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Article

Immediate Impact of the 2021 Harmful Algal Bloom in Southeast Hokkaido on the Rocky Intertidal Benthic Community and Its Spatial Variation

by
Yuan Yao
1,* and
Takashi Noda
2
1
Graduate School of Environmental Science, Hokkaido University, N10W5, Kita-ku, Sapporo 060-0810, Hokkaido, Japan
2
Faculty of Environmental Earth Science, Hokkaido University, N10W5, Kita-ku, Sapporo 060-0810, Hokkaido, Japan
*
Author to whom correspondence should be addressed.
J. Mar. Sci. Eng. 2024, 12(6), 928; https://doi.org/10.3390/jmse12060928
Submission received: 2 May 2024 / Revised: 26 May 2024 / Accepted: 30 May 2024 / Published: 31 May 2024
(This article belongs to the Special Issue Benthic Ecology in Coastal and Brackish Systems)
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Abstract

:
There has been a limited number of studies on the effects of harmful algal blooms (HABs) on natural rocky intertidal ecosystems. From mid-September to early November 2021, an unprecedented HAB caused by Karenia selliformis hit the Pacific coast of southeast Hokkaido, Japan, for the first time, causing massive mortalities among marine organisms. To clarify the immediate impacts of the HAB on the abundance of 10 rocky intertidal species in four functional groups (macroalgae, sessile invertebrates, molluscan grazers, and molluscan carnivores), we focused on two questions: (1) How did the HAB affect the abundance of each species differently at the regional scale? and (2) How did the impacts of the HAB on the abundance of each functional groups vary spatially, and was the spatial variation of the HAB impacts related to the spatial distribution of the cell density of HAB species? To study these issues, we compared census data for 17 years before the HAB and within one month after it for five shores on the southeast coast of Hokkaido. The results showed that two macroalgae species and all three molluscan grazer species declined significantly after the HAB. Moreover, the decrease in molluscan grazers was significantly correlated with cell density. These results suggest that the impacts of the HAB in southeast Hokkaido on the abundance of rocky intertidal organisms are highly variable depending on species and locality, presumably because of differences in species-specific tolerances to HAB toxins and the spatial variation in the density of the HAB organisms.

