antipodolycaena includes four species that are endemic to new zealand : lycaena boldenarum white , 1862 ( type species ) lycaena feredayi ( bates , 1867 ) lycaena rauparaha ( fereday , 1877 ) lycaena salustius ( fabricius , 1793 )

antipodolycaena

antipodolycaena is a subgenus of the genus lycaena which is found only in new zealand . antipodolycaena includes four species that are endemic to new zealand :
how can i put and write and define antipodolycaena in a sentence and how is the word antipodolycaena used in a sentence and examples ? 用antipodolycaena造句 , 用antipodolycaena造句 , 用antipodolycaena造句 , antipodolycaena meaning , definition , pronunciation , synonyms and example sentences are provided by ichacha . net .
robert : hi robin , thank for your clarification on these matters . there is certainly great confusion on the genus naming of admirals & coppers . confusion regarding blues is not as bad , but is still there too . any chance you can point me to the relevant articles by for the vanessa ( field ) & zizina genus ' ? as i would like to read through them . as for the genus lycaena , i have a copy of the russians work ( * see quote ) , but have never heard of antipodolycaena being used , this is news to me . any chance this is to do with smart , p . 1975 : the international butterfly book . n . y . : thomas c . crowell . ? quote * on the systematics of the genera lycaena f . and heliophorus geyer ( lepidoptera : lycaenidae ) by ab zhdanko , institute of zoology , kazakhstan national academy of sciences , alma - ata . english publication in entomological review , 75 ( 9 ) , 1996 . 595 . 789 take care , robert .
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type - species : lycaena boldenarum white , 1862 . trans . r . ent . soc . lond . ( 3 ) , 1 : 26 . [ bhl ]
type specimens : ? type status new zealand : ? locality , ( ? depository ) . .
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robert : quote from : copper on ( 10 aug 2010 ) tue 09 : 30 pm there is no evidence of hybridization between southern and common blue blues in new zealand . i have updated the common & southern blue pages urltoken & urltoken from ; quote in the areas where both the common & southern blue hybridise , like north canterbury & the waiho gorge . these hybrids are extremely viable in pattern on the underwing ( which makes the females impossible to tell apart & the males need close inspection of their genitals to tell ) . to ; quote there are rumours of hybridisation between the common & southern blue in north canterbury & the waiho gorge , however there has being no published evidence of this . for the time being , i ' m going to leave the boulder copper page alone as i have it as lycaena ( boldenaria ) boldenarum & refer to boldenaria as a sub - genus . i put it this way after reading the kazakhstani article i mentioned above as it concluded this same answer . robert .
copper : yes its quite ok to use boldenaria as ` a subgeneric name ; the zizina article is accessible on google scholar and was published in zootaxa 2008 ; the field revision was published in early 1970s in smithsonian contributions to zoology .
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osedax roseus is a species of bathypelagic polychaete worm that lives at abyssal depths and is able to sustain itself on the bones of dead whales .

the species is found in the north east pacific .

osedax roseus

figure 3a from rouse et al . 2008 , whale vertebrae covered in osedax roseus ( arrows ) .
acquisition of dwarf male “harems” by recently settled females of osedax roseus n . sp . ( siboglinidae ; annelida )
“… . receive your own plush , 100 % cotton dwarf male osedax roseus , complete with hooked chaetae… . ”
acquisition of dwarf male
harems
by recently settled females of osedax roseus n . sp . ( siboglinidae ; annelida ) .
figure 3 . mature female osedax roseus colonizing a whale bone . a larvae that lands on her will differniate into a male .
figure 4 . anatomy and size comparison of male and female osedax roseus . not the stark difference in size and morphology between the two sexes .
acquisition of dwarf male
harems
by recently settled females of osedax roseus n . sp . ( siboglinidae ; annelida ) . - pubmed - ncbi
both bonellia viridis and osedax roseus have similar biological mechanisms designs to facilitate environmental sex determination . a sexually undifferentiated larvae becomes male after contact with an adult female . if the larvae don’t interact with a female , then they differentiate into a female themselves . there are different environmental conditions that trigger sexual differentiation .
fish bone ( gzg . v . 20407 ) with osedax borings from the presumably late oligocene part of the makah formation , washington state , usa
um die evolutionsgeschichte des marinen , knochenfressenden wurms osedax zu verstehen , ist es wichtig zu wissen , zu welchen tiergruppen die knochen gehören , die er fressen kann . ursprünglich wurde osedax als wal - spezialist angesehen , weitere untersuchungen zeigten jedoch , dass er ein breites spektrum an wirbeltierresten , inklusive weichteile von walen und knochen von vögeln und fischen , konsumiert . hier werden zum ersten mal bohrspuren in walzähnen und fischknochen aus oligozänen tiefwasserablagerungen der makah , pysht und lincoln creek formationen im westen des us - bundesstaates washington dokumentiert , die solchen des rezenten osedax stark ähneln . die fossilien wurden mittels verdünnter säure aus kalkigen konkretionen herausgelöst und die bohrspuren wurden computer - tomographisch untersucht . diese und bereits bekannte bohrspuren von osedax aus dem westlichen washington zeigen , dass osedax schon im oligozän die gleiche bandbreite von wirbeltierresten besiedelt hat wie heute und auch die gleiche vielfalt an weichkörpermorphologien . diese ergebnisse stützen die these , dass ein breites nahrungsspektrum ein ursprüngliches merkmal von osedax ist .
osedax has a known depth range of 30–3000 m ( 7 ) and can be found in dense colonies that are able to consume an entire whale skeleton within a few years ( 19 ) . molecular clock estimates and the early oligocene boreholes presented here show that osedax has been destroying bones for most of the evolutionary history of whales . osedax has an impact on the taphonomy of whale skeletons that has significantly affected the quantity and especially the quality of fossil whales , as documented here . this previously unrecognized “ osedax effect” is especially well - illustrated in whale fossils that are preserved in deep - water strata where sedimentation rates are low , such as the bioeroded fossils from washington state .
