The effect of a harmful algal bloom (Karenia selliformis) on the benthic invertebrate community and the sea otter (Enhydra lutris) diet in eastern Hokkaido

The effect of a harmful algal bloom (Karenia selliformis) on the benthic invertebrate community and the sea otter (Enhydra lutris) diet in eastern Hokkaido | bioRxiv /* */ /* */ <!-- <!-- /*! * yepnope1.5.4 * (c) WTFPL, GPLv2 */ (function(a,b,c){function d(a){return"[object Function]"==o.call(a)}function e(a){return"string"==typeof a}function f(){}function g(a){return!a||"loaded"==a||"complete"==a||"uninitialized"==a}function h(){var a=p.shift();q=1,a?a.t?m(function(){("c"==a.t?B.injectCss:B.injectJs)(a.s,0,a.a,a.x,a.e,1)},0):(a(),h()):q=0}function i(a,c,d,e,f,i,j){function k(b){if(!o&&g(l.readyState)&&(u.r=o=1,!q&&h(),l.onload=l.onreadystatechange=null,b)){"img"!=a&&m(function(){t.removeChild(l)},50);for(var d in y[c])y[c].hasOwnProperty(d)&&y[c][d].onload()}}var j=j||B.errorTimeout,l=b.createElement(a),o=0,r=0,u={t:d,s:c,e:f,a:i,x:j};1===y[c]&&(r=1,y[c]=[]),"object"==a?l.data=c:(l.src=c,l.type=a),l.width=l.height="0",l.onerror=l.onload=l.onreadystatechange=function(){k.call(this,r)},p.splice(e,0,u),"img"!=a&&(r||2===y[c]?(t.insertBefore(l,s?null:n),m(k,j)):y[c].push(l))}function j(a,b,c,d,f){return q=0,b=b||"j",e(a)?i("c"==b?v:u,a,b,this.i++,c,d,f):(p.splice(this.i++,0,a),1==p.length&&h()),this}function k(){var a=B;return a.loader={load:j,i:0},a}var l=b.documentElement,m=a.setTimeout,n=b.getElementsByTagName("script")[0],o={}.toString,p=[],q=0,r="MozAppearance"in l.style,s=r&&!!b.createRange().compareNode,t=s?l:n.parentNode,l=a.opera&&"[object Opera]"==o.call(a.opera),l=!!b.attachEvent&&!l,u=r?"object":l?"script":"img",v=l?"script":u,w=Array.isArray||function(a){return"[object Array]"==o.call(a)},x=[],y={},z={timeout:function(a,b){return b.length&&(a.timeout=b[0]),a}},A,B;B=function(a){function b(a){var a=a.split("!"),b=x.length,c=a.pop(),d=a.length,c={url:c,origUrl:c,prefixes:a},e,f,g;for(f=0;f<d;f++)g=a[f].split("="),(e=z[g.shift()])&&(c=e(c,g));for(f=0;f<b;f++)c=x[f](c);return c}function g(a,e,f,g,h){var i=b(a),j=i.autoCallback;i.url.split(".").pop().split("?").shift(),i.bypass||(e&&(e=d(e)?e:e[a]||e[g]||e[a.split("/").pop().split("?")[0]]),i.instead?i.instead(a,e,f,g,h):(y[i.url]?i.noexec=!0:y[i.url]=1,f.load(i.url,i.forceCSS||!i.forceJS&&"css"==i.url.split(".").pop().split("?").shift()?"c":c,i.noexec,i.attrs,i.timeout),(d(e)||d(j))&&f.load(function(){k(),e&&e(i.origUrl,h,g),j&&j(i.origUrl,h,g),y[i.url]=2})))}function h(a,b){function c(a,c){if(a){if(e(a))c||(j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}),g(a,j,b,0,h);else if(Object(a)===a)for(n in m=function(){var b=0,c;for(c in a)a.hasOwnProperty(c)&&b++;return b}(),a)a.hasOwnProperty(n)&&(!c&&!--m&&(d(j)?j=function(){var a=[].slice.call(arguments);k.apply(this,a),l()}:j[n]=function(a){return function(){var b=[].slice.call(arguments);a&&a.apply(this,b),l()}}(k[n])),g(a[n],j,b,n,h))}else!c&&l()}var h=!!a.test,i=a.load||a.both,j=a.callback||f,k=j,l=a.complete||f,m,n;c(h?a.yep:a.nope,!!i),i&&c(i)}var i,j,l=this.yepnope.loader;if(e(a))g(a,0,l,0);else if(w(a))for(i=0;i (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0];var j=d.createElement(s);var dl=l!='dataLayer'?'&l='+l:'';j.src='//www.googletagmanager.com/gtm.js?id='+i+dl;j.type='text/javascript';j.async=true;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-M677548'); Skip to main content Home About Submit ALERTS / RSS Search for this keyword Advanced Search New Results The effect of a harmful algal bloom ( Karenia selliformis ) on the benthic invertebrate community and the sea otter ( Enhydra lutris ) diet in eastern Hokkaido View ORCID Profile Jackson Johnstone , Ippei Suzuki , Natsuki Konno , Kyohei Murayama , Satsuki Ochiai , Randall Davis , View ORCID Profile Yoko Mitani doi: https://doi.org/10.1101/2024.04.23.590716 Jackson Johnstone 1 Hokkaido University, Graduate School of Environmental Science , Hakodate, Hokkaido, Japan Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Jackson Johnstone For correspondence: jackson.johnstone.m5{at}elms.hokudai.ac.jp Ippei Suzuki 2 Akkeshi Marine Station, Field Science Center for Northern Biosphere, Hokkaido University , Aikappu, Akkeshi, Hokkaido, Japan Find this author on Google Scholar Find this author