1. Introduction

Harmful algal blooms (HABs) are known as pernicious disturbance events for aquatic organisms and coastal ecosystems, and they cause substantial ecological alteration and financial losses. HABs have caused a large negative economic impact [1,2,3], but there are few studies on the impacts of HABs on natural ecosystems. Knowledge of the ecological consequences of HABs could provide us with important implications for predicting and containing the economic impacts of HABs because many of the large negative economic impacts caused by HABs are thought to alter the structure and function of marine ecosystems, and result in a decline in ecosystem services [4]. Many previous studies focused on the negative impacts of HABs on commercial species and explored the influence of HABs on the abundance, survival, and physical condition [5,6], and the underlying mechanisms behind these negative influences [7,8,9]. In contrast, there are only a limited number of studies examining the ecological consequences of HABs [10,11,12].
To understand the ecological consequences of HABs in coastal ecosystems, a fundamental and crucial task is to elucidate the immediate impact of HABs on the population sizes of multiple species at multiple localities at a regional scale because understanding this impact should improve our understanding of how HABs directly affect the community. The immediate impacts often do not include indirect effects on population dynamics triggered by species interactions. In addition, most coastal organisms form meta-populations consisting of many local populations in which every population experiences a locally variable environment [13]. Therefore, the knowledge about the immediate impacts from direct effects of HABs and the long-term impacts caused by subsequent species interactions can be inferred by following changes in the abundance of every species at multiple localities in a region.
From mid-September to early November 2021, there was an unprecedented large-scale HAB with a dinoflagellate Karenia selliformis as the main species in the coastal waters off the southeast coast of Hokkaido, Japan [14,15]. This was the first time such a severe HAB had been recorded in this area [16]. Because this HAB caused serious fishery losses, as exemplified by those of sea urchins living in the intertidal and subtidal zone (more than 17 billion JPY), it might have also affected various organisms living in rocky intertidal habitats along southeast Hokkaido. Previous studies of the impacts of HABs on rocky intertidal communities indicate that mobile consumers, such as sea urchins and starfish, are susceptible to the gymnodimines and various fatty acid ester metabolites produced by K. selliformis [5,17]. However, sessile invertebrates, such as mussels and oysters, are resilient [18,19], because these species are not found to accumulate the gymnodimines and fatty acid esters [20]. Although these studies explored the toxic mechanisms of K. selliformis on organisms, none of these studies used long-term census data to elucidate the immediate impact of HABs on population sizes of multiple species from different functional groups at multiple sites at a regional scale. The toxins produced by K. selliformis depend on phylotypes. Within the K. selliformis clade, there are at least two different phylotypes with clear phenotypic differences [20], and different phylotypes of K. selliformis have different metabolites, including gymnodimines [5,20], long-chain polyunsaturated fatty acids [17], and other as-yet uncharacterized highly toxic compounds [17]. However, although some studies described that gymnodimines produced by K. selliformis have a lethal effect on sea urchin and starfish [5], the fact that K. selliformis does not produce gymnodimines was also described [17].
Despite the fact that there is still no study focus on the toxins produced by K. selliformis in this HAB event, K. selliformis may cause massive mortality in macroalgae and mollusks. The latest study of the same HAB event in southeast Hokkaido reported that K. selliformis has a lethal effect on juvenile kelp (Saccharina japonica and S. sculpera) caused by bleaching juvenile kelp thalli and the subsequent cell death [21]. This finding implies that K. selliformis may have a lethal effect on other macroalgae living in rocky intertidal habitats. Moreover, previous studies demonstrated that K. selliformis have a lethal effect on many mollusks, including limpets and snails [22], which are the dominant mollusks in rocky intertidal communities. Furthermore, a study of the same HAB event also observed intensive mortalities of limpets and whelks immediately after the HAB occurrence [23]. Although none of the above-mentioned studies fully explained the specific toxicological mechanism of K. selliformis on these species, it is reasonable to conclude that K. selliformis caused these massive mortalities. Because the functional groups of organisms mentioned in previous studies (i.e., macroalgae [kelp], molluscan grazers [limpets], and molluscan carnivores [snails]) are dominant in rocky intertidal communities in southeast Hokkaido, assessing the immediate changes in their abundance after this large HAB could provide important information for exploring subsequent changes in species interactions and population dynamics.
The purpose of this study was to clarify the immediate impacts of the 2021 HAB in southeast Hokkaido on different functional groups including macroalgae (i.e., primary producers), molluscan grazers (i.e., primary consumers), molluscan carnivores (i.e., secondary consumers), and sessile invertebrates (i.e., competitors with macroalgae for space) in rocky intertidal communities, focusing especially on any changes in population size among different species, functional groups, and localities. For this purpose, the following questions about the immediate impacts of the HAB at the population level were addressed: (1) How did the HAB affect the population size of each species at a regional scale and were there differences among functional groups? and (2) How did the impacts of the HAB on the abundance of each functional group vary depending on shore, and were spatial variations of the HAB impacts related to the spatial distribution of cell density of HAB species? To answer these questions, long-term census data from southeast Hokkaido for 17 years before the HAB (from 2004 to 2020) and sample data from within one month after the HAB were analyzed. These large-scale long-term monitoring census data could be used to estimate the differences in population size before and after the HAB occurrence for every species at each location [24,25].

2. Material and Methods

2.1. Study Area

Our study sites were located along over 50 km of shoreline on the Pacific coast of eastern Hokkaido (Figure 1), within the range of the HAB in September 2021. At these study sites, there are various rocky intertidal organisms, including macroalgae, sessile invertebrates (such as barnacles), molluscan grazers, and molluscan carnivores [26]. These species are distributed in the mid-tidal zone within a vertical range of tens of centimeters. The horizontal extent of our study sites (more than 50 km) exceeds the specific distance of genetic dispersal scale for macroalgae (<4.2 km) and littorina (23 km), which indicates that our sample range should have covered the entire range of the metapopulation of most macroalgae and benthic mollusks [27].

2.2. Census Design

Prior to the 2021 HAB, sampling following a hierarchical design (Noda, 2004) was conducted at five shores on the Pacific coast of southeast Hokkaido (Mochirippu [MC]: 43°01′02″ N, 145°01′30″ E; Mabiro [MB]: 42°59′14″ N, 144°53′24″ E; Aikappu [AP]: 43°01′02″ N, 144°50′02″ E; Monshizu [MZ]: 43°02′59″ N, 144°46′42″ E; and Nikomanai [NN]: 42°56′23″ N, 144°40′26″ E) (Figure 1) beginning in 2004. At each shore, 5 permanent plots 50 cm wide by 100 cm high were set up on nearly vertical rocks (25 plots in total), with the vertical midpoints corresponding to the mean tidal level. The distance between neighboring plots ranged from 6.6 to 113 m (mean ± SD, 34.1 m ± 27.8 m). Each plot was evenly divided vertically into 10 quadrats (50 cm wide by 10 cm high). For all censuses, the number of individuals of each mobile species (i.e., molluscan grazers and molluscan carnivores) was obtained for each plot (Figure 1). In addition, the coverage of each sessile species (i.e., macroalgae and sessile invertebrates) was estimated by using a point-sampling method in which each quadrat in a plot was divided into 20 fixed observation points with 2 horizontal rows and 10 vertical columns. The interval between each point was 5 cm both vertically and horizontally. The dominant species occupying each fixed observation point was recorded. Therefore, the coverage of each species was the number of recorded points per 25 cm2, and the coverage was used as the abundance of sessile species. The abundance of rocky intertidal organisms in permanent plots were determined annually at low tide in late October or early November. In November 2021, within 1 month after the HAB off the Pacific coast of eastern Hokkaido, the same census was performed at these sites to assess the immediate impact of the HAB.

