely explain the absence.\nFigure 5. There is some dramatic overreach here. I would bet no significant change in the sea surface data as presented, yet it somehow became a conclusion unsubstantiated by these data.\n267 eelgrass does not grown in winter, period. It may not even be present as it wracks very substantially in the fall and can entirely disappear from area, to reemerge in the spring. This is especially true if reproduction from seed and not clonal reproduction is occurring. This statement reflects a complete disconnect of understanding of the plant physiology. As there are no leaves 99.9% of carbon fixation occurs between May and October.", "reviewer_3": ">>Seagrasses are foundation species in many coastal ecosystems. They provide critical habitat for marine and semi-aquatic wildlife, such as waterfowl, and the reliable, nearshore wildlife harvesting opportunities in seagrass ecosystems have been particularly important for many coastal Indigenous Peoples’ food security and cultural continuity\nThis is an excellent way to start, setting up the importance and why - this often gets lost in western mainstream systems, and to explain it clearly and succinctly is excellent.\n>>Protecting and restoring degraded seagrass ecosystems may thus contribute to numerous benefits of interest to both governments and coastal communities10-12.\nWould like to see this expanded a little and clarify something like 'both cultural, non-Indigenous and ecosystems'\n>>However, the catastrophe went unrecognized by the global research community for nearly two decades.\nHere would be a good place to follow up with an explanation sentence why it went unrecognized - did western scientists ignore Cree? Were calls for help disregarded, not funded? Did the Cree have policies that did not allow research?\nIK is often tracked carefully, but it's a good reminder to western science that this *does* occur and explain why the system got to the point/led up to the point it is at, especially when you follow up with this sentence in the next paragraph \"We present this example because we believe such massive ecological collapses caused in part by past development, are all too common, yet traditional scientific approaches have limited our ability to understand these changes and determine actions to mitigate them36.\" it helps make it more clear to those who don't work or understand IK.\n>>Cree from Chisasibi noted localized eelgrass declines in some areas near the La Grande River (LGR) but no changes were observed in other coastal communities.\nDoes this mean all coastal communities, or only First Nations, or only non-First Nations -?\nSections 2-3 are void of IK - this would be a great place to weave in the IK information that has been documented that would corroborate the information\n>>Based on review of Cree knowledge\nHow? Was this through archived materials, or were First Nations members asked?\n>>Based on review of Cree knowledge and scientific evidence in a detection and attribution framework, we infer that, in Eeyou Istchee,\nThe beginning of this sentence makes it seem as if the 2 ways of knowledge are not equal. A better way to begin this might be \"Based on Cree Indigenous Knowledge systems and scientific evidence\" or \"Based on Cree Indigens Science and western scientific evidence\", this way it illustrates to readers that both systems have validity and assist to prove the decline of eel gras and the ecosystem\n>>Regardless, this large “genomic offset” implies that the northeast James Bay eelgrass population is more vulnerable to climate change than better-studied populations in temperate regions.\nNice finding, and well stated!\n>>along the Swedish west coast after the loss of eelgrass beds, where increased sediment resuspension and proliferation of drifting algal mats prevent both natural recovery and human restoration of eelgrass77.\nIs there Swedish IK information that corresponds to their findings in western science? Just curious\n>>In Québec, as elsewhere, hydropower development is being considered on a scale not seen since the 1970s, alongside other types of developments (mining, ports, etc.). It is vital that future impact assessments proceed differently, considering coastal ecosystems, employing multiple knowledge systems, and trying to anticipate how climate change may compound other impacts.\nexcellent wrap up here\nOverall:\nThe use of the Indigenous term \"Shikaapaashkw\" in the title itself is great, but not explained and a little confusing for readers who may not understand why it was used or what it is, especially if they are looking for information on climate change or IK generally and don't have an ecosystem or eelgrass background.\nThis paper is western science heavy, with the IK not interwoven as well as it could be, and could be utilized to make the points stronger, particularly since one of the claims is that Indigenous are having to adapt. The decline of the grass and the environment is clear, but the IK isn't consistent throughout, and makes it appear as if IK and First Nations were used as leverage to land the funding rather than do honest research inclusive of Indigenous Peoples.\n>>>>Indigenous knowledge\nCree knowledge from the Eeyou coast is well suited to detecting change, as Cree rely on observations of their environment at multiple scales during their harvesting activities5. The Indigenous knowledge component of this study was community-driven, with input from Cree land users, eelgrass ecologists, waterfowl experts, and the project's steering committee6,7. Cree land users co-designed and conducted field work along the coast between January 2016 and August 2021. Cree participated in recording their knowledge between July 2019 and June 2022 including 27 coastal traplines and 66 semi-structured and participatory mapping interviews. The study engaged 95 Eeyou land users, including tallymen and elders. Indigenous knowledge and Western science were both central to this study, influencing planning, data collection, analysis, synthesis, result presentations, and final reports8.\nThis section is lacking the information about what protections this team elicited for data sovereignty of Indigenous groups, and acknowledgement of Indigenous Knowledge sovereignty. Were IRBs used? Did they discuss with First Nations or Cree Councils? Was all sensitive data then given to the Cree and not released, or what happened to the data collected? Studies such as this may release findings and all data without Indigenous groups knowing or understanding, and such knowledge is impossible to then get back in control of. Did the Cree know of and consent to this publication?\nVisuals are very clear and easy to follow, well laid out for manuscript"}, "author_response": "We thank the reviewer for the positive comments.\nI have a few questions and comments:\nPage 9: Climate-driven browning of James Bay Waters. Test states that satellite images show an increase in absorption by CDOM (ag(440 nm)) between 1998 and 2021 throughout eastern James Bay surface waters, particularly during the month of June after 2010 (Figure S7).\nPage 9: Excess LGR fine sediment releases. The radiotracer data seem convincing, but I'm confused by the statement that the LGR has relatively low suspended particular matter now. Does this mean it is or is not a threat to eelgrass?\nLGR as it emerges from the last reservoir LG1 is characterized by low suspended particulate matter (SPM) concentrations, due mostly to the retention of particulates within the upstream reservoirs. Thus, on average, the river is delivering water with low SPM concentrations to the Bay, relative to SPM concentrations in other rivers flowing into the bay. Although mean annual discharge of the river has doubled since hydro development and it is the largest river in terms of discharge along the east coast of James Bay, it is not the largest in terms of SPM delivery. Therefore, the LGR delivery of SPM from the watershed to the Bay should have a limited impact on the underwater light conditions for eelgrass relative to the impact attributable to other rivers. However, there is an additional, unquantified but potentially significant SPM flux due to bank erosion at the mouth of the river (Paquet et al. 2019, HQ and Genivar 2005 – refs 57 and 43 in the manuscript, respectively). These erosion events could result in pulsed releases of suspended sediment and organic matter/debris, likely at times of peak river discharge during winter. Subsequent dispersal of these materials, which may be delayed until the more energetic conditions that follow ice breakup, could impact light conditions at eelgrass beds. The extent of these river impacts has yet to be determined.