on PubMed Search for this author on this site Natsuki Konno 1 Hokkaido University, Graduate School of Environmental Science , Hakodate, Hokkaido, Japan Find this author on Google Scholar Find this author on PubMed Search for this author on this site Kyohei Murayama 1 Hokkaido University, Graduate School of Environmental Science , Hakodate, Hokkaido, Japan Find this author on Google Scholar Find this author on PubMed Search for this author on this site Satsuki Ochiai 1 Hokkaido University, Graduate School of Environmental Science , Hakodate, Hokkaido, Japan Find this author on Google Scholar Find this author on PubMed Search for this author on this site Randall Davis 3 Texas A&M University at Galveston, Department of Marine Biology , Galveston, Texas, United States Find this author on Google Scholar Find this author on PubMed Search for this author on this site Yoko Mitani 4 Kyoto University, Wildlife Research Center , Kyoto, Kyoto, Japan Find this author on Google Scholar Find this author on PubMed Search for this author on this site ORCID record for Yoko Mitani Abstract Full Text Info/History Metrics Preview PDF Abstract In recent decades, the locally extinct sea otter ( Enhydra lutris lutris ) has been recolonizing the coast of eastern Hokkaido. Their diet includes benthic invertebrates such as bivalves, sea urchins, snails, and chitons. In the fall of 2021, a harmful algal bloom (HAB) of Karenia selliformis occurred across Hokkaido’s northern and eastern coasts, leading to a massive mortality of sea urchins. This dinoflagellate produces a neurotoxin (gymnodimine) implicated in shellfish poisoning. To determine the effect of the HAB on the marine community, we conducted benthic surveys using SCUBA and visually monitored the prey items of the sea otters in the affected area from 2020 to 2023. Following the HAB, we observed an 82% decrease in benthic sea urchin density (number m 2 ), leading to their complete absence from the diet of sea otters. Conversely, bivalve density increased six-fold, accompanied by a nearly two-fold rise in their percentage in the sea otters’ diet. Minimal changes were observed in the density of chitons and snails, with no significant alteration in the sea otters’ diet. Despite these changes, the impact of the HAB on otters’ dietary preferences was temporary, as the percentage of dietary sea urchins began recovering one year later. Sea otters augmented their diet with bivalves to compensate for the reduced availability of sea urchins during the HAB with no apparent effects on the number of sea otters or their health. Our results highlight the adaptability of sea otters to adjust their diet according to prey availability. Introduction Red tides, or harmful algal blooms (HABs), are generated by the proliferation of specific phytoplankton varieties, such as dinoflagellates or diatoms. They result in a reddish or brownish tint to the water and produce toxins that can lead to extensive mortality among marine organisms, including fish and shellfish. Warm water dinoflagellates, such as Karenia brevis , can have long-term effects on ecosystems and the economies of local fisheries. K. brevis events have been linked to the mortality of fish and invertebrates in the Gulf of Mexico for over 50 years. The west coast of Florida has experienced several HABs, resulting in the mortality of various marine species. Higher-trophic organisms, such as dolphins and manatees, are also vulnerable to the effects of these toxins. Consequently, HABs have been extensively investigated over the past several decades, often serving as the focus of national and international environmental policy discussions. Commercial and artisanal fisheries rank among the most crucial industries in the Japanese economy, directly or indirectly impacting millions of Japanese citizens. HABs can profoundly disrupt local fisheries, resulting in considerable economic losses. In severe instances, such events may necessitate the complete closure of fisheries in affected areas. HABs have been documented in Japan for centuries, with records dating back to 731 CE ( Fukuyo et al., 2002 ). Many of these occurrences have been observed in southern Japan, particularly in regions like the Seto Inland Sea ( Oghaki et al., 2019 ). The heightened frequency of HABs over the