2.3. Species Selection

To avoid inaccurate assessment of the effect of the HAB on population size, only the species at the regional scale and functional groups at the shore scale that were relatively abundant and observed continuously were selected as the subject species. For sessile species, a threshold of coverage was set as 5 points at the regional scale in each year, and, for mobile species, the threshold was 5 individuals. According to past census data in this area, the sessile invertebrate Chthamalus dalli; macroalgae Corallina pilulifera, Chondrus yendoi, Gloiopeltis furcata, Heterochordaria abietina, and Polysiphonia yendoi; molluscan grazers Littorina sitkana, Lottia cassis, and Lottia sp. (a species of limpet occurring in the area that has not been determined to the date [28]); and the molluscan carnivore Nucella lima meet the threshold values at the regional scale. In addition, the abundance of each functional group was recorded as the total abundance of all species within that functional group at the shore scale. To ensure the accuracy of the assessment, we excluded functional groups that have not been observed for two or more consecutive years. According to past census data in this area, sessile invertebrates, macroalgae, and molluscan grazers meet these threshold values at the shore scale.

2.4. Calculation of Cell Density of HAB Species

The cell density of HAB species was derived by using the surface chlorophyll-a concentrations reported by Kuroda et al. [15], who measured chlorophyll-a concentration along a ship track (during 4–14 October 2021) in their study of the same HAB event. They presented chlorophyll-a concentration values in a census map as colored grid cell (Figure S1A in Supplementary Materials). In addition, they provided a log-log regression equation of Karenia spp. abundance versus chlorophyll-a concentration (R2 = 0.75; Figure 7 in [15]):
Karenia log abundance = 2.032 × Chlorophyll-a concentration + 0.135
In the present study, we selected the colored grid cell perpendicular to the coastline of each shore as chlorophyll-a concentration data, and calculated the cell density of Karenia spp. by the above regression equation (Figure S1B in Supplementary Materials). The detail of data extraction and code execution are shown in Supplementary Materials.