\nThe text in the manuscript was changed to the following: “Presently, the LGR as it emerges from the last reservoir LG1 is characterized by lower concentrations of nutrients, DOC, and SPM, and lower fluxes of these constituents during the growing season compared to before development; this is due mostly to the retention of particulates within the upstream reservoirs and the shifting of discharge into winter48,49. However, there is an additional, unquantified but potentially significant SPM flux due to bank erosion in the lowest reach of the river43,57 that could result in events of high riverine delivery of suspended materials, likely at times of peak river discharge during winter.”\nP 13. Discussion Par 1 states that throughout nearly 2 decades of development, most eelgrass meadows resisted or recovered from salinity and low light stress because of their initial healthy condition, resilience due to stabilizing ESL feedback loop, and stable, regional marine climate. This is an entirely plausible conclusion to draw, but given the emphasis on detection and attribution in the Intro, this assertive language seems a bit loose. Yes, eelgrass meadows appear to have been relatively stable during that initial time period. But what is the evidence that it was because of their initial healthy condition, stabilizing ESL feedback, and a stable marine climate?\nWe thank the reviewer for this comment. Our argument that the resilience of the eelgrass ecosystem during 1978-1995 resulted from initial healthy condition, stabilizing ESL feedback, and a stable marine climate comes from applying the framework for the resilience of seagrass ecosystems (Unsworth et al. 2015 – ref 67 in the manuscript) to the chronology of changes described in the previous sections. We have reworded this section to make that clearer and to include qualifiers that express our degree of confidence in each statement.\nWe also revised this section to address a comment from another Reviewer regarding the paper emphasizing the science more than the Indigenous knowledge aspects. Parts of this paragraph were edited to better show how the ESL feedback loop resonates with the Indigenous knowledge of the coastal Cree land users, who have a specific term to describe the calming effect of the large, dense eelgrass beds that were once widespread along the northeast coast of James Bay.\nRegarding the second comment above, we revised the text to be consistent with the ‘regime shift’ terminology. Local eelgrass losses would have released previously stored sediments, likely exacerbating the poor water clarity and starting to shift the eelgrass ecosystem toward a regime shift.\nFinally, I am not intimately familiar with the quite impressive body of work that this group has done, but there are a number of published papers on seemingly similar themes. So it's not entirely clear to me how novel this one is.\nAs the Reviewer rightly points out, the group has published a number of papers addressing various aspects of this overall issue, ranging from historical eelgrass and climate reconstructions to current oceanographical, biogeochemical and ecological aspects, to sociocultural shifts and explorations of links with Indigenous Knowledge. What we present here is the first attempt to integrate all of these various information and data streams into a single coherent framework that has allowed us to reconstruct and explain the cause of the eelgrass ecosystem collapse in Eeyou Istchee, and to describe some of its associated consequences. We believe that the novelty lies in this unique integration of various types of knowledge and data, which to our knowledge has seldom been carried out, at least not at this spatial and temporal scale.\nThe closest papers to this topic published previously are Idrobo et al. (2024), which uses exclusively Indigenous Knowledge to show that the Fall Goose Hunt in Eeyou Istchee had a “Turning Point” after the eelgrass ecosystem collapse, and Leblanc et al. (2023), which used scientific data to document the timing and spatial extent of the major decline in eelgrass condition between 1995 and 1999 but did not attempt to assign causation.\nCaption was altered to clarify that the red arrows in the causal model show the ESL feedback mechanism, which is illustrated more plainly in the top panel of the figure.\nFig 5: Label for red rectangle in legend is missing\nCorrected\nFig S3: Counts of what? what is a trapline? Not defined in text.\nThe figure shows counts of grid cells (20 m x 20 m) classified according to three categories: bare seabed, patchy eelgrass, or continuous eelgrass. The caption was edited for clarification, removing the term trapline and explaining the ‘counts’, as follows:\nFigure S3. Sites (yellow circles) surveyed by side-scan sonar mounted on an autonomous underwater vehicle (AUV) and processed in A) the La Grande River sector of the coast and B) the Wemindji sector. Panels C-I show counts of the number of grid cells (20 m x 20 m) containing bare seabed (grey bars), patchy eelgrass (orange bars), or continuous eelgrass (blue bars) in each water-depth bin, based on the side-scan sonar imagery. Courtesy: C.J. Peck.\nAn explanation was added to the Methods section, as follows:\nA square grid of 20 m x 20 m was overlaid on the side-scan sonar imagery and each grid cell classified by eye as one of: bare seabed, patchy eelgrass, or continuous eelgrass. Water depths along the survey lines were retrieved and sorted into depth bins for each of the classified areas to produce histograms of the water depth distribution of the eelgrass.\nFig S6: Color symbols in legend are too small to read.\nFigure was resized.\n__________________________________________________________________________________________\nGeneral Comments\nInitially I was highly intrigued by the premise of eelgrass decline in association with these massive hydroelectric developments in the Hudson Bay region. I remain convinced that the declines occurred and that they were influenced by these developments so I think it is a very worthwhile story. However, I can only describe the case made in the present manuscript as inadequate. Naturally, climate change must be invoked, clearly non significant patterns and weather events become a ‘step change’ in the climate. Many misinterpretations of climate science occur here. I would also add that this is a very northerly location, eelgrass grows down to florida and so has a very reasonable tolerance for warmth so it is difficult to find a credible linkage with temperature. Discussion of primary productivity in February: At this time the plant is dormant, mostly underground. While I would strongly suspect that light is a factor, because it almost always is, the data presented is just inadequate to establish this. I find the Indigenous observations to be the most credible part of what is presented and give them higher weight than much of the data presented. The bits and pieces of data, very often inadequately presented, do not help in assigning causality. There are a lot of fancy words about a ‘detection and attribution process’ etc.. The premise of the authors that traditional approaches as stated (not maligning Indigenous science, which I consider to be no different than any other empirical science such as ecology that was founded on observation and deductive reasoning) when accompanied by good data, have been outstanding at assigning causality and providing solutions to mitigation even when events occurred decades in the past. The lack of action to mitigate is a societal decision, not a function of our ability to characterize change and its cause.\nWe have carefully considered the Reviewer’s charge that the case we make in the manuscript is inadequate and made significant improvements to both the results and discussion sections.