rouse , g . w . ; worsaae , k . ; johnson , s . b . ; jones , w . j . ; vrijenhoek , r . c . 2008 . acquisition of dwarf male
harems
by recently settled females of osedax roseus n . sp . ( siboglinidae ; annelida ) . biol bull 214 ( 1 ) : 67 - 82 . , available online at urltoken [ details ]
rouse , g . w . ; worsaae , k . ; johnson , s . b . ; jones , w . j . ; vrijenhoek , r . c . 2008 . acquisition of dwarf male
harems
by recently settled females of osedax roseus n . sp . ( siboglinidae ; annelida ) . biol bull 214 ( 1 ) : 67 - 82 . , available online at urltoken page ( s ) : 71 [ details ]
teeth of two mysticete whales with osedax borings , oligocene , washington state , usa . a , b two teeth ( gzg . v . 20408 ) from the latest oligocene part of the lincoln creek formation . these were used for micro - ct ; renderings in fig . 3 are from specimen a . c – e three teeth ( usnm 539938 ) from the late early oligocene part of the pysht formation . note that osedax borings are restricted to the upper ( presumably exposed ) part of the teeth in c and d and that the broken edges in specimen e are angular and do not go through obvious osedax borings
zombie worms ( osedax roseus ) eat away at the bones of a dead whale that has fallen to the seafloor in sagami bay , japan . these bizarre worms rely on whale bones for energy and are what scientists call “sexually dimorphic”—the male and female forms are markedly different . in this case , the males are microscopic and live inside the bodies of the female worms ! this allows females to produce many , many eggs to disperse across the seafloor . few of these will land close enough to sunken bones to survive .
heck , i’ll pay $ 20 to the first knitter to put up the design for an anatomically correct osedax with a dwarf male ! plus i’ll pay for the shipping to have it . any takers ? i can email you the article .
a significant part of osedax’s diet is digesting the bones of whales . however , whale bones are difficult to find in the ocean . sexually undifferentiated larvae float in the ocean searching for whale bones , and conserving energy until they find their next meal . some people have called this their “zombie state” . once a bone is found , contact with a whale bone triggers the larvae to differentiate into a female ( rouse , 2008 ) . this process is accompanied by an increase in the body mass and anchoring their body into the bone by boring holes to start building a colony on the bone . sexual differentiation takes energy , so this processes does not occur until the osedax has found a food source .
we thank eva vinx ( universität hamburg ) for aid with photography , bob vrijenhoek ( monterey bay aquarium and research institute ) for inviting g . w . r . on cruises to collect live osedax , and gerardo gonzález - barba ( universidad autónoma de baja california sur ) for identifying fossil shark teeth . we also thank bob vrijenhoek and two anonymous reviewers for their efforts to improve the manuscript .
after the osedax have built a colony and females are extracting nutrients from the bone , sexually undifferentiated larvae that land on a female will differentiate to become a male . the larvae enters the female’s tube lumen . researchers are unclear about how the males find the tube lumen , the molecular triggers that facilitate the development of male sexual characteristics , and the role that hormones released by females may play in this process . that researcher still don’t understand . there is a preference for larger females , and increased size of a female is correlated with more dwarf males in their tube lume . ( rouse , 2008 ) .
as it is an annelid , i am fond of osedax . but i am disappointed . and i ' m calling it : this is the first definively - not - a - parasite - of - the - day in a long unbroken record of parasites of the day . you can ' t be a parasite of a dead thing , lest we include hagfish , cookie sleeper sharks , and osteopelta limpets from whale - fall ; or even the myriad and sundry critters that feed on other dead animal carcases . as foul as all of this may be , still i cry
foul
on parasite of the day .
osedax borings in a tooth of a mysticete whale from the latest oligocene part of the lincoln creek formation , washington state , usa ( gzg . v . 20408 ; same specimen as in fig . 2a ) . a–d micro - ct scan images showing cross sections with cavities and their entry holes ; arrow indicating the entry hole to the boring visualized in figs . e and f . e , f micro - ct - based rendering of the trace fossils indicated in fig . d , bone material in gray , and borehole in yellow . e the complete trace fossil seen from the top ( nearly the same orientation as in a–d ) . f longitudinal cross section through the trace fossil
osedax borings in a fish bone from the presumably late oligocene part of the makah formation , washington state , usa ( gzg . v . 20407 ; same specimen as in fig . 4 ) . a–c micro - ct - based rendering of a trace fossil , bone material in transparent blue , flower - like borehole in yellow , showing a vertical cross section including the entry hole ( a ) , the jagged underside ( b ) and a top view with the circular entry hole on the bone’s surface ( c ) . d , e micro - ct images showing the same cross section as in a ( d ) and a cross section with two borings including their entry holes ( e )
the x - ray microcomputed tomography scans of the whale bone that contains the traces of osedax was done using the skyskan1172 system ( skyscan ) at the institut für geowissenschaften , christian - albrechts - universität , kiel , germany . the fossilized bone was scanned with a beam energy of 100 kv , a flux of 100 μa , and a 0 . 5 - mm - thick aluminum filter at a detector resolution of 8 . 7 μm / pixel using a 180° rotation with a step size of 0 . 6° . to study cavity morphology details , a second scan under identical beam conditions was performed , using a 360° rotation with a step size of 0 . 45° at a detector resolution of 8 . 0 μm .