2.5. Statistical Analysis

To evaluate the effects of HAB on each species (i) at the regional scale (ESREGION,i), each functional group (j) at each region (ESREGION,j), and each functional group (j) at each shore (k) (ESSHORE,j,k), we calculated the effect sizes (ESs) of the abundance (A) from the pre-HAB period (2004–2020) to the post-HAB period (2021) with the following formulae [24,25,29,30,31]:
E S R E G I O N , i = l o g ( A R E G I O N , i , p o s t − H A B ) − l o g ( A ¯ R E G I O N , i , p r e − H A B ) S D l o g ( A R E G I O N , i , p r e − H A B )
E S R E G I O N , j = l o g ( A R E G I O N , j , p o s t − H A B ) − l o g ( A ¯ R E G I O N , j , p r e − H A B ) S D l o g ( A R E G I O N , j , p r e − H A B )
E S S H O R E , j , k = l o g ( A S H O R E , j , k , p o s t − H A B + 0.5 ) − l o g ( A ¯ S H O R E , j , k , p r e − H A B + 0.5 ) S D l o g ( A S H O R E , j , k , p r e − H A B + 0.5 )
where l o g ( A R E G I O N , i , p o s t − H A B ) represents the log10(abundance) of each species in the post-HAB year, and l o g ⁡ ( A ¯ R E G I O N , i , p r e − H A B ) and S D l o g ( A R E G I O N , i , p r e − H A B ) represent the mean and standard deviation of the log10(abundance) of each species during the pre-HAB period, respectively; l o g ( A R E G I O N , j , p o s t − H A B ) represents the log10(abundance) of each functional group in the post-HAB year, and l o g ⁡ ( A ¯ R E G I O N , j , p r e − H A B ) and S D l o g ( A R E G I O N , j , p r e − H A B ) represent the mean and standard deviation of the log10(abundance) of each functional group during the pre-HAB period, respectively; l o g ( A S H O R E , j , k , p o s t − H A B + 0.5 ) represents the log10(abundance + 0.5) of each functional group at each shore in the post-HAB year, and l o g ( A ¯ S H O R E , j , k , p r e − H A B + 0.5 ) and S D l o g ( A S H O R E , j , k , p r e − H A B + 0.5 ) represent the mean and standard deviation of log10(abundance + 0.5) of each functional group at each shore during the pre-HAB period, respectively.
To evaluate the biological response of each species (i) and functional group (j) on HAB event, we calculated the relative change (RC) of abundance (A) from the pre-HAB period (2004–2020) to the post-HAB period (2021) with the following formulae [32]:
R C R E G I O N , i = A R E G I O N , i , p o s t − H A B − A ¯ R E G I O N , i , p r e − H A B A R E G I O N , i , p r e − H A B × 100 %
R C R E G I O N , j = A R E G I O N , j , p o s t − H A B − A ¯ R E G I O N , j , p r e − H A B A R E G I O N , j , p r e − H A B × 100 %
R C S H O R E , j , k = A S H O R E , j , k , p o s t − H A B − A ¯ S H O R E , j , k , p r e − H A B A S H O R E , j , k , p r e − H A B × 100 %
where A ¯ R E G I O N , i , p r e − H A B represents the mean abundance of each species during the pre-HAB years at region scale, and A R E G I O N , i , p o s t − H A B represents the abundance of each species in the post-HAB year at region scale; A ¯ R E G I O N , i , p r e − H A B represents the mean abundance of each species during the pre-HAB years at region scale, and A R E G I O N , j , p o s t − H A B represents the abundance of each functional group in the post-HAB year at region scale; A ¯ S H O R E , j , p r e − H A B represents the mean abundance of each functional group during the pre-HAB years at shore scale, and A R E G I O N , i , p o s t − H A B represents the abundance of each species in the post-HAB year at shore scale.
We used Cohen’s standardized measure of difference to assess the significance of effect size. An effect size greater than 1.96 in absolute value suggests that the abundance in the post-HAB year changed significantly compared with the pre-HAB period [33,34]. This threshold of 1.96 corresponds to a two-tailed significance level of p < 0.05, commonly used in hypothesis testing. It is derived from the standard normal distribution and serves as a critical value for determining statistical significance.
These effect size approaches provide an accurate assessment of the immediate impact of the HAB because the effects of environmental stochasticity other than HAB are reduced in two ways: (1) the reference state abundance (abundance when not affected by the HAB) in this study is determined as a multi-year average, so the effect of environmental stochasticity other than the HAB on the change in abundance before and after HAB is small, and (2) the effect of HAB on abundance is assessed as the relative magnitude of the change in abundance before and after the HAB to the magnitude of the temporal variation of abundance in a normal year.
To evaluate whether spatial variations of the HAB impacts are related to the spatial distribution of cell density of HAB species, we employed scatter diagrams and a linear modelling to detect the relationship between E S S H O R E and cell density of HAB species. For each functional group, we used E S S H O R E as the dependent variable, and the cell density of Karenia spp. at each shore as the independent variable. All statistical analyses were conducted in R v. 4.3.1 [35].

3. Results

3.1. Effect of HAB on Population Sizes of Different Species and Functional Groups

Overall, the changes in population size of different species after HAB depend on species (Figure 2A), and the effect size at the regional scale had both positive and negative values (Figure 3, Table 1). Associations between the HAB and macroalgae varied by species, and the effect size of G. furcata and P. yendoi were less than −1.96, representing that these two species decreased significantly (Figure 3, Table 1). And the relative change of G. furcata and P. yendoi was −43.70% and −70.84%, respectively (Table 1). However, the effect size of Littorina sitkana, Lottia cassis, and Lottia sp. was −2.53, −2.15, and −5.99, indicating that all three species of molluscan grazers decreased significantly (Figure 3, Table 1). And the relative change of Littorina sitkana, Lottia cassis, and Lottia sp. was −56.25%, −78.44%, and −85.99%, respectively (Table 1). In addition, the effect sizes of Chthamalus dalli, Nucella lima, and other macroalgae species were between −1.96 and 1.96, indicating that they were not significantly affected by the HAB.
With regard to the effect size of functional groups at the regional scale, the absolute value of the effect size of the macroalgae, sessile invertebrate, and molluscan carnivore was less than 1.96, indicating that they were not significantly affected by the HAB at the regional scale (Figure 2B and Figure 4, Table 2). The effect size of the molluscan grazer was −2.77, indicating that the molluscan grazer decreased significantly at the regional scale. And the relative change of molluscan grazer at regional scale was −58.13% (Table 2). In terms of functional groups at the shore scale, the effect size of sessile animals and macroalgae had both positive and negative values among the shores. The absolute value of the effect size of these two functional groups were less than 1.96, indicating that they were not significantly affected by the HAB at the shore scale (Figure 4, Table 2). However, the effect sizes of molluscan grazers were all negative. The effect size of molluscan grazers at Aikappu, Mabiro, and Nikomanai was −2.187, −2.739, and −11.267, respectively, indicating that the molluscan grazer at these three shores was significantly affected by the HAB at the shore scale (Figure 4, Table 2). In addition, the relative change of the molluscan grazer at Aikappu, Mabiro, and Nikomanai was −55.44%, −67.80%, and −97.75%, respectively (Table 2).