\nWith respect to the climate change section, we note that our paper about ice breakup and marine heat waves in eastern James Bay that was ‘in review’ at the time of submission of this manuscript is now published in Frontiers (Bruneau et al. 2025 – ref 16 in the manuscript). We have thoroughly re-examined the section of this manuscript referring to the changes in the marine climate and the statistics reported therein, and we stand by our work. We also believe we have addressed the Reviewer’s criticism that the results are inadequately presented by re-doing Figure 4 and adding a short paragraph that includes additional statistics (see below for more information).\nThe Reviewer may have misunderstood our argument related to how the extreme climate events are linked to the eelgrass losses. To be more clear, we now start the Discussion with a plain statement that the evidence shows the ecosystem was in a precarious state after the\n5\n>20 years of hydro development and associated environmental changes; the extreme climate events were one more disturbance that, coming when they did, triggered greater losses near Chisasibi and extension of the losses into other areas. Other workers such as Eriander et al (2016) have noted that “a high concentration of fine sediment, water and organic material make the sediment very sensitive to resuspension, which can increase turbidity for a long time following disturbance”. Further, that “eelgrass growth in deeper habitats is challenged both by low light conditions and a short growing season at high latitudes…. growth was very low under these conditions (the plants merely persisted), and the eelgrass would be sensitive to temporary declines in water quality.”\nRegarding Indigenous observations, we thank the reviewer for suggesting that we give them more weight in the manuscript. We have made changes both in the order of sections and the content of both the results and discussion to address this comment.\nTo the Reviewer’s last point, we understand that disagreement about the causes of the eelgrass decline has contributed to the lack of action to mitigate. The integrated knowledge base presented in this paper aims to be salient, legitimate, and credible to the diverse set of regional decision makers, and thus better support coastal management and mitigation decisions.\nBelow we address the Reviewer’s other comments point by point.\nReference\nEriander L, Infantes E, Olofsson M, Olsen JL, Moksnes P-O. Assessing methods for restoration of eelgrass (Zostera marina L.) in a cold temperate region. J. Exp. Mar. Biol. Ecol. 479, 76-88 (2016)\nSpecific comments\nIntroduction general. Nowhere in the introduction or the subsequent result is there any chronology of the hydroelectric development and the reader is left trying to interpret that from what is presented.\nWe edited Section 2 of the Results to clearly give the chronology of hydro development.\nL62 This statement is untrue, seagrasses were devastated by wasting disease in the last century on a spectacular scale and recovered entirely on a scale that probably rivals any know plant species recovery. There are many examples of recovery on a smaller scale documented more\n6\nrecently. The plant shows an enormous and rapid propensity for recovery once the stressor is removed. This argument is very one-sided.\nWe disagree with the Reviewer here; although perhaps the issue is one of scale. According to references cited in the text and other references we reviewed, the trajectory of seagrass recovery after a decline depends on the intensity of stressors over space and time, the seagrass species, and the location (length of growing season). Full recovery after large-scale declines of perennial seagrass species like eelgrass often takes decades (O’Brien et al. 2018 – ref 72 in the manuscript) — and in some cases, recovery may never occur, even after stressors are removed (Moksnes et al. 2018 – ref 77 in the manuscript). Vaudrey et al. (2010) give some other examples of partial seagrass recoveries after losses. For example, they note that Mumford Cove exhibited a 3–5 year time lag between nutrient load reduction and the initiation of seagrass recolonization and a 12–15 year time lag to a relatively stable distribution. In other cases of recovery, the time to initial establishment for sites with no pre-existing seagrass beds ranged from 3 to 8 y (St. Martin River, Boston Harbor) and expansion of seagrass into stable beds ranged from 7 to 16 y. Maximum cover was achieved in 14 to 22 y (Chincoteague, Sarasota, and Tampa bays). Another important point is that what eelgrass ecosystem “recovery” means to Indigenous rights holders and harvesters vs. outside researchers or agencies is quite different. In the case of James Bay, the Eeyou consider ecosystem recovery to include the deep eelgrass and the massive shallow meadows that historically attracted large numbers of geese.\nIn direct response to the reviewer’s point about wasting disease, the only study with clear data on pre-wasting disease eelgrass extent demonstrates that full recovery never occurred (Krause-Jensen et al. 2021 – ref 16 in the manuscript).\nMany documented recoveries note that deep-water longer eelgrass does not recover, even many decades after the decline (Krause-Jensen et al. 2021) and even with active restoration efforts (Eriander et al. 2016). There may be particular challenges for deep eelgrass growing in high latitude areas with low light availability during winter. Eriander et al. (2016) found, following active restoration along the Scandinavian coast, the growth of eelgrass within deeper habitats (3.0–4.5 m) was substantially lower (40% loss to 50% increase) than in shallower habitats. This was apparently due to light limitation and high winter mortality. These workers proposed that while eelgrass persisted under these deep conditions, growth was very low, and the eelgrass was sensitive to temporary declines in water quality because it was near its minimum light requirements. Eriander et al. (2016) noted that the long-term survival of deep beds is uncertain, even after restoration attempts. At the time of writing the article, they note that no eelgrass restoration had been successfully achieved in Scandinavia.\nHowever, to acknowledge the small-scale recoveries that have occurred, we have modified\n7\nour statement to read as follows: “Seagrass decline has been documented in many coastal areas around the globe, and to date, there remain no examples of degraded seagrass ecosystems showing a full recovery at the large scale13,14”.\nReferences\nEriander L, Infantes E, Olofsson M, Olsen JL, Moksnes P-O. Assessing methods for restoration of eelgrass (Zostera marina L.) in a cold temperate region. J Exp Mar Biol Ecol 479, 76-88 (2016).\nVaudrey JMP, Kremer JN, Branco BF, Short FT. Eelgrass recovery after nutrient enrichment reversal. Aquat Bot 93, 237-243 (2010).\nL96 This statement is incorrect, and I note not substantiated by any human knowledge or reference. For the time period in question, global CO2 levels have been on a fairly linear upward trajectory. Regionalization typically refers to the regionalization of global climate models, and as such are unlikely to predict ‘intensification’. This appears to be both an exaggerated and unsubstantiated statement.\nThe reviewer seems to be objecting to the use of the term “intensified” in the following phrase “…sought to identify what caused the decline, including the role (if any) of putative drivers, including La Grande Complex hydroelectric power development (Figure 1, inset) and regional climate change, which intensified after the first phases of hydroelectric development”. We should have said “changes in the regional marine climate” to convey that the region experienced a rapid succession of major environmental changes in the mid- to late-1990s, including hydro development and significant step-changes in several aspects of the regional marine climate, including ice breakup dates and sea surface temperatures. We have removed the term ‘intensified’ and brought the sentence to a close after hydroelectric development.\nL98 The last paragraph comes out as being more of an advertisement than a brief summary of the study that would typically occur in an introduction. It seems to be a bit more methodological than I would expect, suggest shortening considerably and incorporating into the previous paragraph.