Flapping before Flight: High Resolution, Three-Dimensional Skeletal Kinematics of Wings and Legs during Avian Development
Publication Date
April 21, 2016
Journal
PLOS ONE
Authors
Ashley M. Heers, David B. Baier, Brandon E. Jackson & Kenneth P. Dial
Volume
11
Issue
4
Pages
e0153446
DOI
https://dx.plos.org/10.1371/journal.pone.0153446
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0153446
Web of Science
000374898500033
Scopus
84964669913
Mendeley
http://www.mendeley.com/research/flapping-before-flight-high-resolution-threedimensional-skeletal-kinematics-wings-legs-during-avian
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{"title"=>"Flapping before flight: High resolution, three-dimensional skeletal kinematics of wings and legs during avian development", "type"=>"journal", "authors"=>[{"first_name"=>"Ashley M.", "last_name"=>"Heers", "scopus_author_id"=>"36987849300"}, {"first_name"=>"David B.", "last_name"=>"Baier", "scopus_author_id"=>"8656148900"}, {"first_name"=>"Brandon E.", "last_name"=>"Jackson", "scopus_author_id"=>"23667350200"}, {"first_name"=>"Kenneth P.", "last_name"=>"Dial", "scopus_author_id"=>"6603809455"}], "year"=>2016, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84964669913", "scopus"=>"2-s2.0-84964669913", "pui"=>"610063583", "issn"=>"19326203", "doi"=>"10.1371/journal.pone.0153446"}, "id"=>"d6ed6346-8fc5-314f-a23c-2230ca687146", "abstract"=>"Some of the greatest transformations in vertebrate history involve developmental and evolutionary origins of avian flight. Flight is the most power-demanding mode of locomotion, and volant adult birds have many anatomical features that presumably help meet these demands. However, juvenile birds, like the first winged dinosaurs, lack many hallmarks of advanced flight capacity. Instead of large wings they have small \"protowings\", and instead of robust, interlocking forelimb skeletons their limbs are more gracile and their joints less constrained. Such traits are often thought to preclude extinct theropods from powered flight, yet young birds with similarly rudimentary anatomies flap-run up slopes and even briefly fly, thereby challenging longstanding ideas on skeletal and feather function in the theropod-avian lineage. Though skeletons and feathers are the common link between extinct and extant theropods and figure prominently in discussions on flight performance (extant birds) and flight origins (extinct theropods), skeletal inter-workings are hidden from view and their functional relationship with aerodynamically active wings is not known. For the first time, we use X-ray Reconstruction of Moving Morphology to visualize skeletal movement in developing birds, and explore how development of the avian flight apparatus corresponds with ontogenetic trajectories in skeletal kinematics, aerodynamic performance, and the locomotor transition from pre-flight flapping behaviors to full flight capacity. Our findings reveal that developing chukars (Alectoris chukar) with rudimentary flight apparatuses acquire an \"avian\" flight stroke early in ontogeny, initially by using their wings and legs cooperatively and, as they acquire flight capacity, counteracting ontogenetic increases in aerodynamic output with greater skeletal channelization. In conjunction with previous work, juvenile birds thereby demonstrate that the initial function of developing wings is to enhance leg performance, and that aerodynamically active, flapping wings might better be viewed as adaptations or exaptations for enhancing leg performance.", "link"=>"http://www.mendeley.com/research/flapping-before-flight-high-resolution-threedimensional-skeletal-kinematics-wings-legs-during-avian", "reader_count"=>46, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>10, "Professor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Doctoral Student"=>2, "Student > Ph. D. Student"=>14, "Student > Master"=>6, "Other"=>1, "Student > Bachelor"=>10, "Professor"=>2}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Engineering"=>5, "Environmental Science"=>2, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>16, "Medicine and Dentistry"=>3, "Design"=>1, "Veterinary Science and Veterinary Medicine"=>2, "Physics and Astronomy"=>1, "Earth and Planetary Sciences"=>10}, "reader_count_by_subdiscipline"=>{"Design"=>{"Design"=>1}, "Engineering"=>{"Engineering"=>5}, "Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Physics and Astronomy"=>{"Physics and Astronomy"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>10}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>16}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Environmental Science"=>{"Environmental Science"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"Canada"=>1, "Sweden"=>1, "United States"=>3, "Germany"=>1}, "group_count"=>3}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/5001337"], "description"=>"<p><b>Left.