Predator-Induced Fleeing Behaviors in Phytoplankton: A New Mechanism for Harmful Algal Bloom Formation?
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{"title"=>"Predator-Induced Fleeing Behaviors in Phytoplankton: A New Mechanism for Harmful Algal Bloom Formation?", "type"=>"journal", "authors"=>[{"first_name"=>"Elizabeth L.", "last_name"=>"Harvey", "scopus_author_id"=>"36774504400"}, {"first_name"=>"Susanne", "last_name"=>"Menden-Deuer", "scopus_author_id"=>"6507681524"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"issn"=>"19326203", "pui"=>"365766155", "doi"=>"10.1371/journal.pone.0046438", "sgr"=>"84866987466", "scopus"=>"2-s2.0-84866987466", "isbn"=>"1932-6203", "pmid"=>"23029518"}, "id"=>"04a7b087-080e-3b64-a4e5-61c88bc9e52b", "abstract"=>"In the plankton, heterotrophic microbes encounter and ingest phytoplankton prey, which effectively removes >50% of daily phytoplankton production in the ocean and influences global primary production and biochemical cycling rates. Factors such as size, shape, nutritional value, and presence of chemical deterrents are known to affect predation pressure. Effects of movement behaviors of either predator or prey on predation pressure, and particularly fleeing behaviors in phytoplankton are thus far unknown. Here, we quantified individual 3D movements, population distributions, and survival rates of the toxic phytoplankton species, Heterosigma akashiwo in response to a ciliate predator and predator-derived cues. We observed predator-induced defense behaviors previously unknown for phytoplankton. Modulation of individual phytoplankton movements during and after predator exposure resulted in an effective separation of predator and prey species. The strongest avoidance behaviors were observed when H. akashiwo co-occurred with an actively grazing predator. Predator-induced changes in phytoplankton movements resulted in a reduction in encounter rate and a 3-fold increase in net algal population growth rate. A spatially explicit population model predicted rapid phytoplankton bloom formation only when fleeing behaviors were incorporated. These model predictions reflected field observations of rapid H. akashiwo harmful algal bloom (HAB) formation in the coastal ocean. Our results document a novel behavior in phytoplankton that can significantly reduce predation pressure and suggests a new mechanism for HAB formation. Phytoplankton behaviors that minimize predatory losses, maximize resource acquisition, and alter community composition and distribution patterns could have major implications for our understanding and predictive capacity of marine primary production and biochemical cycling rates.", "link"=>"http://www.mendeley.com/research/predatorinduced-fleeing-behaviors-phytoplankton-new-mechanism-harmful-algal-bloom-formation", "reader_count"=>67, "reader_count_by_academic_status"=>{"Unspecified"=>2, "Professor > Associate Professor"=>4, "Researcher"=>15, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>3, "Student > Master"=>13, "Other"=>1, "Student > Bachelor"=>6, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>2, "Professor > Associate Professor"=>4, "Researcher"=>15, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>20, "Student > Postgraduate"=>3, "Student > Master"=>13, "Other"=>1, "Student > Bachelor"=>6, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Environmental Science"=>15, "Biochemistry, Genetics and Molecular Biology"=>4, "Mathematics"=>1, "Agricultural and Biological Sciences"=>36, "Physics and Astronomy"=>2, "Psychology"=>1, "Earth and Planetary Sciences"=>5}, "reader_count_by_subdiscipline"=>{"Physics and Astronomy"=>{"Physics and Astronomy"=>2}, "Psychology"=>{"Psychology"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>5}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>36}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>15}}, "reader_count_by_country"=>{"New Zealand"=>1, "Canada"=>1, "United States"=>3, "Ireland"=>1, "Brazil"=>1, "Poland"=>1, "United Kingdom"=>1, "Chile"=>1, "Spain"=>1}, "group_count"=>4}