cavity morphology in early oligocene rib fragment ( usnm 539939 ) . ( a ) reconstructed image of a ct scan through holes 1 and 3 in fig . 1 a and e . note destroyed trabecular bone just below the left borehole . ( b ) micro - ct–based rendering of a cavity in solid bone ; only a single borehole leads into it , and it is assumed to have been excavated by a single individual of osedax . note the difference between the long and thin vascular canals and the thicker and more irregularly shaped root lobes . ( c ) reconstructed image of a ct scan of the same cavity as in b ; the three small , elliptical holes in the upper half are vascular canals . ( d ) micro - ct–based rendering of another cavity in solid bone . b , borehole on bone ' s surface ; rl , root lobe ; sb , solid bone ; tb , trabecular bone ; vc , vascular canal of the bone .
read , g . ; fauchald , k . ( ed . ) ( 2018 ) . world polychaeta database .
rouse , worsaae , johnson , jones & vrijenhoek , 2008 . accessed through : world register of marine species at : urltoken ; = 588636 on 2018 - 07 - 09
is commonly known as the
bone worms
, although some endearingly call them
zombie worms
as well . these marine polychaete worms were discovered only in 2002 in the deepest parts of monterey bay , california . what were they doing ? if you guessed
parasitizing zombies
, you ' d be sadly wrong . you should put down your comic book and pick up
. if you guessed eating bones from dead whales , you ' d be correct ( you should continue reading also in case there are more gratifying questions to come ) . the animals were
rooted
( like tiny trees ) into the bones and a large
trunk
of the animal above the bone waving in the current .
so at this point you ' ve figured out that they ' re not a whale parasite because the whale is seriously ' belly - up ' at this point . so
is in fact a decomposer . but when rouse took a close look at these worms , he found that they appeared to have no guts whatsoever . so where were they getting their nutrients ? being an expert on marine polychaetes he knew that some deep sea worms had the ability to garner bacteria that derive nutrients from geochemical vents or seeps . as it turns out
was doing something very similar . inside the
roots
of the animal , which are inside the whale bone , the bacteria are helping to digest the yummy fats left by the whale .
you ' d need to turn off the television and pick up a book . if you guessed ,
living as a harem inside the body of the female
you ' d be correct ! rouse initially thought these microscopic
bags of sperm
were parasitic ( yeah ! ) inside the females , surviving on the nutrients she and her endosymbiont bacteria were producing . however , at closer examination they appear to actually be larvae that never develop feeding structures at all , just living off the yolk for the egg sac . never the less , they are able to provide sperm to fertilize the female ' s eggs !
ok , i know what you ' re thinking ,
its icky and it not even a parasite , why am i still reading ? ” because it ' s fascinating ! survival in a vast ocean where there are relatively few dead whales on which to live is a tricky thing ; reproduction is even trickier . the
dwarf males
can disperse over large distances , because the only part of the life cycle that isn ' t attached to a whale bone is the larva . rouse thinks that the sex is environmentally determined : if larvae land on a bone , they become a female , if they land on a female , they become male . if this species only relied on a male settling next to a female to breed , it would seriously diminish the gene pool .
is icky and but it ' s not a whale parasite , though the males are sort of parasites of the females . . . so it is completely fascinating !
has evolved surprising and strange means to eke out an existence at the bottom of the sea where few organisms ( even zombies ) fear to tread .
see also : rouse et al , 2008 . acquisition of dwarf male
harems
by recently settled females of
one more thing , the
males are sort - of parasites of the females
no more than are gestating offspring .
i ' m standing by this . not only is it a cool invert , but i think that these little males , living solely within and living off their mate ' s nutrients and protective body constitutes a parasite enough ( more sexual parasites are coming ) . and , besides , it ' s all about celebrating diversity , especially the fact that we ' re still discovering really wacky and interesting critters every day .
i don ' t check this blog for a few days and what do we have here ? there ' s certainly no shortage of whale parasites to warrant throwing in the famous
bone - eater
here . while i am somewhat disappointed by this , i suppose if one is to look for legal loopholes , you can always say it ' s about the symbionts that live in that worm ' s rootlets . . . even then they are technically mutualists . . . perhaps we can make a bonus double - parasite day in the future to make up for this - there is absolutely no shortage of fascinating * parasites * . . .
i still like this . it ' s not as though
parasite
is a monophyletic group , after all . and yes , tommy - many of the entries pack enough parasite in their punches ( how ' bout them p ' s ? ) to warrant highlighting a cool worm that can drill into bones and suck out the fat !
i just came across this site . great blog . parasites interest me . don ' t know why but either gross - out or evolution factor . another evolution - related interest is the deep sea so i thought i ' d point out on some female anglerfish what was thought to be a parasite was actually a male anglerfish . urltoken urltoken
no they don ' t - to be honest this was the only time on this blog when we featured a creature that wasn ' t actually a parasite ( see the debate above ) . these worms only colonise the bones of carcasses - and carcasses in the deep sea for that matter - so no , they won ' t be present in a human bones .
no tiago . please refer to the discussion above your comment - it ' s not even really a parasite - see the comment by mark siddall .
hint : you ' re just looking at the tip of the iceberg . . .
if you think you or your pets have a parasite , please seek the appropriate care you need from your own doctor or veterinarian .
why parasite of the day ? ( if it ' s not every day . . . )
the united nations declared 2010 the international year of biodiversity . in celebration of the enormous diversity of parasites and to highlight their importance , we created this blog , which showcased a species of parasite every day . now that 2010 is over , we will continue to add more parasites from time to time , and write about any newly published research on parasite species that we have posted about yet .
see this post from the start of 2011 where we discuss the sheer scale of parasite biodiversity , and this post from the end of 2011 pretty much summarizes the mission of this blog .
got parasites ? the american society of parasitologists is interested . we invite you to share with us your observations , ideas and questions about parasites . our members and the journal of parasitology represent a wide range of research interests including ecology , evolution , systematics , immunology , biochemistry and molecular biology . please post any aspect of parasitology you wish to share with us on our facebook group page . please go to our home page at
bush , albert , gerald esch and jacqueline fernandez . parasitism : the diversity and ecology of animal parasites . cambridge university press .