</b> Flight-capable adult birds have many morphological features that are presumably adaptations or exaptations for meeting aerial challenges. Large wings with stiff, asymmetrical primary feathers (A) are thought to stabilize feathers against oncoming airflow [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref048\" target=\"_blank\">48</a>], prevent excessive deformation [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref023\" target=\"_blank\">23</a>], and reduce feather permeability [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref049\" target=\"_blank\">49</a>]. Fused thoracic and sacral vertebrae may increase trunk rigidity and help transmit limb-generated forces to the rest of the body (notarium, B), and/or possibly act as a shock absorber during landing (synsacrum, C) [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref021\" target=\"_blank\">21</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref026\" target=\"_blank\">26</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref028\" target=\"_blank\">28</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref050\" target=\"_blank\">50</a>]. Appendicularly, the robust forelimb apparatus (e.g., sternum with large keel (D), strut-like and well-articulated coracoids (E), bowed ulna (F)) allows for the attachment and contraction of powerful flight muscles (e.g., pectoralis, supracoracoideus) [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref027\" target=\"_blank\">27</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref028\" target=\"_blank\">28</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref026\" target=\"_blank\">26</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref025\" target=\"_blank\">25</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref021\" target=\"_blank\">21</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref051\" target=\"_blank\">51</a>], while the acrocoracoid and triosseal canal (not shown; present in juveniles but less elevated above glenoid) allow the supracoracoideus muscle to act as a pulley, contributing to humeral elevation and rotation [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref028\" target=\"_blank\">28</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref026\" target=\"_blank\">26</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref029\" target=\"_blank\">29</a>–<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref033\" target=\"_blank\">33</a>]. Distally, reduced and fused skeletal elements and channelized limb joints (G, H) are thought to reduce mass and permit rapid, efficient limb oscillation, coordinate elbow and wrist movement, keep a planar wing orientation during the downstroke, and increase stride effectiveness by restricting ankle movements to a single plane of motion [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref027\" target=\"_blank\">27</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref028\" target=\"_blank\">28</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref026\" target=\"_blank\">26</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref022\" target=\"_blank\">22</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref052\" target=\"_blank\">52</a>]. Collectively, these features are a key component of the avian <i>bauplan</i>, and a classic example of anatomical specialization. <b>Right.</b> Developing birds–like early winged dinosaurs–lack many hallmarks of advanced flight capacity [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref010\" target=\"_blank\">10</a>]. Instead of large wings they have small protowings, with a more gracile skeleton and less constrained joints. Immature birds nevertheless flap their rudimentary wings to accomplish a variety of locomotor tasks [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref020\" target=\"_blank\">20</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref053\" target=\"_blank\">53</a>–<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref055\" target=\"_blank\">55</a>]; in fact, many anatomical specializations of adults are acquired long after flight capacity is achieved. Developing birds thereby challenge the traditional, longstanding view of form-function relationships in the theropod-avian lineage (A-H). Cervical vertebrae and pedal phalanges not shown; juvenile keel on top of adult keel, for scale (D); in (G), left image is pronation of carpometacarpus, right is abduction (juvenile joints always more flexible). Although cartilaginous skeletal components are not shown, this does not alter functional interpretations of the juvenile skeleton (e.g., juveniles possess a small cartilaginous extension of the keel, but both the keel and the muscles that attach to it are still proportionally much smaller in juveniles than adults; carpal bones of developing birds have the specialized shapes of adults, but are poorly ossified and not capable of resisting enough joint torque to channelize the wrist joint (G)). Images of feather microstructure (A) reprinted from [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref018\" target=\"_blank\">18</a>] under a CC BY license, with permission from The Company of Biologists Limited, original copyright 2011.</p>", "links"=>[], "tags"=>["volant adult birds", "leg performance", "flight capacity"], "article_id"=>3195754, "categories"=>["Medicine", "Neuroscience", "Evolutionary Biology", "Environmental Sciences not elsewhere classified", "Ecology", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Developmental Biology", "Infectious Diseases"], "users"=>["Ashley M. Heers", "David B. Baier", "Brandon E. Jackson", "Kenneth P. Dial"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153446.