last 50 years, extending to higher latitudes, correlates with increasing global temperatures ( Imai et al., 2006 ; Zohdi & Abbaspour, 2019 ). Historically, open ocean HABs have been rare in the cold waters around Hokkaido, with occurrences primarily concentrated in shallow coastal waters and bays. ( Iwataki et al., 2022 ; Shimada, 2021 ). However, in 2021, a HAB linked to ocean temperatures 1-3°C above average occurred in eastern Hokkaido, resulting in extensive fish and sea urchin mortality ( Kuroda et al., 2021 ; Iwataki et al., 2022 ; Yamaguchi et al., 2022 ). This event significantly affected the sea urchin fishery, which relies on hatchery production for reseeding coastal habitats ( Hasegawa et al., 2022 ; Iwataki et al., 2022 ; Kuroda et al., 2022 ). We used the HAB in 2021 to study the ecosystem-level effects in eastern Hokkaido. Sea otters in this area were extirpated during the 19th-century Maritime Fur Trade but began recolonizing the area in the 1980s ( Hattori et al., 2005 ; Kenyon, 1969 ; Tezuka, 2009 ). While there is limited information regarding the diet of sea otters in Hokkaido, we have observed them eating bivalves ( Clinocardium californiense, Callista brevisiphonata , and others), sea urchins ( Strongylocentrotus intermedius ), crabs ( Paralithodes brevipes and Telmessus cheiragonus ), snails, and chitons ( Cryptochiton stelleri ) ( Mitani et al., 2021 ). Bivalves are the predominant prey for sea otters in our study area, but sea urchins and crabs are also important. In response to the HAB, our null hypothesis was that sea otters would accommodate to the reduced abundance of sea urchins by shifting to other prey, with minimal effects on health and behavior. The alternate hypothesis was that the HAB would severely affect sea otters, including decreased food consumption, emaciation, and possibly death. We also hypothesized that any dietary shifts would depend on the recovery of benthic invertebrates, especially sea urchins. Materials and Methods 1) Study Area Our study area was the Moyururi and Yururi Islands (43.2219°, 145.6244°), about 4 km from the coast and 12 km from Nemuro in Eastern Hokkaido. This area has commercial fisheries for sea urchins, crabs, and various species of kelp. 2) Benthic Survey Benthic surveys were conducted using SCUBA in September 2020, 2022, and 2023 in an area of concentrated sea otter foraging activity along the west coast of Moyururi Island. The sea area was divided by twenty 200 m x 200 m grids, and one point each grid was set. A professional diver sampled benthic invertebrates in four randomly selected 50 cm x 50 cm quadrats around each point. Crabs were counted but not collected, so morphometrics (length, width, and mass) were not recorded. They are also significantly more mobile than other benthic organisms collected, so it would be difficult to confirm the number of crabs in the survey area. All other specimens were frozen at -20°C until species identification and morphometrics were recorded later. Specimens were divided into three size classes: small (2-5 cm), medium (5-10 cm), and large (>10 cm), following Kvitek et al. (1993) . The number of specimens counted or collected was used to estimate each species’ average seafloor density (number m -2 ). 3) Sea Otter Diet We conducted observations of sea otter foraging behavior using binoculars (Nikon StabilEyes 16x32, Nikon, Minato City, Tokyo, Japan) during 30-minute focal follows from June to August 2020, June to September 2021, and May to September 2022 from a small boat. The location of each focal follow was recorded using GPS (Garmin, Olathe, Kansas, USA). When a sea otter began feeding, we documented dive duration, prey type (to the highest specificity possible), prey number, prey size, and inter-dive interval. Only focal follows with 5-10 foraging dives were included in our analysis to avoid sampling bias ( Watt et al., 2000 ; LaRoche et al., 2021 ). Prey size was estimated relative to the width of a sea otter paw (i.e., 5 cm; Kvitek et al., 1993 ). 