combes , claude . the art of being a parasite . university of chicago press .
desowitz , robert . new guinea tapeworms and jewish grandmothers . norton & company .
desowitz , robert . the malaria capers : tales of parasites and people . norton and compay .
moore , janice . parasites and the behavior of animals . oxford university press .
zuk , marlene . riddled with life : friendly worms , ladybug sex , and the parasites that make us who we are . mariner books
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rouse gw 1 , worsaae k , johnson sb , jones wj , vrijenhoek rc .
scripps institution of oceanography , 9500 gilman drive , la jolla , california 92093 - 0202 , usa . grouse @ urltoken
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an adult bonellia viridis female excretes the signaling hormone bonellin ( figure 1 ) to attract larvae ( malard , 2013 ) . bonellin is found only in females , and is also a biocide that kills prey that the worm eats . it’s most important role is to signal that a female is ready to mate . being in the presence of bonellin attracts the undifferentiated larvae to enter a hole in the female’s proboscis .
figure 1 . the chemical structure of bonellin , the signaling horomone that regulates the feeding and reproductive habits of bonellin .
once inside the proboscis , the larvae travels toward a tube filament in female’s uterus , which has been affectionately called the “little man room” . ( gauthier , 1983 )
the larvae experiences physiological changes to differentiates into a male like developing gonads that allow him to start producing sperm to fertilize the female’s eggs . more research is needed to understand the specific genes that are activated to allow the larvae to transition from an undifferentiated sex to a male . in exchange for fertilizing the female’s eggs , the male receives protection from predators and a steady food source by living inside the female .
figure 2 . the male bonellia viridis lives inside the tube lumen of the mature female .
edited by robert c . vrijenhoek , monterey bay aquarium research institute , moss landing , ca , and accepted by the editorial board march 19 , 2010 ( received for review february 22 , 2010 )
) , depending on the rate used , but these estimates have not yet been corroborated by fossil evidence .
) . the symbionts are housed mainly in tissue that forms a “root system” extending into the bone . the action of the roots and associated bacteria results in the destruction of the bone interior . the roots are connected to the main body of the worm that emerges from the bone via a circular hole on the bone surface (
in the geologic past . here we report oligocene whale bones that show such traces .
the scan to survey the rib fragment ( 326 transmission images ) was reconstructed in a 1 , 832 × 900 matrix of 2 , 029 slices with a resolution of 8 . 7 μm / voxel using the skyscan software nrecon running on a cluster of three networked pcs . the program uses a modified feldkamp algorithm . the segmentation of bone and boreholes was done with the skyscan software ct analyzer . before the subsequent generation of the 3d models by adaptive rendering , the data sets were downsized to one - third with an isotropic voxel resolution of 26 . 0 μm in a 610 × 300 matrix of 677 slices . visualization of the 3d models was done by the skyscan software ctvol . for the study of cavity morphology details , 800 transmission images were reconstructed in a 2 , 088 × 1 , 136 matrix of 1 , 998 slices . segmentation and rendering were done on volumes of interest with a resolution of 8 . 0 μm / voxel .
author contributions : s . k . designed research ; s . k . and j . l . g . performed research ; w . - a . k . and g . w . r . analyzed data ; and s . k . , j . l . g . , w . - a . k . , and g . w . r . wrote the paper .
this article is a pnas direct submission . r . c . v . is a guest editor invited by the editorial board .
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researchers used field data from 2012 to 2015 to study mortality and allele frequency changes in the sea star pisaster ochraceus during a mass mortality event in northcentral california , and found that surviving adult and juvenile sea stars experienced 81 % mortality and allele shifts , according to the authors .
a survey of more than 4 , 600 american adults conducted in 1995 - 1996 and in 2011 - 2014 suggests that among individuals of low socioeconomic status , negative affect increased significantly between the two survey waves , whereas life satisfaction and psychological well - being decreased .
a study of cognitive ability in norwegian males born from 1962 to 1991 suggests that environmental factors rather than changing genetic composition of families likely account for most of the change in norwegian population iq .
the mathematical tools behind recent gerrymandering cases have brought a modicum of precision into the political arena—but this rigor hasn’t always been enough to spur policy changes .
these chicas are freaky . but if you lived on a whale vertebrae and eat through bone , perhaps you’d be a little on the kinky side too , right ?
, the “bone - devouring” worm is weird . now , i know long time deep sea news readers will be a little used to us talking about odd critters in the ocean , maybe you’ve come to expect it and are no longer shocked . we have even
. but this is one critter that would infuse the pope with fear and disgust .
, complete with hooked chaetae ( see photo below ) while supplies last . what is really cool is that all whale bone - eating worms appear to have dwarf males .
“mature sperm gather anteriorly in the body of the male and a sperm duct runs into the head ( fig . 7c ) , where sperm presumably exit the body” .
yep , the dwarf males of the bone - eating worms jizz out of their heads . disgusting . its like puking up your sperm or impregnating your wife by spitting on her ovaries .
fig . 7b : “differential interference contrast micrograph of male , 172 μm showing three of the posterior hooks and an anterior ( putative ) prototroch . early spermatids or spermatogonia are visible anterior to later spermatids . ”
) males fruiting around inside of a female in what is akin to an internal bukkake - fest with the female enthralled in her detestable orgy , covered in the love ooze of her harem . in fact , rouse
. followed the worms through time and found that the larger , older ladies had a larger harem size . i wonder what the relationship between male size and female age is . are males smaller in younger , smaller females or is there no detectable difference in male size ( or sperm output / spermatozoa size ) across all size ranges / ages of females ?