3.2. The Relationship between Effect Size and Cell Density of Karenia spp.

The response of the effect size to the cell density of Karenia spp. varied among functional groups (Figure 5). Only the effect size of the molluscan grazer was significantly negatively correlated with cell density (p < 0.01, Figure 5). In addition, macroalgae and sessile invertebrates showed a low sensitivity to cell density (Figure 5), and no significant relationships between effect size and cell density of Karenia spp. were found in the linear modeling (p > 0.05, Figure 5).

4. Discussion

In this study, the immediate impact of the 2021 HAB in southeast Hokkaido on the population sizes of 10 common species and the abundance of three functional groups in a rocky intertidal community was examined. Census data from 17 years before the HAB and within one month following the HAB were examined for 25 rocks at five shores along the coastline of southeast Hokkaido, Japan. Our results showed that two of five macroalgae species and all three molluscan grazer species significantly declined at the regional scale after the HAB occurred. In addition, only molluscan grazers declined significantly at three shores after the HAB. Furthermore, the effect size of molluscan grazers at the shore scale was significantly negatively correlated with the cell density of Karenia spp.
While various year-to-year environmental fluctuations may drive community dynamics in rocky intertidal assemblages [31,36,37], their influences on the results of this study should be small. From October 2020 to October 2021, there was no other disturbance that would cause massive mortality (e.g., earthquake, tsunami, typhoon, ice scouring, marine heatwave, etc.) on the Pacific coast of southeast Hokkaido other than the HAB. Furthermore, other environmental factors that determine the population dynamics of rocky intertidal species, such as air temperature, sea water temperature, coastal topographic properties, and microtopography of rock surfaces, were stable during that period. In addition, the E S S H O R E of other functional groups (macroalgae and sessile invertebrates) that were not affected by the HAB did not show any obvious consistent spatial patterns or significant variation, which was another evidence that the effects of environmental fluctuations on community dynamics were weak.
Three molluscan grazers (Littorina sitkana, Lottia cassis, and Lottia sp.) and two macroalgae (Gloiopeltis furcata and Polysiphonia yendoi) significantly declined in abundance at the regional scale, but other macroalgae species and the sessile invertebrate and molluscan carnivore were unaffected. This difference can presumably be explained by differences in the species-specific tolerance to biological toxins produced by K. selliformis, which is generally thought to produce gymnodimines and cause mass mortalities in a wide range of marine life [20], although there currently is no unified explanation for the mechanism of the lethal effect of K. selliformis on a wide range of marine organisms. A non-gymnodimine-producing phylotype of K. selliformis that causes massive fauna mortality by producing large amounts of long-chain polyunsaturated fatty acids and/or as-yet uncharacterized highly toxic compounds has also been reported [17]. Previous studies demonstrated that damage from K. selliformis differs among taxonomic groups. For example, K. selliformis has been shown to have a lethal effect on many mollusks, including octopus, limpets, and snails [22], as well as lethal effects on two juvenile kelp sporophytes Saccharina japonica and S. sculpera [21]. However, there are no reported negative effects of K. selliformis on barnacles. In addition, massive kills of fish [38,39] and shellfish [40,41] caused by K. selliformis have been reported around the world, but some bivalves that feed on K. selliformis can survive when it is present, and gymnodimines can be found accumulated in their tissues [40,42]. Furthermore, there are no reported negative effects of K. selliformis on macroalgae. The reason for these differences may be that different species have different tolerances for the biological toxins produced by HAB species.
Many studies of the toxicity of other HAB-causing species also showed that fish, shellfish, and invertebrates have different tolerances to species, such as Karenia brevis [43] and Karenia mikimotoi [44]. Compared to the impacts of the HAB along the west coast of South Africa [12] and other disturbances with a similar geographical scale such as oil spills [45,46,47], earthquakes [25], nuclear disaster [48], and ice scouring [49] that have caused massive mortality on most species in rocky intertidal communities, the HAB in southeast Hokkaido had more obvious species-specific impacts that reduced the abundance of molluscan grazers and some macroalgae species. In addition, fisheries’ damage from the HAB was high for sea urchins, but oysters, scallops, and crabs were less affected [20,41]. These observations indicate that such strong species-specific impacts are a unique feature of the consequences of the 2021 Hokkaido HAB dominated by K. selliformis.
The significant decline in G. furcata and P. yendoi at the regional scale did not manifest at the functional group level at the shore scale. The response of macroalgae to the HAB was not uniform at the species level, and some other species that were not included in the analysis at the species level on the regional scale may increase after the HAB occurred (Figure 3), which may offset the decline in G. furcata and P. yendoi on the functional group level at the shore scale caused by the HAB. In addition, the scale transition theory provides a systematic framework to explain the problem of scaling up local-scale interactions to regional-scale dynamics with field data [50,51]. When evaluating the population dynamics of the same species at different spatial scales, the predictions of dynamics at different scales diverge due to the interaction between the nonlinearity in the population dynamics at the local scale and the spatial heterogeneity in the abundance and environmental factors that influence population dynamics (i.e., the intensity of the HAB in this study) at the regional scale [51,52]. Therefore, the inconsistency of the significance of the HAB on effect size at different scales may be a result of the uneven distribution of the abundance of these two species at the regional scale and the spatial heterogeneity of environmental factors that influence population dynamics. Consequently, the increase in other macroalgae species and the scale transition theory are not mutually exclusive and may operate simultaneously.
The spatial variation of the HAB impact in this study can be explained by the spatial pattern of the K. selliformis cell density in offshore waters. Similarly, for an HAB along the coast of South Africa, the mortalities of several intertidal species were higher where the HAB intensity was stronger [12]. In general, the severity of the impact from a disturbance (e.g., the resulting degree of population decline) is likely to depend primarily on the intensity of the disturbance (i.e., strength of forcing) [24]. Indeed, severity–intensity relationships within a single disturbance event have been documented in rocky intertidal organisms for various disturbance events occurring at scales from several to several tens of kilometers. For oil spills, the mortality of rocky intertidal organisms varies locally depending on the levels of oil pollution [45,46,47]. For the Fukushima nuclear disaster, the abundance of surviving organisms decreased significantly with decreasing distance from the nuclear power plant [48]. For ice scarring, habitats that freeze for longer periods of time lose more biomass of sessile species in rocky intertidal habitat [49].
The spatial variation of the impact of the HAB on the abundance of molluscan grazers in this study can be explained by the spatial pattern of K. selliformis cell density in offshore waters. Although the toxicological mechanisms of K. selliformis have not yet been clarified, this association between cell density and the decrease in functional group abundance indicated that a high concentration of toxins in the HAB caused the local mass mortality of molluscan grazers. For other dinoflagellates, previous studies indicated that the cell density of toxin-producing algae is always associated with the survival, mortality, or growth rate of molluscan species through various toxicological mechanisms [53]. For example, the survival rate of the abalone Haliotis discus significantly decreased with the increasing cell density of Alexandrium pacificum under a cultured condition [54]. This decline in survival rate may be caused by various toxicological mechanisms documented in bivalves, such as increased oxygen consumption, increased ammonia and phosphate excretion, and decreased Na+-K+ ATPase activity [53].
After the HAB in 2021, the abundance of molluscan grazers suddenly decreased at the shore scale, while the abundance of macroalgae and sessile animals remained unchanged. The loss of molluscan grazers could subsequently affect community dynamics through the trophic cascade [55,56]. The decline in abundance of molluscan grazers will result in an increase in their food resource—macroalgae—and further decreases in the abundance of competitors of macroalgae, i.e., sessile invertebrates (e.g., barnacles) [57]. Indeed, the experimental removal of molluscan grazers often results in increased macroalgae and decreased sessile invertebrates in rocky intertidal habitats [58,59,60].
Among the three molluscan grazers that suffered heavy HAB-induced population decline, L. cassis and Lottia sp. have a planktonic larval stage, whereas L. sitkana lacks a planktonic larval stage. This difference in life history may cause differences among species in the speed of population recovery at these three shores [61]. For species capable of larval dispersal, population recovery at Aikappu, Mabiro, and Nikomanai should benefit from larvae supplied from undamaged populations near each shore. On the other hand, the population recovery of non-planktonic species would completely depend on local reproduction. Thus, the speed of recovery at shores where molluscan grazers have significantly declined may be faster for populations of L. cassis and Lottia sp. than for L. sitkana.

