Warming ocean temperatures, temperature anomalies, and marine heatwaves (MHW) are becoming stronger, longer and more frequent (Frölicher et al., 2018; Hobday et al., 2018; Gupta et al., 2020). Temperature affects all aspects of biology, from subcellular biochemical reaction rates to reproductive success, evolutionary mutation rates and selection pressures (Hoegh-Guldberg and Bruno, 2010; Doney et al., 2011). It is therefore not surprising that temperature anomalies can have pervasive impacts on marine productivity (Beaugrand and Reid, 2003; Montie et al., 2020), community structure (Wernberg et al., 2013; McPherson et al., 2021) and ecosystem processes (Smale et al., 2019; Gupta et al., 2020). These ecological changes are particularly noticeable when warm anomalies and MHWs affect large habitat-forming foundations species, like seagrass (Thomson et al., 2015; Arias-Ortiz et al., 2018), coral reefs (Le Nohaïc et al., 2017) and kelp (Wernberg et al., 2013, 2016). Impacts from MHWs on kelp have been documented in Tasmania (Oliver et al., 2018), Western Australia (Wernberg et al., 2013, 2016), North America (Arafeh-Dalmau et al., 2019; Rogers-Bennett and Catton, 2019) and Europe (Filbee-Dexter et al., 2020), and have, in extreme cases, caused range contractions and regional extinctions (Smale and Wernberg, 2013; Wernberg et al., 2016; Straub et al., 2019; Smale, 2020). High temperatures often have predictable physiological effects on kelp tissue and population growth rates (Tait, 2014; Mabin et al., 2019). However, impacts on abundances, communities and ecosystem functioning are complicated by indirect effects, altered competitive hierarchies, the timing and magnitude of specific MHWs as well as latitudinal distribution and thermal responses of individual kelp species (Doney et al., 2011; Wernberg et al., 2016; Smale et al., 2019). For example, it has been shown that MHWs can have a strong negative impact on kelps near their warm equatorial range limit, but no or positive effects near their colder poleward range (Wernberg et al., 2010, 2016; Reed et al., 2016; Arafeh-Dalmau et al., 2019; Cavanaugh et al., 2019), highlighting the importance of measuring impacts and variation across latitudes.

To date, most research about impacts from MHW on kelp forests have focused mainly on temperature effects alone (Reed et al., 2016; Wernberg et al., 2016; Arafeh-Dalmau et al., 2019; Cavanaugh et al., 2019; Straub et al., 2019; Filbee-Dexter et al., 2020; Smale, 2020). A few studies have shown that grazing and wave exposure may alter and even increase temperature-induced loss of kelp beds (Ling et al., 2009; Rogers-Bennett and Catton, 2019; Butler et al., 2020). Bell et al. (2015) showed that over large biogeographic gradients, decadal climatic patterns (e.g., the North Pacific Gyre Oscillation Index), nitrate availability and wave disturbance largely accounted for giant kelp biomass and had profound spatial differences in effect sizes. Because ecological stressors rarely operate in isolation (Crain et al., 2008; Harvey et al., 2013; McPherson et al., 2021), it is of fundamental importance to identify and test for MHW impacts in concert with other stressors, like low nutrient levels and reduced water clarity. For example, range contraction of giant kelp (Macrocystis pyrifera) near its southern limit in Mexico correlate with cyclical El Niño events because a combination of warm waters and low nutrient levels reduce growth, reproduction and survival (Hernandez-Carmona et al., 2001; Edwards and Hernandez-Carmona, 2005). However, there are few, if any, kelp studies that have formally tested for interactive effects between temperature anomalies, nutrient availability, and water clarity across a latitudinal gradient.

New Zealand, like several other bioregions (Gupta et al., 2020), recently experienced the warmest summer on record associated with the extreme Tasman Sea MHW over the austral summer of 2017–18 when sea surface temperature increased to more than 23°C (c. 4–5°C greater than average) around some parts of South Island (Salinger et al., 2019; Thomsen et al., 2019; Salinger et al., 2020). This heatwave caused migrations of northern warm-water fishes, glacial melting, early harvest of summer fruit, and loss of large habitat-forming intertidal southern bull kelp (Durvillaea spp.) (Salinger et al., 2019; Thomsen et al., 2019; Thomsen and South, 2019; Salinger et al., 2020). However, it is unknown if other marine foundation species were affected and if co-occurring stressors modified impacts. In contrast to many other coastlines inhabited by kelp, the southern New Zealand coastline is characterized by high sediment runoff and therefore low water clarity, partly associated with natural conditions (steep topography, soft bedrocks, high precipitation) and partly by extensive land-usage changes, such as converting natural forest to pasture (Ewers et al., 2006; Schiel and Howard-Williams, 2016). It is therefore possible that low water clarity modified ecological impacts from the 2017/18 MHW.