“many … males fruiting around inside of a female in what is akin to an internal bukkake - fest with the female enthralled in her detestable orgy , covered in the love ooze of her harem . ”
“its like puking up your sperm or impregnating your wife by spitting on her ovaries . ”
oh my goodness ! i certainly was not expecting to run across that when i checked the scienceblogs this morning .
so the males live inside the female on top of everything else ? what is it with deep sea living and parasitic males ? so polyandrous , dead whale bone eating , parasitic males… . kinkiest species ever !
er…looking at the micrographs in the paper and roughing the dimensions , this one would be hard for a knitter to pull off keeping them roughly to scale with each other . since he’s such a tiny wimp comparatively… 1 / 60 to 1 / 80th of her size . either the female would be 6m long for a 2cm male or the male would be only a few knots for a 20cm female .
i can’t help with the knitting but i’d certainly add my $ 20 to kevin’s . please note kevin said “anatomically correct” which doesn’t necessarily mean to scale !
the views , opinions , and language of kevin zelnio do not reflect the views , opinions , and language of deep - sea news , its sponsors , … .
i throw in some money if somebody wants to make me one too . in reality i have always wanted a crouchet giant isopod . any takers ? where is ellie ( urltoken ) at ?
yes i’m serious . i’ll write you a check or via paypal , $ 20 to put the designs up on the web for anyone to use . we can put it up here at deep sea news if you don’t have a website or blog of your own . i want a female bone - devouring worm with dwarf male . dwarf male must have hooked chaetae and females must have all typical zombie worm appearances . i can envision maybe a flap you can turn that reveals the dwarf male attached to the female’s oviduct ? lol
not quite what you’re asking for . . . but here are a couple of marine animal knitters :
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are marine annelids with the ability to exploit bones on the seafloor for nutrition , presumably by living in symbiosis with collagenolytic bacteria ( rouse et al .
is able to exploit has been the matter of a controversial debate ( glover et al .
) because it has an important implications for its origin , diversification and dispersal . most
pointed to an eocene origin , coincident with the rise of whales ( rouse et al .
can colonize other substrates as well , including spermaceti , soft tissue and blubber of whales ( fujikura et al .
had to have the ability to consume substrates other than whale bones , at least early in its evolutionary history . here we document traces of
in fossil whale teeth and fish bones from oligocene deep - water sediments in western washington state , usa ( fig .
traces in oligocene whale and bird bones from this area ( kiel et al .
fossil locality map . a sekiu river ( uwbm loc . c1660 ) . b murdock creek ( lacmvp loc . 5412 ) . c knappton ( lacmvp loc . 4510 )
gzg : geoscience museum , university of göttingen , germany . lacm : natural history museum of los angeles county , invertebrate ( ip ) and vertebrate ( vp ) paleontology sections , los angeles , ca , usa . usnm : smithsonian natural history museum , washington , d . c . , usa . uwbm : university of washington , burke museum , seattle , wa , usa .
a jaw fragment including several teeth ( gzg . v . 20408 ) , possibly from a small , toothed mysticete whale , was collected in a concretion on the north shore of the columbia river , pacific county , washington state , usa , in the northern part of the bay between grays point and knappton , in the latest oligocene ( prothero et al .
) part of the lincoln creek formation . the locality is in section 9 , t9 n , r9 w , knappton quadrangle ( usgs ) , 7 . 5 min series , 1949 ( photo revised 1984 ) , pacific county , washington ; this is lacmvp locality 4510 . the sediments in this area were deposited in water depths between 300 and 900 m based on benthic foraminifera ; estimates based on mollusk and fish assemblages give slightly shallower depths ( moore
) . bones and teeth were etched from the concretion using dilute ( 5–10 % ) formic acid ; two teeth were used for micro - ct analysis .
further whale teeth are from a small , toothed mysticete ( usnm 539938 ) from the late early oligocene part of the pysht formation . we have previously reported
borings from a rib fragment and other bones of this specimen ( kiel et al .
) . it was collected on the beach terrace east of murdock creek in clallam county , washington state , usa ( lacmvp loc . 5412 and lacmip loc . 6295 ) , from deep - water sediments that are well - known for their vertebrate fossils , mostly whales ( goedert et al .
) , citing local and regional problems with the biostratigraphy and magnetostratigraphy , have shown it simply as oligocene .
another cetacean specimen ( uwbm 95841 ) in which the teeth show boreholes is from the late oligocene part of the makah formation , from the same area as the fish bones described herein ( uwbm loc . c1660 ) . it consists of a fragment of a nodule with a skull fragment and either a fragment of dentary or maxilla , or both , and at least six teeth . it is possibly part of a toothed mysticete , and the roots of two of the teeth show the same curve and posterior extension as the tooth from usnm 539938 in fig .
the x - ray micro - computed tomography scans of the fish bone fragment ( gzg . v . 20407 ) and the two whale teeth ( gzg . v . 20408 ) were done using the skyskan1172 system ( skyscan , belgium ) . the fossil fragments were scanned with a beam energy of 100 kv , a flux of 100 μa , and a copper–aluminum filter at a detector resolution of 7 . 45 μm per pixel using a 360 - degree rotation with a step size of 0 . 6 degrees . the scan to survey the specimen ( 600 transmission images ) was reconstructed in a 3 , 124 × 3 , 600 matrix of 3 , 408 slices with a resolution of 7 . 45 μm per voxel using the skyscan software nrecon running on an intel - based macintosh computer employing the multi - boot utility boot camp . the program nrecon uses a modified feldkamp algorithm . the segmentation of bone / tooth and boreholes was done with the skyscan software ct analyzer . for the study of cavity morphology details of the fish bone , a volume of interest in a 1 , 471 × 1 , 609 matrix of 1 , 851 slices was chosen . cavities inside the whale tooth were studied in a volume of interest in a 1 , 524 × 1 , 998 matrix of 2 , 801 slices . visualization of the 3d models was done by the skyscan software ctvol .
the jaw fragment from lacmvp loc . 4510 near knappton was heavily corroded before being fossilized ; the associated teeth have their crowns corroded away , and also the roots show strong traces of corrosion ( fig .
a , b ) . boreholes are mostly circular with sharp edges , have diameters up to 0 . 5 mm , although most are smaller , and are concentrated on the upper half of the teeth but are also present on the lower half . micro - ct scans show that the boreholes penetrate the teeth to a depth of about 0 . 5 mm or more before they start to broaden or to branch in various directions ; the maximum length of individual cavities is around 3 mm ( fig .