5. Conclusions

In this study, long-term census data from five shores were used to evaluate the impacts of the 2021 HAB in southeast Hokkaido on the rocky intertidal community. Only two of five macroalgae species, G. furcata and P. yendoi, and three molluscan grazer species, L. sitkana, L. cassis, and Lottia sp., had significant population declines at the regional scale. At the functional group level at the shore scale, molluscan grazers declined significantly at three of the five shores. In addition, the effect size of molluscan grazers was significantly negatively correlated with the cell density of Karenia spp. These results imply that the effects of this HAB were highly species-specific and related to the density of the HAB-causing species in offshore waters. Because the toxicity of K. selliformis is still unclear, the mechanisms of species-specific and spatial variations of the HAB effects cannot be explained.
After the sudden loss of grazer species, the increasing coverage of macroalgae and decreasing coverage of sessile animals resulting from the trophic cascade are predicted. Because of differences in the larval dispersal ability, population recovery is expected to be faster in grazer species with planktotrophic larvae than in species with direct development.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/jmse12060928/s1, Figure S1. (A) Surface chlorophyll-a concentrations (colored grid cells) along the ship track during 4–14 October 2021 conducted by Kuroda et al. [15] Grid cells show averages across 45″ (longitude) × 30″ (latitude) (i.e., an approximately 1 × 1 km rectangle). Karenia spp. abundance at a depth of 10 m is also shown by the area of red circles. We added five black hollow circles in original figure to indicate the census shore in present study. And we added the black solid lines perpendicular to the shoreline of census shores to represent the colored grid cells that used to calculate the cell density of Karenia spp. in present study. (B) The enlarged view of the color grid cells, and the chlorophyll-a concentration calculated by RGB color value. Figure S2. The reconstructed legend color space according to Figure 4 in Kuroda et al. (2022) [15]. The reconstructed approach was shown in the code execution below.