4) Data Analysis We compared the seafloor densities for bivalves, sea urchins, snails, chitons, and crabs pre-(2020) and post-HAB (2022, 2023). Additionally, we compared sea otter prey compositions (percentage of dietary bivalves, crabs, sea urchins, chitons, and snails) before (2020-2021), immediately after (2022), and one year after (2023) the HAB. Prey species that could not be identified were categorized as unknown and excluded from the analysis. Other prey items that were anecdotally observed, such as sea cucumbers and hermit crabs, were also excluded from the analysis. A Shapiro-Wilks normality test confirmed normal distributions for both benthic organism number and sea otter dietary percentage data. Tukey’s HSP tests were conducted to identify differences ( Almeida et al., 2012 ; Estes et al., 1995 ; Johnson et al., 2020 ; LaRoche et al., 2021 ; Patel et al., 2023 ). Results 1) Benthic Surveys On average, 235 benthic specimens were collected from 20 grids ( Table 1 ) during each survey. Before the HAB (2020), sea urchins (6.7 per m 2 ) had the highest seafloor density, followed by snails (1.5 per m 2 ), chitons (0.6 per m 2 ), and bivalves (0.3 per m 2 ). Immediately after the HAB (2022), sea urchins (1.2 per m 2 ) decreased significantly (82%) from pre-HAB levels (Tukey’s HSD test, p < 0.05), while bivalves (1.8 per m 2 ) displayed a 6-fold increase (p = 0.066) ( Fig. 2 ). No significant differences were observed for chitons (0.4 per m 2 ) and snails (2.8 per m 2 ) between 2020 and 2022 (Chitons p = 0.845, Snails p = 0.364). One year after the HAB (2023), the density of bivalves (1.3 per m 2 , p = 0.712) declined 28% from levels immediately after the HAB but remained elevated by 4.3-fold compared to pre-HAB densities. Likewise, snails (2.0 per m 2 , p = 0.645) decreased by 29%, sea urchins (2.3 per m 2 , p = 0.115) increased by 2-fold, and chitons (0.5 per m 2 , p = 0.959) remained unchanged. View this table: View inline View popup Download powerpoint Table 1. Seafloor densities (per m 2 ) of invertebrates sampled during surveys before (2020) and after (2022 and 2023) the HAB Download figure Open in new tab Fig. 1. The study area for the benthic surveys at Moyururi Island in Eastern Hokkaido. Square blocks show the 200 m 2 quadrats surveyed utilizing random quadrat sampling. Download figure Open in new tab Fig. 2. Number (per m 2 ) of major sea otter prey items sampled from SCUBA survey: a (Sea Urchins), b (Chitons), c (Bivalves), d (Snails) retrieved during benthic quadrat surveys of 2020, 2022, and 2023. Asterisks(*) above the graph display a significant difference (p < 0.05) between two years. 2) Sea Otter Diet From 2020-2022, 265 foraging dives during 34 focal follows were monitored, and 508 prey items were recorded ( Table 2 ). Before the HAB (October 2021), there were no significant differences in the percentages of prey captured during focal follows ( Table 2 ). The predominate prey were bivalves ( x - = 34.8%; range 31.8-36.5%), crabs ( x - = 13.7%; range 12.9-15.3%), and sea urchins ( x - = 7.8; range 4.7-13.7%). The average percentages for chitons and snails were less than 5%. Immediately after the HAB in 2022, the percentage of dietary bivalves increased significantly (2-fold) to 67.3% (Tukey’s HSD test, p < 0.05), while sea urchins completely disappeared from the diet ( Fig. 3 ). One year after the HAB (2023), the percentage of sea urchins increased significantly to 13.9% (p < 0.05) and the percentage of bivalves returned to near the pre-HAB level of 37.5% (p < 0.05). The percentages of chitons, snails, and crabs in the diet were not significantly different across the entire survey period. View this table: View inline View popup Download powerpoint Table 2. Mean (+I SD) percentage of prey in focal follow pre-HAB (2020, 202 I) and post-HAB (2022 and 2023) Download figure Open in new tab Fig. 3. Observed average proportion of major prey items of sea otters: a (Sea Urchins), b (Chitons), c (Bivalves), d (Snails), and e (Crabs) per bout in the Sea Otter diets at Moyururi and Yururi Islands from 2020/ 2021, 2022, and 2023. Error bars represent ±I SE. Asterisks(*) above the graph display a significant difference (p < 0.05) between two or more years. Discussion Our benthic surveys revealed an 82% decrease in sea urchin density and a 6-fold increase in the number of bivalves immediately after the HAB in 2022 ( Table 1 ). By the following year (2023), the average sea urchin density showed partial recovery, while clam density remained elevated compared to 2020. However, our surveys were not