\nWe edited the second half of the introduction as mentioned above. The last paragraph now follows naturally from the one at line 86 starting “Here, we present a new synthesis of recent evidence and transdisciplinary knowledge…”. We believe it is important to keep this\n8\nparagraph because it introduces the detection and attribution method and describes the words we used in the manuscript to reflect the strength of inference and uncertainty.\nReviewer #1 expressed their support for this ‘weight of evidence’ approach. We did manage to shorten this last paragraph of the Introduction from 198 to 147 words.\nFigure 2. It is unclear where the eelgrass limits for salinity and temperature came from. From both extensively looking at literature, and empirical observations, eelgrass can be highly abundant when temperatures are above 25 degrees C. It may in fact be necessary to stimulate flowering shifting from clonal to sexual reproduction, I am unsure where this came from. Secondly >5 psu (ppt is generally unused now as it refers to direct ion measurements not usually conducted) 75% of the time seems to be a really odd way to represent this. I have found the experimental literature value of 10 PSU corresponds really well to the distribution in estuaries using the mean salinity.\nA number of papers are cited in the text that show that eelgrass tolerates 10–27°C in summer, but subarctic populations appear more sensitive to extreme temperatures (< 25 °C) (Olesen et al. 2015 – ref 75 in the manuscript; Newton & Mudge 2003; Beca-Carretero et al. 2018).\nFor the Causal Model figure, we have changed ppt to psu and added a reference in the figure caption but we still feel that salinity >5 is an appropriate threshold even considering recent literature such as Zhang et al. (2022).\nZostera marina is well established to persist at salinities as low as 5 psu (den Hartog 1970). According to most sources, 10-25 psu is an optimal range for the species as a whole, though we note this species is widely distributed from Japan to Europe and has adapted to a great variety of local habitat conditions. It is found in the St. Lawrence marine system with salinity as low as 4 psu, in estuaries in British Colombia with salinities as low as 2 psu (Mary O’Connor, personal observation), and in the Baltic Sea with salinity as low as 6.5 psu (Rohr et al. 2018). It persisted in experimental treatments with salinity as low as 2.5 psu in Denmark (Biebl & McCoy 1971, Nejrup & Pederson 2008).\nReferences:\nBeca-Carretero P, Olesen B, Marba N, Krause-Jensen D. Response to experimental warming in northern eelgrass populations: Comparison across a range of temperature adaptations. Mar Ecol Prog Ser 589, (2018).\nBiebl, R. &, C.P. McRoy C. P. Plasmatic resistance and rate of respiration and photosynthesis of Zostera marina at different salinities and temperatures. Mar. Biol., 8, 48-56 (1971).\n9\nden Hartog C. The Sea-Grasses of the World. North-Holland Publishing Company (1970).\nNejrup, L. B. &, Pedersen, M. F. Effects of salinity and water temperature on the ecological performance of Zostera marina. Aquat. Bot. 88, 239-246 (2008).\nNewton A, Mudge SM. Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuar Coast Shelf Sci 57, 73–85 (2003).\nRöhr, M. E., Holmer, M., Baum, J. K., Björk, M., Boyer, K., Chin, D., et al. Blue carbon storage capacity of temperate eelgrass (Zostera marina) meadows. Global Biogeochemical Cycles, 32, 1457–1475 (2018).\nZhang YH, Yu B, Liu YC, Ma W, Li WT, Zhang PD. The influence of decreased salinity levels on the survival, growth and physiology of eelgrass Zostera marina. Mar Environ Res 182, 105787 (2022).\nFigure 3. The figure needs to clarify that in years with no or zero data, data was not in fact collected. The reader cannot distinguish between a zero value and the absence of data at present.\nAdditional information was added in the caption.\nL162 This is a very poor description of the hydrology. What is a ‘natural discharge’. Is that the mean annual discharge? And why is this number, whatever it is, being compared to a single month of February in the text? Why focus on February when the plant is pretty much absent. Eelgrass can disappear totally from areas in winter and reemerge in May. So why focus this on February? The mean annual discharge is shown in the figure, which establishes that this increased in LGR due to rerouting another river. However, this graph does nothing to show changes in the annual pattern of flow, which may very well be critical here and is essential for interpretation.\nAs the reviewer points out, changes in the annual pattern of flow are critical here and essential for interpretation. This is the reason we included details about the changes in flow for the month of February – i.e., as an example of how strongly the seasonality of flow was modified. We also note that historical data are limited but discharge data for February have been reported on several occasions (see refs 46 and 47 in the manuscript) so it is one of the months that is possible to compare before and after development. We also argue that\nWe have tried to smooth this portion of the text and be more specific in our terminology. The edited text at line 190 now reads as follows:\nDevelopment of LGR increased winter river flows, freshwater plume, and sediment and fluxes: The La Grande Complex, comprising 11 power generating stations, 74 generating units, and nine reservoirs, was constructed in three phases43,46,47. During Phase I (1973–1985), four rivers, including the Eastmain River, were partially diverted into the LGR watershed, increasing its flow. Peak LGR discharge shifted from spring to winter, with February flow rising from 520 m³ s-1 in 1975 to 1,750 m³ s-1 in 1980, and 3,000 m³ s-1 in 198446. Annual discharge from the Eastmain River after diversion dropped to about 10% of historical values. In Phase II (1987-1996), additional reservoirs and generation stations were added to the La Grande Complex, including La Grande-1 (LG1), <40 km from the bay, with a design flow of 5950 m3 s-1 43. In Phase III (2002-2013), partial diversion of the Rupert River further increased the average annual LGR discharge to 3782 m3 s-1, about double its pre-development discharge and nearly half the total discharge to James Bay48 (Figure 4). In recent years, high winter discharges were sustained at ~4,800 m3 s-1 continuously throughout the January–March period47.\nL167 There would seem to be little need to italicize annual here.\nThere are a variety of descriptions here, flow regime, overall discharge, salinity that are mixed together in such a form as to be entirely uninterpretable. Flow timing and quantity should be shown in a before and after hydrograph with daily average discharges as obviously things are happening in months other than February. If sediment changed, annual loads for a number of years before and after should be tabulated.\nThe descriptions given in this section reflect the limited historical data that are available. For example, it is not possible to show a “before and after” hydrograph with daily average discharges as suggested by the reviewer because some of these data do not exist (e.g., LG1 discharges became available only in 1995 after its commissioning) and other data related to ongoing flow regulation are proprietary. We hope we have made the discharge changes easier to understand by adding them into the description of the three phases of development at the beginning of this section of the manuscript.\nRegarding changes in sediment, we have edited the text at line 290 in the section entitled: “Excess sediment and organic loading impacted the LGR sector” to make the sediment changes clearer. Some of the changes are poorly quantified but we have stated the facts as reported by Hydro-Québec and its consultants.\nLine 181 I find the title of this section to be entirely unsubstantiated. No doubt there was an El Nino. This is weather, not climate. Sea surface temperature deviation seems increasingly\n11\nvariable but there is certainly no upward or downward trend. Excluding the strong El Nino year a trend is questionable. MHW is pretty arbitrary statistical definition and it is unclear that this in any way causes exceedances of the physiological range of temperature relevant to the plant. Overall though, while global change is occurring gradually, there is little evidence here of a ‘step change’ in ‘climate’, and the period examined is at the minimum for examining climate. There is a 3000 year reconstruction of climate in the area Vallerand 2024 that suggest temperature of 2 degrees higher than now on average, so the argument of this influencing zostera (which does very well in much warmer areas) is exceedingly weak.