Author Contributions

Conceptualization, Y.Y. and T.N.; data curation, Y.Y.; formal analysis, Y.Y.; investigation, Y.Y. and T.N.; supervision, T.N.; visualization, Y.Y.; writing—original draft, Y.Y.; writing—review and editing, T.N. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by grants-in-aid from the Japan Society for the Promotion of Science to T.N. (nos. 20570012, 24570012, 15K07208, 18H02503, and 23H02546).

Data Availability Statement

The data presented in this study are available upon request from the corresponding author. The data are not publicly available because this dataset may be included as part of other ongoing studies.

Acknowledgments

We are grateful to all the researchers and students who helped with the field data collection, without which our study would not have been possible. This study received generous support and encouragement from local fishermen and the fisheries office of the Fisherman’s Cooperative Association in Akkeshi.

Conflicts of Interest

The authors declare no conflicts of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of the data; in the writing of the manuscript; or in the decision to publish the results.

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Jmse 12 00928 g001
Figure 1. Diagram of study site locations and census design. Five shores were chosen along the Pacific coast of eastern Hokkaido, Japan. At each shore, five permanent plots (50 cm wide by 100 cm high) were set up on nearly vertical rocks (25 rocks in total), with the vertical midpoints corresponding to the mean tidal level. Each plot was evenly divided vertically into 10 quadrats (50 cm wide by 10 cm high). The white circles in the quadrat diagram represent fixed observation points.
Figure 1. Diagram of study site locations and census design. Five shores were chosen along the Pacific coast of eastern Hokkaido, Japan. At each shore, five permanent plots (50 cm wide by 100 cm high) were set up on nearly vertical rocks (25 rocks in total), with the vertical midpoints corresponding to the mean tidal level. Each plot was evenly divided vertically into 10 quadrats (50 cm wide by 10 cm high). The white circles in the quadrat diagram represent fixed observation points.
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Figure 2. The log10(abundance) before and after the HAB event for each species at regional scale (A) and for each functional group at shore scale (B). The color represents the functional group. The circle with error bar represents the mean and standard error of log10(abundance) in pre-HAB period (one sample for each species (A) or each functional group at each shore (B) are collected from 2004 to 2020 annually, with a total of 17 years). The square represents the log10(abundance) in the post-HAB period (one sample for each species (A) or each functional group at each shore (B) are collected in 2021).
Figure 2. The log10(abundance) before and after the HAB event for each species at regional scale (A) and for each functional group at shore scale (B). The color represents the functional group. The circle with error bar represents the mean and standard error of log10(abundance) in pre-HAB period (one sample for each species (A) or each functional group at each shore (B) are collected from 2004 to 2020 annually, with a total of 17 years). The square represents the log10(abundance) in the post-HAB period (one sample for each species (A) or each functional group at each shore (B) are collected in 2021).
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Figure 3. The effect size of different species at the regional scale. The dashed gray lines from top to bottom represent 1.96, 0, and −1.96, respectively. An effect size of greater than 1.96 in absolute value indicates a statistically significant difference in the population size before and after the HAB. Hollow dots represent insignificant difference, and solid dots represent significant different. The color of dots represents the functional group.
Figure 3. The effect size of different species at the regional scale. The dashed gray lines from top to bottom represent 1.96, 0, and −1.96, respectively. An effect size of greater than 1.96 in absolute value indicates a statistically significant difference in the population size before and after the HAB. Hollow dots represent insignificant difference, and solid dots represent significant different. The color of dots represents the functional group.
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Figure 4. The effect size of different functional groups at the shore scale. The dashed gray lines from top to bottom represent 1.96, 0, and −1.96, respectively. An effect size of greater than 1.96 in absolute value indicates a statistically significant difference in the population size before and after the HAB. Hollow dots represent insignificant difference, and solid dots represent significant different. The color of dots represents the functional group. AP, Aikappu; MB, Mabiro; MC, Mochirippu; MZ, Monshizu; NN, Nikomanai.