comprehensive and susceptible to interannual sampling bias. Nevertheless, our data indicated a pronounced decrease in sea urchin density after the HAB, with a partial recovery one year later. Additionally, clam density appeared to increase post-HAB and remain elevated. An earlier study showed that the HAB caused mass mortality of sea urchins and moderate effects on chitons and snails throughout the coastal waters of eastern Hokkaido, similar to HABs in other regions (Friligos and Gotsis-Skretas, 1989; Jin et al., 2008 ; Backer, 2009 ; Ohgaki et al., 2019; Iwataki et al. 2022 ; Orlova et al., 2022 ). Consequently, the HAB likely caused the decrease in sea urchin density and distribution around the Moyururi and Yururi Islands. Reseeding with hatchery-raised sea urchins did not occur in our study area after the HAB, so the partial recovery represents a natural process that may take about three years before sea urchins reach the size consumed by sea otters (Ochiishii Fisheries Cooperative, pers. comm.). We observed an increase in the density of bivalves after the HAB. Bivalves filter phytoplankton from the water column for nutrition and may exhibit higher growth rates during HABs ( Foe & Knight, 1985 ). Certain algal blooms, such as brown tide algae ( Aureococcus anophagefferens ) along the northeastern coast of the United States, can adversely affect bivalves by inhibiting larval growth (( Rolton et al., 2014 ; Przeslawski et al., 2008 ). However, some bivalves are not affected by the brevetoxin-producing algae Karenia selliformis ( Yao & Takashi, 2023 ). Generally, more intense planktonic blooms are associated with higher water temperatures ( Peeters et al., 2007 ; Visser et al., 2016 ), and such conditions were observed before the HAB in our study area ( Yamaguchi et al., 2022 ). Our results may indicate enhanced bivalve growth, as small (2-5 cm) bivalves significantly increased abundance (Tukey’s HSD Test, p < 0.05). However, we cannot rule out interannual sampling bias. Chitons and snails did not significantly change in abundance over the three years. We observed a shift in the sea otter diet immediately after the HAB and during the recovery period one year later. Before the HAB, sea urchins accounted for 9.2% (range 4.7-13.7%) of the diet. However, following the HAB, sea urchins disappeared from the diet ( Table 2 ), reflecting their diminished abundance. Despite this, the number of sea otters in the study area remained constant (Suzuki et al., in prep). Bivalves were the predominant prey (34.1%) before the HAB, with their contribution to the diet doubling to 67.3% after the HAB ( Table 2 ). The likely cause for this increase was prey-switching when sea urchins decreased in abundance. This switch may have been facilitated by the enhanced growth of bivalves, leading to increased abundance in larger size classes. Our results suggest that as generalists ( Davis and Bodkin, 2021 ), sea otters responded to the shifting benthic community structure by consuming prey that became more abundant because of the HAB. Sea otter populations in California and the Aleutian Islands, Alaska, show a greater preference for sea urchins compared with those in eastern Hokkaido ( Estes et al., 1978 ; Estes et al., 1980 ; LaRoche et al., 2021 ; Watt et al., 2000 ). Sea otter dietary preference correlates with prey abundance, and they do not necessarily require a wide range of prey to thrive (Ostfeld 1982; Tinker et al. 2008 ; Wolt et al. 2012 ; Davis et al. 2021 ). The unusual HAB ( Gail, 1950 ; Orlova et al., 2002 ) in eastern Hokkaido provided an opportunity to observe the ecosystem effects at two trophic levels ( Hasegawa et al., 2022 ; Iwataki et al. 2022 ; Kuroda et al. 2021 ; Kuroda et al., 2022 ). Because of the dietary adaptability of sea otters ( Davis and Bodkin, 2021 ), the HAB had no obvious effect on the health and abundance of sea otters in our study area. As sea urchins recover, their dietary contribution may return to pre-HAB levels, especially with the reseeding of small, hatchery sea urchins. Acknowledgments We thank Professors K. Miyashita and M. Nakaoka from Hokkaido University Fisheries Science Center for providing advice and access to research facilities. Captain Y. Kotani supported sea otter observations and piloted the research