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Ontogeny_of_flight_aptations_/3195754", "title"=>"Ontogeny of flight aptations.", "pos_in_sequence"=>2, "defined_type"=>1, "published_date"=>"2016-04-21 06:02:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001463"], "description"=>"<p>r<sub>s</sub>: Spearman’s rank correlation coefficient; A-J: adult mean–juvenile mean; x, y, z: joint rotations shown in Fig D (z, top row: flexion-extension; y, middle row: abduction-adduction; x, bottom row: long axis rotation); avg (average), max (maximum), min (minimum), and range: kinematic variables tested for statistical significance (Table E in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.s001\" target=\"_blank\">S1 File</a>).</p>", "links"=>[], "tags"=>["volant adult birds", "leg performance", "flight capacity"], "article_id"=>3195868, "categories"=>["Medicine", "Neuroscience", "Evolutionary Biology", "Environmental Sciences not elsewhere classified", "Ecology", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Developmental Biology", "Infectious Diseases"], "users"=>["Ashley M. Heers", "David B. Baier", "Brandon E. Jackson", "Kenneth P. Dial"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153446.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Ontogenetic_trends_and_differences_between_adults_and_juveniles_flap_running_up_60_65_inclines_hind_limb_kinematics_/3195868", "title"=>"Ontogenetic trends and differences between adults and juveniles flap-running up 60–65° inclines: hind limb kinematics.", "pos_in_sequence"=>5, "defined_type"=>1, "published_date"=>"2016-04-21 06:02:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001184", "https://ndownloader.figshare.com/files/5001199", "https://ndownloader.figshare.com/files/5001214", "https://ndownloader.figshare.com/files/5001238", "https://ndownloader.figshare.com/files/5001250", "https://ndownloader.figshare.com/files/5001283"], "description"=>"<div><p>Some of the greatest transformations in vertebrate history involve developmental and evolutionary origins of avian flight. Flight is the most power-demanding mode of locomotion, and volant adult birds have many anatomical features that presumably help meet these demands. However, juvenile birds, like the first winged dinosaurs, lack many hallmarks of advanced flight capacity. Instead of large wings they have small “protowings”, and instead of robust, interlocking forelimb skeletons their limbs are more gracile and their joints less constrained. Such traits are often thought to preclude extinct theropods from powered flight, yet young birds with similarly rudimentary anatomies flap-run up slopes and even briefly fly, thereby challenging longstanding ideas on skeletal and feather function in the theropod-avian lineage. Though skeletons and feathers are the common link between extinct and extant theropods and figure prominently in discussions on flight performance (extant birds) and flight origins (extinct theropods), skeletal inter-workings are hidden from view and their functional relationship with aerodynamically active wings is not known. For the first time, we use X-ray Reconstruction of Moving Morphology to visualize skeletal movement in developing birds, and explore how development of the avian flight apparatus corresponds with ontogenetic trajectories in skeletal kinematics, aerodynamic performance, and the locomotor transition from pre-flight flapping behaviors to full flight capacity. Our findings reveal that developing chukars (<i>Alectoris chukar</i>) with rudimentary flight apparatuses acquire an “avian” flight stroke early in ontogeny, initially by using their wings and legs cooperatively and, as they acquire flight capacity, counteracting ontogenetic increases in aerodynamic output with greater skeletal channelization. In conjunction with previous work, juvenile birds thereby demonstrate that the initial function of developing wings is to enhance leg performance, and that aerodynamically active, flapping wings might better be viewed as adaptations or exaptations for enhancing leg performance.</p></div>", "links"=>[], "tags"=>["volant adult birds", "leg performance", "flight capacity"], "article_id"=>3195613, "categories"=>["Medicine", "Neuroscience", "Evolutionary Biology", "Environmental Sciences not elsewhere classified", "Ecology", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Developmental Biology", "Infectious Diseases"], "users"=>["Ashley M. Heers", "David B. Baier", "Brandon E. Jackson", "Kenneth P. Dial"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0153446.s001", "https://dx.doi.org/10.1371/journal.pone.0153446.s002", "https://dx.doi.org/10.1371/journal.pone.0153446.s003", "https://dx.doi.org/10.1371/journal.pone.0153446.s004", "https://dx.doi.org/10.1371/journal.pone.0153446.s005", "https://dx.doi.org/10.1371/journal.pone.0153446.s006"], "stats"=>{"downloads"=>1, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Flapping_before_Flight_High_Resolution_Three_Dimensional_Skeletal_Kinematics_of_Wings_and_Legs_during_Avian_Development/3195613", "title"=>"Flapping before Flight: High Resolution, Three-Dimensional Skeletal Kinematics of Wings and Legs during Avian Development", "pos_in_sequence"=>1, "defined_type"=>4, "published_date"=>"2016-04-21 06:02:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001373"], "description"=>"<p>Locomotor ontogeny provides key functional, ecological, and evolutionary insight into the avian body plan, by revealing how transitional, morphing