\nThis comment appears to have two distinct criticisms. First, that “there is little evidence here of a ‘step change’ in ‘climate’.” We have therefore provided additional evidence in Figure 4 that there is, indeed, a step change. A Pettitt test (a non-parametric test for change points) and Mann-Whitney test (assessing difference in medians) around the best change point year of 1998 were applied to all time series. This shows that the changes are large enough (and sustained enough) that it is reasonable to reject the null hypothesis of no step change (p < 0.05 comparing before/after 1998 for all variables). In the case of the river discharge, there are really two change points, 1986 being even stronger than 1998, so 1998-2024 is compared to 1986-1997 instead of 1951-1997. For the SSTs, 1996 is also a good change-point year, so 1979-1995 is compared to 1998-2021 (although using 1979-1997 would also yield a significant result). For the sea ice breakup, MHWs, and wind variables, 1998 is unambiguously the best change point as described at line 230 in the document.\nWe have also made it clearer that we do not mean to imply that the El Niño itself was a new climate, but rather than this extreme year may have helped push the system into a new state (a state that has persisted ever since). Global changes are indeed gradual, but the focus of this paper is on a regional change, and regionally, when overlaying internal variability on a long-term gradual global trend, it is quite possible for varying periods of abrupt change and near stagnation. (Results presented in a recent paper by England et al. on the variability of Arctic sea-ice trends illustrate this, as well: https://blog.fdik.org/2025-04/1281734.pdf).\nThe other key criticism appears to be that the Reviewer doubts the observed changes are sufficient to impact the eelgrass. Part of the reviewer’s logic is that the number of MHW days is arbitrary, which is why we also chose to present average SSTs as an additional measure. However, using just June for SSTs and seasonal MHW days was a bit of a mismatch.\nTherefore, we have changed Figure 4 to include average SSTs for June-October instead of just June.\nAnother part of the reviewer’s logic is that, based on the paleo record, they doubt the magnitude of change (in climate) is enough to impact the eelgrass. As mentioned above, here, we are not asserting that the extreme climate events (early ice breakup and intensification of marine heat waves) alone were the cause of the massive eelgrass declines. Rather, we argue that these events were just a trigger, something that alone likely would have represented just a short-term setback to eelgrass growth, but ultimately tipped off the\n12\nmassive die-off, because the eelgrass ecosystem had been pushed to near its tipping point by the environmental changes of decades of development. This is now stated clearly in the first part of the Discussion.\nLine 203, eelgrass declines are almost always due to light, so I have no doubt that the altered hydrology and salinity in conjunction with increased sediment has something to do with this. However, there seems to a paucity of information here. The authors are clearly aware of the irradiance required for eelgrass, yet compare the light attenuation to a single number in the Wadden sea despite a huge amount of literature on the subject. There is also no connection between the stated single value for light attenuation and the growth potential. FYI a value of 1.2 allows eelgrass to grow deeper than two meters and 1.79 does allow eelgrass to grow at depths of 1 to 2 meters, so does not entirely explain the absence.\nWe agree there is a huge amount of literature on the subject of light attenuation and the irradiance required for eelgrass, but we found few measurements for northern seasonally ice-covered populations. In our observations, which include records from two PAR sensors deployed on bottom-mounted moorings from March to August 2019, we found that only 0 to 11% of the surface (or incident) irradiance was transmitted through the water column to the water-sediment interface. This is below the minimal light requirements for northern eelgrass, which were found to be between 12% and 18% incident light (Lee et al. 2007– ref 60 in the manuscript). Furthermore, the estimate of the bulk PAR diffuse attenuation coefficient for the water column above the moorings, with PAR loggers at an average depth of 3.6 m, averaged 1.01 m⁻¹. We cannot provide much further detail in the manuscript because of limited space.\nHowever, we have revised this section at line 273 removing the reference to the Wadden Sea and referring to our observations: “During 2017-2021, Secchi disc depths along the coast were typically 2 m or less (Figure S6) and photosynthetically active radiation (PAR) at the seabed (2-4 m) was very low due to light attenuation by a combination of turbidity and CDOM.”\nWe removed the phrase “climate driven” agreeing that the causes of the observed browning are unknown, although there is increasing evidence that hydrology may play a role. As to\n13\nwhether CDOM is affecting PAR availability for eelgrass, the reviewer is right that CDOM absorption is minimal at > 600 nm, yet it is high between 400 and 500 and it definitively overlaps with the Soret band of chlorophyll absorption, so there will definitely be competition for light between CDOM and chlorophyll. We note that several east James Bay rivers have very high CDOM absorption coefficients (aCDOM(440) >10 m-1; Évrard et al. 2023), and that the James Bay rivers have among the highest DOC export yields reported for Northern rivers (except for LGR, de Melo et al. 2022 – ref 48 in the manuscript). Near these river mouths and also in the southern part of James Bay, where river influence is highest and most rivers are rich in CDOM, we also found a higher light attenuation coefficient in the water column compared to areas further north along the coast. We are not familiar with CDOM measurements for northern New Brunswick coastal waters or their effects on eelgrass light availability and health but we agree that further study of CDOM effects on eelgrass light availability are needed, especially in the context of the ongoing browning of inland waters across the Northern Hemisphere.\nReference:\nÉvrard, É., Fink-Mercier, C., Galindo, V., Neumeier, U., Gosselin, M. & Xie, H. Regulated vs. unregulated rivers: Impacts on CDOM dynamics in the eastern James Bay. Mar. Chem. 256, 104309, https://doi.org/10.1016/j.marchem.2023.104309 (2023).\nWe have added data to support the concept of a change in winds and storms. Average wind speed (at 10 m) is now reported in Figure 4 along with the other variables. It’s a small increase, but it is statistically significant (again, using p < 0.05) and, notably, the best change point is the same year as for the sea ice and the MHWs (1998). The coincidence of these changes does not prove a physical connection, of course, but it is certainly consistent with one. To better reflect the nature of the evidence we have changed “frequency and intensity of storms” to “spring storminess”. With this we are not claiming that these patterns have never occurred in the past or that they will necessarily persist in the future, we are simply describing the patterns as observed during the relevant time frame of this study.\nWe are not sure what, specifically, the reviewer objects to in Figure 5. We regret that the word ‘suspected’ was missing from the figure in the file and wonder if this caused confusion. We feel this figure is important to summarize the environmental changes described briefly in the text and to show that the LGR sector has experienced several environmental changes from hydro development that the other sectors have not experienced. We have revised the caption to more clearly explain what we are trying to show in this figure.