) . similar boreholes were seen on the surfaces of three teeth and two tooth roots from a toothed mysticete ( usnm 539938 ) from lacmvp loc . 5412 at murdock creek ( fig .
c , d ) . as in the sample from knappton , the borings are restricted to the upper half of the teeth , have sharp edges , two reach 0 . 5 mm in diameter , but most are smaller than 0 . 3 mm . a few such boreholes are also seen on the crown , typically in areas that also show traces of physical abrasion ( or wear ) , for example , at tips of the cusps of the teeth . bones , possibly part of a toothed mysticete ( uwbm 95841 ) from the late oligocene part of the makah formation ( uwbm loc . c1660 ) , were strongly corroded before being fossilized , and the teeth that are well exposed because of weathering ( additional preparation has not been done ) all show some borings . in two teeth that are exposed in cross section , the entire crown has been destroyed , with borings down into the root as well .
the preserved surface of the micro - ct scanned fish bone fragment shows 28 holes with a diameter > 0 . 1 mm and at least another 15 holes with an often considerably smaller diameter ( fig .
) . most holes are nearly circular and have sharp edges , and the micro - ct scans show that these boreholes lead through a short tunnel into cavities within the bone ( fig .
) . the cavities are of various shapes including shallow - radiating ( fig .
) , branching , or like clusters of grapes , and they are frequently , but not always , interconnected . the figured single cavity reaches a width of 6 . 5 mm and a depth of 2 mm .
in modern and fossil bones typically show a short tunnel leading from a circular hole in the surface of the bone into a cavity in the interior of the bone ( fujikura et al .
) ; this characteristic can also be seen in the traces documented here . while
often colonizes bones in such dense aggregations that their root systems form large cavities inhabited by many individuals , cavities with only a single borehole leading into them ( single cavities ) are thought to reflect the shape of the root system of an individual animal and are thus of particular diagnostic value ( kiel et al .
, bottom of their fig . 6b ) and to cavities documented from a pliocene whale in italy ( higgs et al .
borings . however , the shape of the root system can vary significantly within species and appears to be controlled mainly by differences in bone structure ( kiel et al .
) , makes rock - boring sponges the more likely candidate for these borings . although we did indeed find only interconnected cavities with multiple boreholes leading into them in the bird bones , this does not exclude
) . such high borehole densities are thus an invalid argument for reinterpretation of the borings seen in the oligocene bird bones as sponge borings . furthermore , mollusk shells collected at the same locality as the bored bird bones ( e . g . , squires and goedert
’ - type borings . it seems unlikely to us that rock - boring sponges would colonize bird bones but not the co - occurring mollusk shells .
, however , would certainly show such a behavior . therefore , we maintain our view that the boreholes in the oligocene bird bones were made by
species found at 1 , 000 m depth in monterey canyon colonized a turkey carcass deployed roughly 10 m from an existing whale - fall ( r . c . vrijenhoek , pers . comm . 2012 ) .
many of the whale teeth have their crowns corroded away . this may seem strange considering that they are made of hard enamel ( calcium phosphate with little organic matrix ) , whereas the root is covered by a thin layer of softer cementum ( maas
) and should therefore be easier to attack . however , the enamel is very thin on these teeth , and a specimen where the crown is corroded but not totally destroyed shows that the broken edges are straight or angular , but do not go through any of the few boreholes ( fig .
) . a similar scenario seems possible for the corroded teeth : boreholes are concentrated just underneath the crown , indicating that the teeth were attacked while still in situ . thus , if some predator had attacked the
specimens that had colonized the enclosing jaw bone , the thin crown could have been broken as ‘collateral damage . ’ the common scratch marks in this area ( fig .
was reported from the teeth of sperm whales ( suborder odontoceti ) that were sunk off the coast of japan ( fujiwara et al .
) after a mass stranding event . interestingly , in the vertebrate remains from the oligocene strata in western washington , we have so far not observed
borings in bones or teeth positively identified as being from odontoceti ( e . g . , barnes and goedert
, as well as those in bones from oligocene deep - water sediments in western washington previously reported by us ( kiel et al .
) , exhibit a wide variety of shapes , including radiating and flower - like , grape - like and irregular - branching , and they frequently merge to form large cavities with multiple entry holes . this diversity of shapes does not necessarily imply species diversity , but shows that the morphological diversity seen in the root systems of extant
) was already developed by the oligocene time . similarly diverse as the shape of the root system of
is the range of substrates that it was able to colonize by the oligocene : whale bones and teeth , and fish and bird bones . to summarize , fossil
, and from three different rock units with a stratigraphic age spanning most of the oligocene . this shows that
was well established in the northeastern pacific ocean by the oligocene time and supports the view of rouse et al . (
we thank gerhard hundertmark and thomas dinter ( göttingen ) for photography , bettina reichenbacher ( munich ) , giorgio carnevale ( torino ) and norbert micklich ( darmstadt ) for help identifying the fish remains , and shannon johnson and bob vrijenhoek ( moss landing ) for access to whale bones in their collection and for stimulating discussions . nick higgs ( london ) and andrzej kaim ( warsaw ) are thanked for their constructive reviews that helped to improve the manuscript . financial support was provided by the deutsche forschungsgemeinschaft through grant ki802 / 6 - 1 to sk .
this article is distributed under the terms of the creative commons attribution license which permits any use , distribution , and reproduction in any medium , provided the original author ( s ) and the source are credited .