anatomies function. (A) From a functional perspective, adult birds are the endpoints of an ontogenetic and evolutionary continuum and cannot clearly elucidate how specific morphological attributes affect to the ability to become airborne. Nearly all adult birds share a suite of specialized morphologies, are flight-capable or secondarily flightless, and may not provide enough variation in morphology and flight capacity to expose relationships between these two variables (though adult birds of some species fly poorly [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref062\" target=\"_blank\">62</a>], they have not been studied). In a traditional, adultocentric framework that perceives many morphological features as aptations for aerial locomotion, most relationships between form and locomotor function are therefore assumed rather than empirically tested. (B) Juvenile birds have rudimentary locomotor structures, and engage in pre-flight flapping behaviors as they morph into adulthood and acquire flight capacity. Though poorly studied [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref007\" target=\"_blank\">7</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref057\" target=\"_blank\">57</a>], morphing juveniles fill a longstanding gap in knowledge and help clarify functional attributes of the avian body plan. By revealing form-function relationships that underlie obligately-bipedal to flight-capable transitions (i-iv), and thereby establishing how features are related to flight, developing birds can provide key insight into locomotor aptations. (C) For example, previous work has shown that juvenile chukars with rudimentary flight apparatuses (image i) transition from leg- to wing-based modes of locomotion by using their legs and wings cooperatively, and generating small but important amounts of aerodynamic force (iii, data from [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref018\" target=\"_blank\">18</a>]) that increase throughout ontogeny and allow birds to flap-run up steeper obstacles and eventually fly (iv, data from [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref020\" target=\"_blank\">20</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref053\" target=\"_blank\">53</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref055\" target=\"_blank\">55</a>,<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref061\" target=\"_blank\">61</a>]). Here, we quantify the ontogeny of skeletal kinematics (ii), to better understand relationships between form, function, performance, and behavior. Image i in (C) reprinted from [<a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.ref010\" target=\"_blank\">10</a>] under a CC BY license, with permission from Cell Press, original copyright 2012.</p>", "links"=>[], "tags"=>["volant adult birds", "leg performance", "flight capacity"], "article_id"=>3195802, "categories"=>["Medicine", "Neuroscience", "Evolutionary Biology", "Environmental Sciences not elsewhere classified", "Ecology", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Developmental Biology", "Infectious Diseases"], "users"=>["Ashley M. Heers", "David B. Baier", "Brandon E. Jackson", "Kenneth P. Dial"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153446.g002", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Relationships_between_form_function_performance_and_behavior_/3195802", "title"=>"Relationships between form, function, performance, and behavior.", "pos_in_sequence"=>3, "defined_type"=>1, "published_date"=>"2016-04-21 06:02:53"}
  • {"files"=>["https://ndownloader.figshare.com/files/5001394"], "description"=>"<p>r<sub>s</sub>: Spearman’s rank correlation coefficient; A-J: adult mean–juvenile mean; x, y, z: joint rotations shown in Fig C (z, top row: elevation-depression (shoulder) or flexion-extension (elbow, wrist); y, middle row: protraction-retraction (shoulder) or abduction-adduction (elbow, wrist); x, bottom row: long axis rotation); avg (average), max (maximum), min (minimum), and range: kinematic variables tested for statistical significance (Table E in <a href=\"http://www.plosone.org/article/info:doi/10.1371/journal.pone.0153446#pone.0153446.s001\" target=\"_blank\">S1 File</a>).</p>", "links"=>[], "tags"=>["volant adult birds", "leg performance", "flight capacity"], "article_id"=>3195823, "categories"=>["Medicine", "Neuroscience", "Evolutionary Biology", "Environmental Sciences not elsewhere classified", "Ecology", "Astronomical and Space Sciences not elsewhere classified", "Biological Sciences not elsewhere classified", "Developmental Biology", "Infectious Diseases"], "users"=>["Ashley M. Heers", "David B. Baier", "Brandon E. Jackson", "Kenneth P. Dial"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0153446.g003", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/Ontogenetic_trends_and_differences_between_adults_and_juveniles_flap_running_up_60_65_inclines_forelimb_kinematics_/3195823", "title"=>"Ontogenetic trends and differences between adults and juveniles flap-running up 60–65° inclines: forelimb kinematics.", "pos_in_sequence"=>4, "defined_type"=>1, "published_date"=>"2016-04-21 06:02:53"}

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{"start_date"=>"2016-01-01T00:00:00Z", "end_date"=>"2016-12-31T00:00:00Z", "subject_areas"=>[]}
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