\n267 eelgrass does not grown in winter, period. It may not even be present as it wracks very substantially in the fall and can entirely disappear from area, to reemerge in the spring. This is especially true if reproduction from seed and not clonal reproduction is occurring. As there are no leaves 99.9% of carbon fixation occurs between May and October.\nWe do not agree with the reviewer on this point and cite a paper that proves eelgrass can grow in winter in northern areas (Olesen et al. 2015 – ref 43 in the manuscript). To quote from this paper, “The long leaf lifespan of these northern eelgrass populations indicates that they maintain metabolically active leaves during winter, as has been observed in other subarctic eelgrass populations and in freshwater macrophytes under winter ice cover (McRoy 1969 – ref 62 in the manuscript, Boylen & Sheldon 1976).” We also have observed eelgrass under the sea ice along the Eeyou Istchee coast (Chris Peck and Zou Zou Kuzyk, unpublished) and found evidence of winter growth in rhizomes of eelgrass from perennial beds (Mary O’Connor and Kaleigh Davis, unpublished data). We do agree that most of the carbon fixation occurs in summer, but this does not rule out that physiological stress during winter or early spring could hinder eelgrass growth and recovery.\nReferences\nBoylen CW, Sheldon RB. Submergent macrophytes: growth under winter ice cover. Science 194, 841−842 (1976).\n___________________________________________________________________________\n>>Seagrasses are foundation species in many coastal ecosystems. They provide critical habitat for marine and semi-aquatic wildlife, such as waterfowl, and the reliable, nearshore wildlife harvesting opportunities in seagrass ecosystems have been particularly important for many coastal Indigenous Peoples’ food security and cultural continuity\nThis is an excellent way to start, setting up the importance and why - this often gets lost in western mainstream systems, and to explain it clearly and succinctly is excellent.\nThank you for the kind remarks on our paper.\n>>Protecting and restoring degraded seagrass ecosystems may thus contribute to numerous benefits of interest to both governments and coastal communities10-12.\nWould like to see this expanded a little and clarify something like 'both cultural, non-Indigenous and ecosystems'\nReworded as follows: “Protecting and restoring degraded seagrass ecosystems may thus contribute to numerous benefits of interest to both Indigenous and non-Indigenous coastal communities, as well as for the ecosystems themselves.”\n>>However, the catastrophe went unrecognized by the global research community for nearly two decades.\nHere would be a good place to follow up with an explanation sentence why it went unrecognized - did western scientists ignore Cree?\nThe Crees voiced their concerns at the onset of the eelgrass decline and presented these at the House of Common of Canada in 2008. Although the decline was acknowledged, no academic or government-led scientific effort was made to investigate its causes. We added this to the introduction.\nWere calls for help disregarded, not funded?\nWhile the Department of Fisheries and Oceans Canada recognized the need to further assess the situation following the Cree presentation at the House of Commons of Canada in 2008 (FOPO et al. 2008 – ref 39 in the manuscript), the Canadian government did not initiate any research program in the region. Hydro-Québec did not extend its monitoring efforts to include scientific research.\nDid the Cree have policies that did not allow research?\nIK is often tracked carefully, but it's a good reminder to western science that this *does* occur and explain why the system got to the point/led up to the point it is at, especially when you follow up with this sentence in the next paragraph \"We present this example because we believe such massive ecological collapses caused in part by past development, are all too common, yet traditional scientific approaches have limited our ability to understand these changes and determine actions to mitigate them36.\" it helps make it more clear to those who don't work or understand IK.\nWe have tried to improve the balance between IK and science throughout the manuscript. In this instance, we have edited the above sentence slightly to read “We present this case as an example of how large-scale ecological collapses—often linked to past development—are widespread, yet traditional scientific methods alone have struggled to explain or guide responses to them33.” We also removed material from the preceding paragraph that was not necessary for the Introduction and detracted from the main points.\nThe Cree knowledge of the eelgrass ecosystem collapse is now included as the first section of the Results part of the paper entitled “Components and collapse of an eelgrass-goose-Eeyou system”.\n>>Cree from Chisasibi noted localized eelgrass declines in some areas near the La Grande River (LGR) but no changes were observed in other coastal communities. Does this mean all coastal communities, or only First Nations, or only non-First Nations -?\nHere we meant other Cree coastal communities south of Chisasibi. We reworded this sentence to clarify the meaning.\nSections 2-3 are void of IK - this would be a great place to weave in the IK information that has been documented that would corroborate the information\nThank you for this suggestion. As mentioned, we have taken your suggestion to heart and added section 1 at the start of the results containing the Cree knowledge of the eelgrass-goose ecosystem and the collapse. We also have included IK more thoroughly in subsequent section as specified below.\n2. Detection of environmental changes\nDevelopment of LGR increased winter river flows, freshwater plume, and sediment and fluxes\nWe added the following:\nMarine climate underwent a step change in 1998\nWe added the following:\n“Coastal Eeyou have remarked on the way climate change is transforming coastal ecosystems and mention, in particular, loss of sea ice45.”\nWater clarity decreased along the Eeyou Istchee coast\nWe reworded one sentence to keep more details and context of the Cree knowledge:\n“Eeyou report that coastal marine water changed from transparent blue to murky brown in Chisasibi between 1986 and the early 1990s and a decade later in Wemindji45.”\n>>Based on review of Cree knowledge\nHow? Was this through archived materials, or were First Nations members asked?\nYes, both. Cree land users co-designed and conducted field work along the coast between January 2016 and August 2021 and iteratively reviewed results and contributed to refining the study questions, design, and implementation year after year. Cree participated in recording their knowledge between July 2019 and June 2022 including 27 coastal traplines and 66 semi-structured and participatory mapping interviews.\nTo make this information clearer from the outset, we have added the following sentence to the Introduction:\n“The evidence incorporated diverse perspectives, ranging from Cree Indigenous Knowledge shared in interviews to long-term eelgrass monitoring data collected over 30 years.”\n>>Based on review of Cree knowledge and scientific evidence in a detection and attribution framework, we infer that, in Eeyou Istchee,\nThe beginning of this sentence makes it seem as if the 2 ways of knowledge are not equal. A better way to begin this might be \"Based on Cree Indigenous Knowledge systems and scientific evidence\" or \"Based on Cree Indigens Science and western scientific evidence\", this way it illustrates to readers that both systems have validity and assist to prove the decline of eel gras and the ecosystem\nWe apologize for giving this impression. We reworded this first part of the Discussion so that it reads as follows:\n“Indigenous Cree hunters in James Bay, subarctic Canada, have observed many changes in the coastal environment as they adapt to shifts and changes in local and regional conditions that impact the goose hunt40. Pairing this Indigenous understanding with scientific data in a detection and attribution approach, we conclude that the cumulative effects of hydroelectric\n18\ndevelopment in the region and on the La Grande River, in particular, over >20 years gradually overcame the natural resilience of the eelgrass ecosystem, setting the stage for a regional ecosystem collapse triggered by extreme climate events in 1998. The loss of eelgrass cover and biomass has not reversed decades later, nor have the massive flocks of geese returned to using the coastal habitat along the northeast coast (Figure 6).”