barnes , l . g . , and j . l . goedert . 2001 . stratigraphy and paleoecology of oligocene and miocene desmostylian occurrences in western washington state , usa .
braby , c . e . , g . w . rouse , s . b . johnson , w . j . jones , and r . c . vrijenhoek . 2007 . bathymetric and temporal variation among
bone worms and associated megafauna on whale - falls in monterey bay , california .
fujikura , k . , y . fujiwara , and m . kawato . 2006 . a new species of
fujiwara , y . , m . kawato , t . yamamoto , t . yamanaka , w . sato - okoshi , c . noda , s . tsuchida , t . komai , s . s . cubelio , t . sasaki , k . jacobsen , k . kubokawa , k . fujikura , t . maruyama , y . furushima , k . okoshi , h . miyake , m . miyazaki , y . nogi , a . yatabe , and t . okutani . 2007 . three - year investigations into sperm whale - fall ecosystems in japan .
glover , a . g . , k . m . kemp , c . r . smith , and t . g . dahlgren . 2008 . on the role of bone - eating worms in the degradation of marine vertebrate remains .
goedert , j . l . , r . l . squires , and l . g . barnes . 1995 . paleoecology of whale - fall habitats from deep - water oligocene rocks , olympic peninsula , washington state .
goffredi , s . k . , v . j . orphan , g . w . rouse , l . jahnke , t . embaye , k . turk , r . lee , and r . c . vrijenhoek . 2005 . evolutionary innovation : a bone - eating marine symbiosis .
higgs , n . d . , a . g . glover , t . g . dahlgren , and c . t . s . little . 2011 . bone - boring worms : characterizing the morphology , rate , and method of bioerosion by
higgs , n . d . , c . t . s . little , a . g . glover , t . g . dahlgren , c . r . smith , and s . dominici . 2012 . evidence of
jones , w . j . , s . b . johnson , g . w . rouse , and r . c . vrijenhoek . 2008 . marine worms ( genus
kiel , s . 2010 . on the potential generality of depth - related ecologic structure in cold - seep communities : cenozoic and mesozoic examples .
kiel , s . , and j . l . goedert . 2007 . six new mollusk species associated with biogenic substrates in cenozoic deep - water sediments in washington state , usa .
kiel , s . , j . l . goedert , w . - a . kahl , and g . w . rouse . 2010 . fossil traces of the bone - eating worm
kiel , s . , w . - a . kahl , and j . l . goedert . 2011 .
maas , m . c . 2007 . the histology of bones and teeth . in
moore , e . j . 1984 . molluscan paleontology and biostratigraphy of the lower miocene upper part of the lincoln creek formation in southwestern washington .
nesbitt , e . a . , r . a . martin , n . p . carroll , and j . grieff . 2010 . reassessment of the zemorrian foraminiferal stage and juanian molluscan stage north of the olympic mountains , washington state and vancouver island .
okoshi , k . , fujiwara , y . , and the scientific shipboard party , 2011 . r / v kaiyo + rov hyper - dolphin 3000 cruise report , ky11 - 01 leg 2 cruise in sagami bay , jamstec .
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, ed . prothero d . r . , 377–394 . the pacific section sepm .
prothero , d . r . , j . m . hoffman , and j . l . goedert . 2008 . paleomagnetism of the oligocene and miocene lincoln creek and astoria formations , knappton , washington .
rouse , g . w . , s . k . goffredi , s . b . johnson , and r . c . vrijenhoek . 2011 . not whale - fall specialists ,
rouse , g . w . , s . k . goffredi , and r . c . vrijenhoek . 2004 .
snavely , p . d . j . , a . r . niem , n . s . macleod , j . e . pearl , and w . w . rau . 1980 . makah formation—a deep - marginal - basin sequence of late eocene and oligocene age in the northwestern olympic peninsula , washington . u . s .
vrijenhoek , r . c . , p . collins , and c . l . van dover . 2008 . bone - eating marine worms : habitat specialists or generalists ?
vrijenhoek , r . c . , s . b . johnson , and g . w . rouse . 2009 . a remarkable diversity of boneworms (


the pinhead pearlfish , carapus boraborensis , is a species of slender , ray-finned fish in the family carapidae found in the tropical indo-pacific ocean ; it normally lives inside the body cavity of a sea cucumber such as the pineapple sea cucumber ( thelenota ananas ) or the leopard sea cucumber ( bohadschia argus ) .

pinhead pearlfish

@ firstdogonmoon the cucumber or pinhead pearlfish ! superb choice . some pearlfish also eat the cucumber ' s gonads . . . strange and stranger !
kate cranney on twitter :
@ firstdogonmoon the cucumber or pinhead pearlfish ! superb choice . some pearlfish also eat the cucumber ' s gonads . . . strange and stranger !
a small reddish - brown eel - like fish covered in fine dark speckles . the pinhead pearlfish lives within holothurians , and emerges through the cloacal opening of the sea cucumber at night .
some species of this family , however , are possibly parasitic . these live inside sea cucumbers where they will first eat the gonads of their host and then live inside the anal pore . the pinhead pearlfish ( carapus boraborensis ) is suspected to be parasitic whereas the silver pearlfish ( encheliophis homei ) is suspected to be non - parasitic based on stomach content analysis and where they are found within a cucumber when dissected .
( pacific pearlfish ) is found in the eastern pacific in the body cavity of cockles , pearl shells , and pen shells .