vessel, and T. Tani conducted the benthic surveys. We thank students for assistance in the benthic specimen analysis. Hokkaido University allowed the use of the Hakodate Fisheries Science Center and the Akkeshi Marine Station for research and lodging. Special thanks to the Ochiishi and Nemuro Fisheries Cooperatives for permitting the benthic sampling and information on the reseeding of hatchery-raised sea urchins. This study was funded by the Asahi Glass Foundation in 2020-2021 (to I.S. and Y.M.), the Sasakawa Peace Foundation in 2021 (to S.O. and Y.M.), the Hokkaido University DX Doctoral Fellowship for 2022-2023 (to J.J.), the Pro Natura Fund (to I.S., R.D., and Y.M.), and the JSPS (Japanese Society for the Promotion of Science) Invitational Fellowships for Research in Japan (to R.D. and Y.M.). Footnotes Conceptualization: JJ, IS, YM; Data collection: JJ, IS, NK, KM, SO, YM; Data analysis & visualization: JJ; Writing – Original Draft Preparation: JJ, IS; Writing – review and editing: All authors; Funding acquisition: JJ, IS, YM, RD; Methodology: JJ, IS, YM, RD, SO; Project Administration: YM, IS. References ↵ Almeida D , Copp GH , Masson L , Miranda R , Murai M , Sayer CD . Changes in the diet of a recovering Eurasian otter population between the 1970s and 2010 . Aquatic Conservation: Marine and Freshwater Ecosystems 2012 ; 22 : 26 – 35 OpenUrl Andrade-Villagran PV , Aguero MJ , Navarro , JM , and Urzua A. The paralytic shellfish toxin effect on bioenergetic constituents of the fishery resource Chorus giganteus (Gastropoda: Muricidae) . Marine Environmental Research 2022 ; 180 : 105735 OpenUrl ↵ Backer LC . Impacts of Florida red tides on coastal communities . 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Harmful algal blooms (red tide): a review of causes, impacts, and approaches to monitoring and prediction . International Journal of Environmental Science and Technology 2019 ; 16 : 1789 – 1806 OpenUrl View the discussion thread. Back to top Previous Next Posted April 26, 2024. Download PDF Email Thank you for your interest in spreading the word about bioRxiv. NOTE: Your email address is requested solely to identify you as the sender of this article. Your Email * Your Name * Send To * Enter multiple addresses on separate lines or separate them with commas. You are going to email the following The effect of a harmful algal bloom (Karenia selliformis) on the benthic invertebrate community and the sea otter (Enhydra lutris) diet in eastern Hokkaido Message Subject (Your Name) has forwarded a page to you from bioRxiv Message Body (Your Name) thought you would like to see this page from the bioRxiv website. 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Share The effect of a harmful algal bloom ( Karenia selliformis ) on the benthic invertebrate community and the sea otter ( Enhydra lutris ) diet in eastern Hokkaido Jackson Johnstone , Ippei Suzuki , Natsuki Konno , Kyohei Murayama , Satsuki Ochiai , Randall Davis , Yoko Mitani bioRxiv 2024.04.23.590716; doi: https://doi.org/10.1101/2024.04.23.590716 Share This Article: Copy Citation Tools The effect of a harmful algal bloom ( Karenia selliformis ) on the benthic invertebrate community and the sea otter ( Enhydra lutris ) diet in eastern Hokkaido Jackson Johnstone , Ippei Suzuki , Natsuki Konno , Kyohei Murayama , Satsuki Ochiai , Randall Davis , Yoko Mitani bioRxiv 2024.04.23.590716; doi: https://doi.org/10.1101/2024.04.23.590716 Citation Manager Formats BibTeX Bookends EasyBib EndNote (tagged) EndNote 8 (xml) Medlars Mendeley Papers RefWorks Tagged Ref Manager RIS Zotero Tweet Widget Facebook Like Google Plus One Subject Area Ecology Subject Areas All Articles Animal Behavior and Cognition (7649) Biochemistry (17738) Bioengineering (13925) Bioinformatics (42059) Biophysics (21496) Cancer Biology (18643) Cell Biology (25577) Clinical Trials (138) Developmental Biology (13406) Ecology (19946) Epidemiology (2067) Evolutionary Biology (24370) Genetics (15627) Genomics (22551) Immunology (17772) Microbiology (40497) Molecular Biology (17212) Neuroscience (88786) Paleontology (667) Pathology (2845) Pharmacology and Toxicology (4835) Physiology (7663) Plant Biology (15177) Scientific Communication and Education (2047) Synthetic Biology (4304) Systems Biology (9838) Zoology (2272)