\n>>Regardless, this large “genomic offset” implies that the northeast James Bay eelgrass population is more vulnerable to climate change than better-studied populations in temperate regions.\nNice finding, and well stated!\nThank you for your kind words.\n>>along the Swedish west coast after the loss of eelgrass beds, where increased sediment resuspension and proliferation of drifting algal mats prevent both natural recovery and human restoration of eelgrass77.\nIs there Swedish IK information that corresponds to their findings in western science? Just curious\nGood suggestion! But unfortunately we were not successful in finding Swedish IK information on this topic.\n>>In Québec, as elsewhere, hydropower development is being considered on a scale not seen since the 1970s, alongside other types of developments (mining, ports, etc.). It is vital that future impact assessments proceed differently, considering coastal ecosystems, employing multiple knowledge systems, and trying to anticipate how climate change may compound other impacts.\nThank you.\nexcellent wrap up here\nOverall:\nThe use of the Indigenous term \"Shikaapaashkw\" in the title itself is great, but not explained and a little confusing for readers who may not understand why it was used or what it is, especially if they are looking for information on climate change or IK generally and don't have an ecosystem or eelgrass background.\nWe revised the title to help address this. It now reads:\n“Losing Shikaapaashkw: eelgrass ecosystem collapse and social-ecological regime shift driven by hydropower development and climate change”.\nThis paper is western science heavy, with the IK not interwoven as well as it could be, and could be utilized to make the points stronger, particularly since one of the claims is that Indigenous are having to adapt. The decline of the grass and the environment is clear, but the IK isn't consistent throughout, and makes it appear as if IK and First Nations were used as leverage to land the funding rather than do honest research inclusive of Indigenous Peoples.\nWe have taken this comment to heart and revised several parts of the Introduction, Results, and Discussion to try to improve the interweaving of the IK and science and make clear that throughout all aspects of the research program, Indigenous knowledge and scientific knowledge were considered as distinct but equal sources of information. In particular, the new section at the start of the Results, “Components and collapse of an eelgrass-goose-Eeyou system”, combines content from the last section of the results with some of the system description from the introduction with the intent of forefronting Cree knowledge and clearly presenting this knowledge and experience as a result, reflective of its validity as one of the primary pillars of evidence reported in this research. In addition, we edited the other results sections (detection of eelgrass change, detection of environmental change) so they better intermingle Cree knowledge with science results. We believe the new proposed section 1 of the results better forefronts Cree knowledge and experience, then follows it with very strong and compelling combined evidence focused on eelgrass and the environment.\nWe note that the Cree initiated and funded the research, so it was very much not a situation in which their involvement was leveraged for funding. We have written about this process in another paper (Fink-Mercier et al. 2024 – ref 29 in the manuscript). We have added this in the acknowledgements. We very much would like to avoid giving the impression that their participation was leveraged, so we sincerely appreciate this comment.\n>>>>Indigenous knowledge\nCree knowledge from the Eeyou coast is well suited to detecting change, as Cree rely on observations of their environment at multiple scales during their harvesting activities5. The Indigenous knowledge component of this study was community-driven, with input from Cree land users, eelgrass ecologists, waterfowl experts, and the project's steering committee6,7. Cree land users co-designed and conducted field work along the coast between January 2016 and August 2021. Cree participated in recording their knowledge between July 2019 and June 2022 including 27 coastal traplines and 66 semi-structured and participatory mapping interviews. The study engaged 95 Eeyou land users, including tallymen and elders. Indigenous knowledge and Western science were both central to this study, influencing planning, data collection, analysis, synthesis, result presentations, and final reports8.\nThis section is lacking the information about what protections this team elicited for data sovereignty of Indigenous groups, and acknowledgement of Indigenous Knowledge sovereignty. Were IRBs used? Did they discuss with First Nations or Cree Councils? Was all sensitive data then given to the Cree and not released, or what happened to the data collected? Studies such as this may release findings and all data without Indigenous groups knowing or understanding, and such knowledge is impossible to then get back in control of. Did the Cree know of and consent to this publication?\nWe apologize for this oversight. Yes, the Cree know of and consented to submitting this article for review for publication. The paper was presented, discussed and revised based on feedback provided by the representatives of the coastal Cree communities who participate in the project’s steering committee, in accordance with the process implemented throughout the project. The Cree not-for-profit organization Niskamoon set the terms of the research protocol specifying that coastal Cree land users must be involved in all fieldwork, with priority always given to family-members of the traplines where the work is to be carried out, and that an iterative exchange of knowledge was to take place between the researchers and Cree land users. No trapline was visited without the express permission of the tallyman. The terms also specified that all data and knowledge generated through the research program be returned to the participating communities in a format that encouraged discussion and sharing. Cree Ecological Knowledge documented by the program remains the sole collective property of the Cree Nation. The researchers conducted knowledge exchange workshops with land users in each community during winter, spring, and summer of 2022, followed by a Results Symposium in September 2022 that was aired live on the community radio. The integration report was completed in 2023, after these consultations, and distributed for feedback. This manuscript was prepared last specifically to ensure that all the coastal community members had the opportunity to learn about and give feedback on the results.\nThe Indigenous Knowledge subsection of the Methods was revised as follows:\n“The Indigenous knowledge component of this study was community-driven, with input from Eeyou land users, eelgrass ecologists, waterfowl experts, and the project's steering committee6,7. Eeyou engagement in every step of the research was specified in the formal research agreements between the Eeyou organizations and the universities, and these terms were adhered to by the university researchers. These agreements specified protocols for returning all data to the communities and respecting privacy of material in interviews, consistent with established FAIR and CARE principles.\nThe Behavioural Research Ethics Board of the University of British Columbia approved the components of this research that relied on formal interviews with Eeyou people (H20-02942)6. This work fully complies with the Tri-Council Policy Statement: Ethical Conduct for Research Involving Humans (TCPS 22018). The ethical obligations surrounding informed consent in research involving Indigenous Peoples align with Article 9.1 of the TCPS. Additionally, this study adhered to the principles outlined in individual Research and Information Sharing Agreements executed between the principal investigator and the respective First Nations Governments. Through formal interviews, Eeyou participated in recording their knowledge between July 2019 and June 2022 including 27 coastal traplines\n21\nand 66 semi-structured and participatory mapping interviews. The study engaged 95 Eeyou land users, including tallymen and elders. Indigenous knowledge and Western science were both central to this study, influencing planning, data collection, analysis, synthesis, result presentations, and final reports.