Macrocystis is an iconic and conspicuous, habitat-forming, foundation species inhabiting shallow subtidal rocky reefs along the southern coastline of New Zealand, with a northern range around 41°S on the southern part of the North Island (Hay, 1990; Nelson, 2020). Macrocystis beds are highly productive and characterized by high biodiversity and extensive surface-floating canopies (Foster and Schiel, 1985; Hepburn et al., 2007; Reed et al., 2016; Mabin et al., 2019; Tait, 2019). Previous research from New Zealand has shown that Macrocystis responds negatively to low light levels and that low water clarity and sedimentation reduce its maximum depth to only 10–15 m (Desmond et al., 2015; Tait, 2019), a compressed range compared to 30–50 m depth distribution in clearer waters in North America (Foster and Schiel, 1985; Graham et al., 2007). Understanding whether recent MHWs and low water clarity in concert affected Macrocystis is critical in understanding and managing effects of sediment loads from land-based sources, as the ocean warms and extreme heat events become more common (Frölicher et al., 2018; Hobday et al., 2018; Oliver et al., 2019).

Here, we quantified the abundances of Macrocystis canopy cover over 5 years, including the most extreme MHW on record, and within 3 zones in each of four regions, covering its latitudinal range on mainland New Zealand. More specifically, we analyzed satellite images over 60 months to determine if sea surface temperature and temperature anomalies affected the cover of surface canopies and if diffuse downwelling attenuation (K_d) and chlorophyll-a (a reasonable proxy for nutrient limitation; Goes et al., 1999, 2000) modified or enhanced temperature effects.

One consequence of reaching the sea surface is that spectral signatures of Macrocystis are relatively easily detected by satellites (Bell et al., 2020; Mora-Soto et al., 2020), whereas most other marine macroalgae (except intertidal species) are continuously submerged and their spectral signatures dissipated through the water column. Cavanaugh et al. (2011) presented a thorough example of the requirements for gauging surface canopies over time through remote sensing by satellites; they were able to ground-truth kelp biomass by comparing data from subtidal surveys over different seasons and years to canopy cover using remote sensing products. In New Zealand, unfortunately, there are few estimates of Macrocystis biomass but, nevertheless, remotely quantifying the areal coverage of Macrocystis provides scalable metrics of ecosystem health (Hamilton et al., 2020). One important benefit of passive remote monitoring by satellites is that it removes or reduces the requirement for in situ subtidal surveys, while providing a platform to examine kelp bed size efficiently and objectively over broad geographical ranges and significant oceanographic gradients. However, the limitations and assumptions of using satellite imagery for these purposes must also be recognized.

Passive remote sensing is now widely used (Bell et al., 2020; Huovinen et al., 2020; Mora-Soto et al., 2020; Hamilton et al., 2020) and the approach generally computes vegetation indices based on measurements of near infrared electro-magnetic radiation. These indices detect vegetation not occluded by overlying water, giving a direct measurement of only the floating portion of macroalgal canopies. By limiting detection to surface canopies, these datasets are unable to integrate the full population dynamics of Macrocystis and give no insight into the presence of subsurface forests. Although these satellite methods cannot observe subsurface forests, surface cover of Macrocystis is a key indicator of the health and vitality of the depth integrated giant kelp populations so that, remotely sensed time series have great potential for identifying the integrated responses of kelp beds to multiple stressors (Cavanaugh et al., 2011).

Mean SST anomalies between December 2015 and December 2020 showed strong warming trends along much of the coastline of southern New Zealand (Figure 1A). The normally cooler southern regions had the greatest mean anomalies (+1.5–2°C warmer than average) between 2015 and 2020. Conversely the normally warmer northern regions experienced some of the coolest mean temperature anomalies (−0.5–0°C cooler than average) across the whole region (Figure 1A). The influence of mean monthly temperature anomalies on the mean monthly cover of Macrocystis varied across regions, with minor warm anomalies (c. +1°C) reducing the kelp cover toward the northern limits of its range, whereas at the southern-most region (4. South), large anomalies (c. +3°C) had a negative but less dramatic effect on coverage (Figure 1B). In the central regions (2. North-East, 3. South-East) warm anomalies associated with summer MHWs caused notable reductions in surface canopies (Figure 1B). The central region (2. North-East) had the most extreme warm anomalies (4.7°C above average for December 2017, during the severe MHW), and the biggest range of anomalies (Supplementary Figure 3). The southern two regions had no monthly mean temperatures below average for the 5-year period (Supplementary Figure 2).