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/567682"], "description"=>"<p>Predictions of phytoplankton abundance and distribution in a spatially explicit model that does (top) and does not (bottom) include empirically observed phytoplankton avoidance of predator inhabited, deeper waters. All parameters, including growth rates were empirically measured and, with the exception of fleeing behaviors, identical in all model runs.</p>", "links"=>[], "tags"=>["predator-induced", "fleeing", "behaviors", "phytoplankton", "bloom"], "article_id"=>238176, "categories"=>["Inorganic Chemistry", "Microbiology", "Plant Biology"], "users"=>["Elizabeth L. Harvey", "Susanne Menden-Deuer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046438.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_predator_induced_fleeing_behaviors_on_phytoplankton_bloom_formation_/238176", "title"=>"Effect of predator-induced fleeing behaviors on phytoplankton bloom formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-28 02:16:16"}
  • {"files"=>["https://ndownloader.figshare.com/files/567570"], "description"=>"<p>Population growth rate (µ day<sup>−1</sup>) of <i>H. akashiwo</i> either in a halocline (black) or linear (gray) salinity gradient in the phytoplankton only control (left) and in the presence of the predator (right). Phytoplankton fleeing behaviors and availability of a low salinity refuge effectively reduced predator-prey encounter rates and resulted in significant growth of <i>H. akashiwo</i> in the presence of the predator.</p>", "links"=>[], "tags"=>["phytoplankton"], "article_id"=>238078, "categories"=>["Inorganic Chemistry", "Microbiology", "Plant Biology"], "users"=>["Elizabeth L. Harvey", "Susanne Menden-Deuer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046438.g005", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Salinity_structure_impact_on_phytoplankton_growth_rate_/238078", "title"=>"Salinity structure impact on phytoplankton growth rate.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-28 02:14:38"}
  • {"files"=>["https://ndownloader.figshare.com/files/567318"], "description"=>"<p>Mean (a) swimming speed (µm s<sup>−1</sup>), (b) vertical velocity (µm s<sup>−1</sup>) and (c) root mean square distance (RMSD) (mm) of <i>H. akashiwo</i> in the absence (white triangles) and presence of the predator (red circles) above the halocline. Movement behaviors reflect significantly more retentive swimming above the halocline in response to the presence of the predator below the halocline.</p>", "links"=>[], "tags"=>["halocline"], "article_id"=>237819, "categories"=>["Inorganic Chemistry", "Microbiology", "Plant Biology"], "users"=>["Elizabeth L. Harvey", "Susanne Menden-Deuer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046438.g003", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Above_halocline_movement_behaviors_/237819", "title"=>"Above halocline movement behaviors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-28 02:10:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/567219"], "description"=>"<p>Vertical flux (log cells µm<sup>−2</sup> sec<sup>−1</sup>) of <i>H. akashiwo</i>, below the halocline, in the absence (top) and presence (bottom) of the predator. Warmer colors = upward flux and cooler colors = downward flux of phytoplankton cells. After 6 h, in the presence of the predator, the vertical flux of <i>H. akashiwo</i> was strongly and persistently upward. In contrast, the vertical flux of <i>H. akashiwo</i> in the absence of a predator was initially downward and then directionally inconsistent resulting in no effective change in population distribution.</p>", "links"=>[], "tags"=>["halocline"], "article_id"=>237717, "categories"=>["Inorganic Chemistry", "Microbiology", "Plant Biology"], "users"=>["Elizabeth L. Harvey", "Susanne Menden-Deuer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046438.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Below_halocline_vertical_flux_/237717", "title"=>"Below halocline vertical flux.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-28 02:08:37"}
  • {"files"=>["https://ndownloader.figshare.com/files/567108"], "description"=>"<p>Mean (a) swimming speed (µm s<sup>−1</sup>), (b) mean vertical velocity (µm s<sup>−1</sup>), and (c) root mean square distance (RMSD) (mm) of <i>H. akashiwo</i> in the absence (white triangles) and presence of the ciliate predator (purple circles) below the halocline. Error bars here and in all figures are one standard error (SE) of the mean. Frequently SE was small and contained within the symbols. Movement behaviors reflect significantly greater speed and upward motility below the halocline in response to the presence of the predator.</p>", "links"=>[], "tags"=>["halocline"], "article_id"=>237606, "categories"=>["Inorganic Chemistry", "Microbiology", "Plant Biology"], "users"=>["Elizabeth L. Harvey", "Susanne Menden-Deuer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046438.g001", "stats"=>{"downloads"=>12, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Below_halocline_movement_behaviors_/237606", "title"=>"Below halocline movement behaviors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-28 02:06:46"}