\nThrough the processes developed under the research agreements with Niskamoon and the project steering committee8, Eeyou land users co-designed and conducted field work along the coast between January 2016 and August 2021. Details on the interweaving of Eeyou knowledge and science through informal channels are given in Fink-Mercier et al. (2024)8 and the project’s final report (Kuzyk ZA, et al. Understanding Shkaapaashkw (ᔑᑳᐹᔥᒄᐦ): Eelgrass Health and Goose Presence in Eastern James Bay. Final Report from the Eeyou Coastal Habitat Comprehensive Research Project (CHCRP). Prepared for Niskamoon Corporation. University of Manitoba (2023). DOI: https://doi.org/10.34992/4K4Z-TF96).”\nVisuals are very clear and easy to follow, well laid out for manuscript\nThank you.\n22"}, {"round": 2, "reviewer_comments": {"reviewer_1": "The authors have taken the comments and criticism of all three reviewers seriously and made substantial, conscientious efforts to respond to them. They clarified several confusing passages, revised the key figure 4, and re-organized portions of the text to make the arguments clearer and better substantiated. I believe the MS is much improved. A few, relatively minor comments:\nThe authors cite Eriander et al. (2016) at several points in the rebuttal letter, but the paper is apparently not cited in MS. If it is important in supporting their argument, it should be cited.\nResponse to reviewers, p 2: Reviewer 2 of original MS took issue with the author's statement on line 62: \"seagrass decline has been documented in many coastal areas around the globe, and to date, there remain few examples of degraded seagrass ecosystems showing a full recovery.\" The reviewer argues that this statement is untrue. The authors disagree with the reviewer and then cite numerous examples of how long it takes seagrass to recover. But the disrupted statement was not about the time course of recovery, but rather whether full recovery actually happens. One could nitpick about what a “full recovery” actually is - and I agree that there are \"few\" - but I also agree with reviewer 2: th eelgrass lost to widespread wasting disease in the 1930s did fully recover in many areas naturally, and in the case of the Virginia coastal lagoons recovered much later as a result of active restoration, which is widely seen as the most successful restoration of seagrass in the world. The authors seek to refute the reviewer’s comment by noting that there is only one study with \"clear data\" pre-wasting disease (Krause-Jensen). That may be, but there is also the lived experience of thousands of people living along the coasts of Atlantic Europe and North America who saw the grass come back from a severe or completely degraded state over the years. It's a bit ironic that, in a paper that seeks explicitly to elevate traditional, in this case indigenous, knowledge, such experience is not considered. To be clear, I have no quibble with the main argument – the evidence is strong that seagrasses take a long time to recover in general, if they ever do. But I agree with reviewer 2 that this statement was misleading. Unfortunately, the revised text actually makes matters worse by adding that there are no examples of full recovery \"at the large scale\". In fact, the recovery in North Atlantic after the wasting disease is perhaps the only known recovery of seagrass at the large scale! It should be acknowledged even if it is a special case.", "reviewer_3": "All changed and revisions are excellent. This team has clarified everything sufficiently, and well. These are noteworthy, and important results.\nThe work supports the claims and conclusions. No further revisions necessary.\nNo flaws found\nMethodology is sound\nEnough data for the study to be reproduced\nNice revision!"}, "author_response": "Response to Reviewers’ Comments (Second Round)\nReviewer #1 (Remarks to the Author):\nThe authors have taken the comments and criticism of all three reviewers seriously and made substantial, conscientious efforts to respond to them. They clarified several confusing passages, revised the key figure 4, and re-organized portions of the text to make the arguments clearer and better substantiated. I believe the MS is much improved. A few, relatively minor comments:\nWe thank the reviewer for these positive comments.\nThe authors cite Eriander et al. (2016) at several points in the rebuttal letter, but the paper is apparently not cited in MS. If it is important in supporting their argument, it should be cited.\nWe have added Eriander et al. (2016) to the reference list.\nResponse to reviewers, p 2: Reviewer 2 of original MS took issue with the author's statement on line 62: \"seagrass decline has been documented in many coastal areas around the globe, and to date, there remain few examples of degraded seagrass ecosystems showing a full recovery.\" The reviewer argues that this statement is untrue. The authors disagree with the reviewer and then cite numerous examples of how long it takes seagrass to recover. But the disrupted statement was not about the time course of recovery, but rather whether full recovery actually happens. One could nitpick about what a “full recovery” actually is - and I agree that there are \"few\" - but I also agree with reviewer 2: th eelgrass lost to widespread wasting disease in the 1930s did fully recover in many areas naturally, and in the case of the Virginia coastal lagoons recovered much later as a result of active restoration, which is widely seen as the most successful restoration of seagrass in the world. The authors seek to refute the reviewer’s comment by noting that there is only one study with \"clear data\" pre-wasting disease (Krause-Jensen). That may be, but there is also the lived experience of thousands of people living along the coasts of Atlantic Europe and North America who saw the grass come back from a severe or completely degraded state over the years. It's a bit ironic that, in a paper that seeks explicitly to elevate traditional, in this case indigenous, knowledge, such experience is not considered. To be clear, I have no quibble with the main argument – the evidence is strong that seagrasses take a long time to recover in general, if they ever do. But I agree with reviewer 2 that this statement was misleading. Unfortunately, the revised text actually makes matters worse by adding that there are no examples of full recovery \"at the large scale\". In fact, the recovery in North Atlantic after the wasting disease is perhaps the only known recovery of seagrass at the large scale! It should be acknowledged even if it is a special case.\nWe have revised this paragraph to acknowledge the North Atlantic eelgrass recovery.\nThe paragraph now reads: “Many seagrass populations around the globe have massively declined in the past century. Few have fully recovered to their historical depth and spatial extents, although North Atlantic eelgrass lost to widespread wasting disease in the 1930s is considered naturally recovered in many areas, and recovered as a result of active restoration in other areas13,14. Incomplete recovery of degraded seagrass ecosystems is often characterized by lower shoot density15, reduced depth extent16, and/or reduced spatial extent16-18 of meadows relative to historical observations, as well as reduced usage by wildlife and ecological functions such as carbon storage19. The reasons for failure to fully recover can be unclear, especially when proximate causes of declines and related environmental conditions have improved18-21.”\nReviewer #3 (Remarks to the Author):\nAll changed and revisions are excellent. This team has clarified everything sufficiently, and well. These are noteworthy, and important results.\nThe work supports the claims and conclusions. No further revisions necessary.\nNo flaws found\nMethodology is sound\nEnough data for the study to be reproduced\nNice revision!\nWe thank the reviewer for these positive comments."}]

Decision letter