At the northern extent of Macrocystis, SST averaged 16°C over the 5-year period (December 2015 till December 2020), but at the southern boundaries of giant kelp the average dropped to c. 13.5°C (Figure 2A). The mean and full range of temperatures experienced (as shown by the span of the x-axis, Figure 2B) within regions varied over the 5 years, the North region averaged c. 16°C and spanned 9°C, North-East averaged c. 15°C and spanned 11.5°C, South-East averaged had c. 14.0°C and spanned a 9.5°C range, and the South region averaged c. 13.5°C and had the narrowest thermal range (7.5°C) (Figure 2B). Declining cover of Macrocystis was observed in all regions, but by far the biggest response was in the North-East and South-East regions where temperatures above c. 18°C caused large reductions of Macrocystis canopy cover (Figure 2B).

The effect of water clarity on kelp coverage varied across regions, as did the range of light attenuation observed. Macrocystis populations in the North (1) experienced uniformly higher water clarity (i.e., K_d), with no detectable response in kelp cover relating to it as a single factor (Figure 3A). However, the North-East and South-East regions (2–3) experienced the greatest range of water clarity, which related to a loss of canopy cover. This relationship was clear only for the North-East region (2), however, as the apparent negative relationship in the South-East region was dependent on only one reading of high K_d and did not depict a reliable trend (Figure 3B). Conversely kelp coverage of the South region (4) was, somewhat anomalously, positively related to increasing K_d (Figure 3B). This region had a positive relationship between kelp coverage and potential nutrient availability (i.e., chl-a; Figure 3B), but this was not statistically significant.

The time series of kelp coverage averaged across all regions and zones showed a dip in kelp coverage that was coincident with the severe MHW in 2017–2018 (Figures 4A,B and Supplementary Figure 3). Water clarity and chl-a showed no discernible temporal trend (Figures 4C,D), although there was a slight depression of chl-a during the 2017–2018 MHW. To assess covariance among predictor variables (chl-a, K_d, temperature anomalies) we assessed the strength of linear and non-linear correlation using a separate GAM model excluding the influence of predictors on kelp coverage. Covariance analyses of these variables showed strongest correlations between chl-a and K_d, and temperature anomalies and chl-a (Table 1). There was no significant correlation between temperature anomalies and water clarity (Table 1).

Across all regions, the coverage of kelp showed strong trends with temperature, and K_d (Figure 5). Temperature anomalies had a peak positive effect on kelp coverage between +1 and +2°C, and a pronounced negative effect beyond +2°C (Figure 5A). Maximum monthly temperatures between 9 and 18°C were associated with stable coverage of kelp, but coverage declined steeply beyond 18°C (Figure 5B). Kelp coverage was highly variable at the low ends of K_d (clearer water) and declined beyond K_d values of 0.3 (Figure 5C). Increasing potential nutrient availability (as indicated by chl-a) had no discernible overall effect on kelp cover (Figure 5D). While interactions between chl-a and other parameters were tested, none contributed to deviance explained and were dropped from the final model. General additive models (GAM) indicated that temperature anomalies, maximum monthly temperature, and light attenuation contributed most to the cover of Macrocystis (Table 2 and Supplementary Figure 2). Concurvity, or collinearity of variables showed that model parameters were between 0.5 and 0.17 (values close to one indicate redundancy). The interactive model also revealed a significant two-way interaction between temperature anomalies and K_d (Table 2 and Supplementary Figure 4).

The interactive effect between temperature anomalies and K_d was shown in a two-way interactive model, where rising temperature anomalies and falling water clarity combined to strengthen the decline in kelp coverage (Figure 6). In clear water (i.e., low K_d) temperature anomalies had little effect on kelp cover between −2 and +1°C, but beyond +1°C kelp coverage declined more rapidly. This effect was accentuated in low water clarity (i.e., high K_d).