  • {"files"=>["https://ndownloader.figshare.com/files/299787"], "description"=>"<div><p>In the plankton, heterotrophic microbes encounter and ingest phytoplankton prey, which effectively removes >50% of daily phytoplankton production in the ocean and influences global primary production and biochemical cycling rates. Factors such as size, shape, nutritional value, and presence of chemical deterrents are known to affect predation pressure. Effects of movement behaviors of either predator or prey on predation pressure, and particularly fleeing behaviors in phytoplankton are thus far unknown. Here, we quantified individual 3D movements, population distributions, and survival rates of the toxic phytoplankton species, <em>Heterosigma akashiwo</em> in response to a ciliate predator and predator-derived cues. We observed predator-induced defense behaviors previously unknown for phytoplankton. Modulation of individual phytoplankton movements during and after predator exposure resulted in an effective separation of predator and prey species. The strongest avoidance behaviors were observed when <em>H. akashiwo</em> co-occurred with an actively grazing predator. Predator-induced changes in phytoplankton movements resulted in a reduction in encounter rate and a 3-fold increase in net algal population growth rate. A spatially explicit population model predicted rapid phytoplankton bloom formation only when fleeing behaviors were incorporated. These model predictions reflected field observations of rapid <em>H. akashiwo</em> harmful algal bloom (HAB) formation in the coastal ocean. Our results document a novel behavior in phytoplankton that can significantly reduce predation pressure and suggests a new mechanism for HAB formation. Phytoplankton behaviors that minimize predatory losses, maximize resource acquisition, and alter community composition and distribution patterns could have major implications for our understanding and predictive capacity of marine primary production and biochemical cycling rates.</p> </div>", "links"=>[], "tags"=>["predator-induced", "fleeing", "behaviors", "harmful", "algal", "bloom"], "article_id"=>119114, "categories"=>["Inorganic Chemistry", "Microbiology", "Cell Biology"], "users"=>["Elizabeth L. Harvey", "Susanne Menden-Deuer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046438", "stats"=>{"downloads"=>2, "page_views"=>14, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Predator_Induced_Fleeing_Behaviors_in_Phytoplankton_A_New_Mechanism_for_Harmful_Algal_Bloom_Formation_/119114", "title"=>"Predator-Induced Fleeing Behaviors in Phytoplankton: A New Mechanism for Harmful Algal Bloom Formation?", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-28 02:31:54"}
  • {"files"=>["https://ndownloader.figshare.com/files/567409"], "description"=>"<p>Modulation of phytoplankton movements as a function of predator-derived cues. Difference in (a) swimming speed (µm s<sup>−1</sup>) and (b) vertical velocity (µm s<sup>−1</sup>), above and below the halocline (dotted line), (c) root mean square distance (mm), a proxy of population dispersal rates and (d) characteristic swimming tracks and speeds in the different predator exposure treatments; black circles denote the beginning of a swimming track. Fleeing behavior by the phytoplankton was significant but quantitatively different in response to specific predator-derived cues as evident in swimming metrics, tracks, and dispersal.</p>", "links"=>[], "tags"=>["predator-derived", "stimuli"], "article_id"=>237906, "categories"=>["Inorganic Chemistry", "Microbiology", "Plant Biology"], "users"=>["Elizabeth L. Harvey", "Susanne Menden-Deuer"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0046438.g004", "stats"=>{"downloads"=>1, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Impact_of_predator_derived_stimuli_on_movement_behaviors_/237906", "title"=>"Impact of predator-derived stimuli on movement behaviors.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-09-28 02:11:46"}

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Relative Metric

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