Figure 4. The effect size of different functional groups at the shore scale. The dashed gray lines from top to bottom represent 1.96, 0, and −1.96, respectively. An effect size of greater than 1.96 in absolute value indicates a statistically significant difference in the population size before and after the HAB. Hollow dots represent insignificant difference, and solid dots represent significant different. The color of dots represents the functional group. AP, Aikappu; MB, Mabiro; MC, Mochirippu; MZ, Monshizu; NN, Nikomanai.
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Figure 5. The relationship between E S S H O R E of three functional groups (macroalgae, molluscan grazers, and sessile invertebrates) and the cell density of Karenia spp. at each shore. For the regression analyses, the cell density (cells/mL) of Karenia spp. at each shore and  E S S H O R E of each functional group were treated as independent and dependent variables, respectively.
Figure 5. The relationship between E S S H O R E of three functional groups (macroalgae, molluscan grazers, and sessile invertebrates) and the cell density of Karenia spp. at each shore. For the regression analyses, the cell density (cells/mL) of Karenia spp. at each shore and  E S S H O R E of each functional group were treated as independent and dependent variables, respectively.
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Table 1. The effect size and relative change of each species at regional scale. The minus (−) sign is for decrease, and omit any sign for increases. The effect size greater than 1.96 or lower than −1.96 is highlighted in bold with asterisk (*).
Table 1. The effect size and relative change of each species at regional scale. The minus (−) sign is for decrease, and omit any sign for increases. The effect size greater than 1.96 or lower than −1.96 is highlighted in bold with asterisk (*).
Functional GroupSpeciesEffect SizeRelative Change
Sessile invertebrateChthamalus dalli0.8416.87%
MacroalgaeChondrus yendoi−1.77−54.81%
Corallina pilulifera1.3527.03%
Gloiopeltis furcata−2.18 *−43.70%
Heterochordaria abietina1.0021.82%
Polysiphonia yendoi−2.27 *−70.84%
Molluscan grazerLittorina sitkana−2.53 *−56.25%
Lottia cassis−2.15 *−78.44%
Lottia sp.−5.99 *−85.99%
Molluscan carnivoreNucella lima−0.92−78.22%
Table 2. The effect size and relative change of each functional groups at regional scale and shore scale. The minus (−) sign is for decrease, and omit any sign for increases. The effect size greater than 1.96 or lower than −1.96 is highlighted in bold with asterisk (*).
Table 2. The effect size and relative change of each functional groups at regional scale and shore scale. The minus (−) sign is for decrease, and omit any sign for increases. The effect size greater than 1.96 or lower than −1.96 is highlighted in bold with asterisk (*).
ShoreFunctional GroupEffect SizeRelative Change
Region Scale/Macroalgae−0.34−5.59%
/Molluscan grazer−2.733 *−58.13%
/Sessile invertebrate0.841−16.866%
Local ScaleAPMacroalgae−0.505−66.99%
MBMacroalgae0.259−35.44%
MCMacroalgae1.566404.95%
MZMacroalgae−0.851−100.00%
NNMacroalgae1.065185.50%
APMolluscan grazer−2.187 *−55.44%
MBMolluscan grazer−2.739 *−67.80%
MCMolluscan grazer−0.28−22.29%
MZMolluscan grazer−1.378−67.93%
NNMolluscan grazer−11.267 *−97.75%
APSessile invertebrate−0.078−59.93%
MBSessile invertebrate0.82373.84%
MCSessile invertebrate0.365−16.58%
MZSessile invertebrate−0.825−92.85%
NNSessile invertebrate0.339−1.27%
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Yao, Y.; Noda, T. Immediate Impact of the 2021 Harmful Algal Bloom in Southeast Hokkaido on the Rocky Intertidal Benthic Community and Its Spatial Variation. J. Mar. Sci. Eng. 2024, 12, 928. https://doi.org/10.3390/jmse12060928

AMA Style

Yao Y, Noda T. Immediate Impact of the 2021 Harmful Algal Bloom in Southeast Hokkaido on the Rocky Intertidal Benthic Community and Its Spatial Variation. Journal of Marine Science and Engineering. 2024; 12(6):928. https://doi.org/10.3390/jmse12060928

Chicago/Turabian Style

Yao, Yuan, and Takashi Noda. 2024. "Immediate Impact of the 2021 Harmful Algal Bloom in Southeast Hokkaido on the Rocky Intertidal Benthic Community and Its Spatial Variation" Journal of Marine Science and Engineering 12, no. 6: 928. https://doi.org/10.3390/jmse12060928

APA Style

Yao, Y., & Noda, T. (2024). Immediate Impact of the 2021 Harmful Algal Bloom in Southeast Hokkaido on the Rocky Intertidal Benthic Community and Its Spatial Variation. Journal of Marine Science and Engineering, 12(6), 928. https://doi.org/10.3390/jmse12060928

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