Giant kelp, Macrocystis pyrifera, is one of earth’s fastest growing photosynthetic organisms, and is a key contributor to carbon fixation and habitat provision for temperate marine ecosystems across a large extent of the world’s temperate coastlines (Schiel and Foster, 2015; Miller et al., 2018). Recent studies have shown that Macrocystis and other large kelps have had retractions or reductions in their distribution in the northern hemisphere (Arafeh-Dalmau et al., 2019; Rogers-Bennett and Catton, 2019) in response to environmental fluctuations and combined physical and trophic interactions (Ling et al., 2009, 2015; Bell et al., 2015). In southern Australia, Macrocystis has experienced massive retractions, and is nearing functional extinction in some regions in response to oceanographic shifts affecting nitrogen concentrations, temperature, and larval delivery of a key sea urchin grazer (Johnson et al., 2011; Mabin et al., 2019; Butler et al., 2020). The results of our study suggest that if current seawater warming trends continue, they could affect the cover of Macrocystis across much of its current range in southern New Zealand. Although temperature was the major driver we identified, it is also evident that declining water clarity has negative effects on giant kelp. We also showed that the negative effect from high water temperature is exacerbated by low water clarity. Unlike other studies (Dean and Jacobsen, 1986; Mabin et al., 2019), however, the correlation between MHW events and depressed chlorophyll-a (as a proxy for nutrient limitation) was not evident.

The southernmost region studied (−46° latitude) showed some resilience to warming events but those just to the north (−45° latitude) were more affected. This may have been due to the intensity of the MHWs in those regions, which highlights that MHWs do not have a uniform and constant effect along a heterogeneous coastline. The steep decline with increasing temperatures in the central regions may be due to potentially greater susceptibility of cold-adapted populations. At the northern extent of Macrocystis distribution (–41° S) temperatures during the 5-year study period were colder on average (compared to the 38-year time series of sea surface temperature; Reynolds and Banzon, 2008), but even small positive anomalies were associated with reductions in cover. This is surprising given that the extreme warm temperatures experienced in New Zealand are 3–5°C cooler than those experienced by Macrocystis forests in California (2014–2016; Cavanaugh et al., 2019). Some evidence suggests that higher latitude populations are more vulnerable to reproductive failures under temperature stress (Hollarsmith et al., 2020). Additional stressors may also be responsible for this massive disparity in temperature thresholds. Of the parameters tested (expect temperature) at a larger scale over all regions, only declining water clarity (increasing K_d) was associated with loss of kelp canopies. In situ studies within the South-East region (3) showed declines in all life history stages of Macrocystis at sites with locally compromised light availability (Tait, 2019). Although the surface canopies detected during this study are less immediately threatened by low water clarity, the ability of juvenile gametophytes and sporophytes to grow and reach the surface will be compromised at light limited locations, or during prolonged low light events. Our study shows that the consequences of warmer temperatures are greater in conditions of compromised light where greater metabolic demand (Mabin et al., 2019) is not met by sufficient light delivery to the benthos (Tait, 2019).

Unlike other studies (e.g., Snyder et al., 2020), we show poor correlation between SST and nitrogen concentration. There was, however, good agreement between in situ measurements of total nitrogen and chl-a concentration for sites covering much of the study region. We attribute this lack of alignment between this study and other research (Snyder et al., 2020) to the high riverine influence along the southern New Zealand coast and large-scale land-use changes (Schiel and Howard-Williams, 2016; Stevens et al., 2021) and the coastal focus of this study. While the chl-a concentration (Pinkerton et al., 2018) and water clarity algorithms used in this study have been developed to better account for the often turbid waters of southern New Zealand, these case-2 coastal waters present challenges for determining metrics of both light availability (K_d) and phytoplankton biomass. However, the utility of remote sensing to retrospectively assess the effects of multiple physical and biotic parameters on kelp beds has great utility to better understand the interaction between local and global scale stressors.

Studies in Central and Southern California have shown highly correlated occurrences of low nitrogen and high temperature (Snyder et al., 2020), while we show some correlation between chl-a (as a reasonable proxy for nutrient availability) and temperature, but not K_d and temperature, suggesting that MHW events in New Zealand possibly influence nutrient limitation but not water clarity. There was, however, little indication that nitrogen levels frequently fall below thresholds for nutrient limitation of Macrocystis (Dean and Jacobsen, 1986). Laboratory based assessments of multiple photo-physiological metrics across individual stressor variables (temperature, light availability, and nitrogen availability) clearly show negative impacts of warm temperatures, low light availability, and low nutrient concentrations (Mabin et al., 2019). However, the growth of juvenile sporophytes was not affected greatly by nitrogen concentrations (Mabin et al., 2019). Specific combinations of conditions experienced by real-world populations can significantly affect the outcomes to macroalgae. For example, nutrient history prior to heat-wave events has significant bearing on the outcomes for Macrocystis populations (Fernández et al., 2021), suggesting that the timing and length of heat-wave events or conditions of limited nutrients have significant effects on kelp bed persistence. Our results indicate that chl-a is a reasonable proxy for total nitrogen concentrations, but we present little evidence of major declines in Macrocystis associated with periods of low chl-a (as detected remotely). Despite the fundamental relationship between warm temperatures and low nutrient concentrations (Snyder et al., 2020), the combined evidence of this study and others (Cavanaugh et al., 2019; Butler et al., 2020) is that these kelp forests are highly susceptible to MHWs. We show that reductions in water clarity present a major challenge to the resilience of Macrocystis at elevated temperatures. Few studies have used remotely sensed metrics of water clarity to assess the consequences to remotely sensed kelp beds over large spatial scales, and our research presents compelling evidence that regions of low water clarity increase the susceptibility of kelp beds to heat waves.

The use of satellite remote monitoring for tracking populations of Macrocystis is limited to detecting the surface canopies as populations at the benthos cannot be sighted but nevertheless enables kelp forest health and abundance to be monitored remotely over large areas. There is, however, a lag between environmental change and Macrocystis response, so that legacy effects of significant oceanographic and climatic events require further evidence to quantitatively tie-down the independent effects of multiple variables. For example, numerous studies point to the key role of significant wave height in affecting kelp bed dynamics (Cavanaugh et al., 2011; Reed et al., 2011; Bell et al., 2015; Castorani et al., 2018). Synthesis of long-term observations using satellite remote sensing revealed that recovery of Macrocystis canopies following winter storms was highly correlated to spring sea surface temperatures (SST) (Cavanaugh et al., 2011). Remote tracking of Macrocystis populations has enabled analyses of broad scale processes relating to oceanographic trends (Cavanaugh et al., 2011; Hamilton et al., 2020), and these methods have equal promise for better understanding the point-source and diffuse influences of land-use changes.

New Zealand has experienced some of the most intense marine heat waves on record in the past 5 years (Salinger et al., 2019, 2020) causing localized losses of southern bull kelp (Thomsen et al., 2019). Rapid rates of land-use change associated with agriculture and urbanization have greatly altered the land-water interface globally, including in New Zealand, where rates of sedimentation have also increased (Goff, 1997). The proximity of Macrocystis forests in the nearshore zone to sources of sediments greatly affects the demography of populations of large brown algae that are the facilitators of diversity and energy flow in nearshore waters. Sediments may prevent attachment of algal propagules to benthic surfaces (Taylor and Schiel, 2003: Schiel et al., 2006), smother those that have settled (Schiel and Gunn, 2019), and result in a poor conversion from juvenile Macrocystis sporophytes to adult plants reaching the surface (Tait, 2019). The consequences of poor land-management and high levels of sediment runoff must urgently be addressed in the face of increasing occurrences of MHWs (Schiel and Howard-Williams, 2016).

Declines in Macrocystis have been ascribed to anomalous warm events, but other mechanisms for kelp loss include altered trophic interactions and destructive grazing by urchins (Ling et al., 2009; Rogers-Bennett and Catton, 2019; Butler et al., 2020) and nutrient limitation (Dean and Jacobsen, 1986; Hernandez-Carmona et al., 2001; Edwards and Hernandez-Carmona, 2005; McPherson et al., 2021). Many regions, however, such as southern New Zealand, have relatively few instances of overgrazing by urchins (Schiel and Foster, 2015). At this stage, it is unknown how many other regions are experiencing consequences of anthropogenically altered sediment regimes on the abundance and distribution of kelp forests. This is likely to be exacerbated with global warming, as increasing loss of glaciers (Smith et al., 1999) threatens to increase transport of terrigenous sediments to the oceans. In temperate regions where coastal marine ecosystems meet managed terrestrial environments, appropriate interventions to reduce the rate of terrigenous sediment inputs may greatly improve outcomes for giant kelp forests and enhance their resilience to threats associated with MHWs and other global or regional stressors. Failure to act in supporting temperate kelp forest ecosystems has major implications to the operation of global carbon sink pathways (Filbee-Dexterand Wernberg, 2020), and overall ecosystem stability.

The datasets presented in this study can be found in online repositories (https://www.researchgate.net/publication/353677624_Kelp_cover_2021_3). The script repository can be found below: https://code.earthengine.google.com/?accept_repo=users/leightait/shared.

LT conceived the research, prepared and analyzed data, and drafted the manuscript. FT and MP prepared and analyzed data and to the draft manuscript. MT and DS contributed to the research concept and to writing the manuscript. All authors contributed to the article and approved the submitted version.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.