( bivalve pearlfish ) occurs in marine waters off western australia . it prefers to reside within sea cucumbers and the mantle cavity of bivalves
parmentier , e . and vandewalle , p . ( 2003 ) morphological adaptations of pearlfish ( carapidae ) to their various habitats . science publisher
before entry , a pearlfish will normally spend several minutes inspecting the entire body length of a cucumber before proceeding to the back end . a knocking or tapping movement is performed near the anus as if
asking
to gain entry . reports indicate that pearlfish normally back in tail first but have also been observed to enter head first . more than one pearlfish has been known to live inside a cucumber at any one time as well making for a somewhat cramped living environment . this trait has been observed with the silver pearlfish where sexual pairing has been found within a cucumber .
the great pearlfish , conqueror of sea cucumber bums , devourer of reproductive organs , all - around decent critter to anything but a sea cucumber .
( pearlfish ) is found in the western pacific on reefs . this fish lives in the body cavity of sea cucumbers by day and forages at night
this bizarre little fish lives inside the anus of a leopard sea cucumber ( bohadschia argus ) . i was filming a number of different fishes in the shallows , and only took a short clip of this sea cucumber . it wasn ' t until i looked at the footing that i saw the little pearlfish . pearlfish get their name from the members of their family that live inside oysters .
but the sea cucumber may not be entirely defenseless against the invasions of the pearlfish . some species have what could be functioning as a built - in gate in their anus — a handy accessory considering that in addition to the pearlfish , crabs and clams have also been known to make themselves at home inside the poor critters ( the sea cucumber , it seems , like any good host , can never really enjoy itself at its own party ) .
depending on what species it is , the pearlfish initiates one of two relationships once inside : a commensal one , in which it simply takes up space without either helping or adversely affecting the sea cucumber , or a rather more parasitic one , in which it chows down on its host’s gonads .
the pearlfish finds its reluctant host likely by smell , according to biologist eric parmentier of belgium’s university of liège . it then must choose the right end to enter , using its lateral line — sensory organs that detect movements in water — to home in on the outflow from the respiratory tree at the anus .
such pearlfishes come in a range of species , and don’t necessarily limit themselves to invading sea cucumbers . they’ll also work their way into sea stars , and are so named because they’ve been found dead inside oysters , completely coated in mother - of - pearl . beautiful , really , though i reckon the pearlfish would beg to differ .
pearlfish ( family carapidae ) are scaleless , their bodies are somewhat translucent , and they look remotely like eels when they swim outside of their host . they can be found in the atlantic , pacific and indian oceans and have been found down to depths of over 2 , 000 meters . some of the species can reach upwards of 50 cm in length when full grown .
ophidiiformes represent the
cusk eels
and some species within the family carapidae ( pearlfish ) live symbiotically within benthic invertebrates . the relationship of the fish to the host is quasi - parasitic ; only in a few cases is the parasitism overt . in most cases , the fish either consumes food that could be used by the host or , in most cases , simply takes up space
you’re breathing through your anus , by the way , and when you take a breath , the pearlfish strikes — squirming up your butt , making itself comfortable in your respiratory organ , and eating your gonads . or , they’ll go up in pairs and have sex in your body cavity . and that’s when you realize that you must have been a really awful human being in a past life . like , the type of person who talks on their phone in a movie theater kind of awful .
so like a disgraced samurai disemboweling himself , the sea cucumber gifts the world with its intestines , whether the world wants them or not . interestingly , though , the pearlfish doesn’t itself seem to trigger this reaction for reasons that aren’t yet clear . and it’s important to consider that the fish in fact benefits from the evisceration , because by using the sea cucumber as a home , it necessarily adopts its host’s predators . its survival depends on the sea cucumber’s ability to defend itself , which is quite intriguing from an evolutionary perspective .
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eel - like , moderate to shallow body depth ; maxilla free and movable ; cardiform teeth present ; branchiostegal membranes partly or completely united ; swim bladder with thin terminal membrane or bulb but no constriction ; lacking enlarged dentary or premaxillary fangs , dentary diastema , pelvic fins , and swim bladder rocker bone ; pectoral fins small , less than 29 % head length ; body thick , robust and highly pigmented ; 15 - 17 precaudal vertebrae .
uncommon species . shallows water of coral reefs . lives within holothurians ( e . g . thelenota ananas < \ i > , bohadschia argus < \ i > and stichopus chloronotus < \ i > ) .
indo - pacific : mauritius to the society islands , north to taiwan and the yaeyama islands ; including mariana and caroline islands .
greek , enchelys , = eel + greek , ophis = serpent ( ref . 45335 )
marine ; demersal ; depth range 1 - 150 m ( ref . 34024 ) . tropical
maturity : l m ? range ? - ? cm max length : 30 . 0 cm tl male / unsexed ; ( ref . 4104 )
dorsal soft rays ( total ) : 31 - 42 ; anal soft rays : 45 - 57 ; vertebrae : 119 - 126 . eel - like , moderate to shallow body depth ; maxilla free and movable ; cardiform teeth present ; branchiostegal membranes partly or completely united ; swim bladder with thin terminal membrane or bulb ; lacking enlarged dentary or premaxillary fangs , dentary diastema , pelvic fins , and swim bladder rocker bone ( ref . 34024 ) . pectoral fins small , less than 29 % head length ; body thick , robust and highly pigmented ( ref . 34024 ) .
uncommon species ( ref . 34024 ) . lives within holothurians ( e . g . thelenota ananas and bohadschia argus ) ( ref . 1602 ) .
nielsen , j . g . , d . m . cohen , d . f . markle and c . r . robins , 1999 . ophidiiform fishes of the world ( order ophidiiformes ) . an annotated and illustrated catalogue of pearlfishes , cusk - eels , brotulas and other ophidiiform fishes known to date . fao fish . synop . 125 ( 18 ) : 178p . rome : fao . ( ref . 34024 )
) : 23 . 6 - 28 . 9 , mean 27 . 5 ( based on 920 cells ) . phylogenetic diversity index ( ref .
bayesian length - weight : a = 0 . 00102 ( 0 . 00046 - 0 . 00225 ) , b = 3 . 06 ( 2 . 88 - 3 . 24 ) , in cm total length , based on all lwr estimates for this body shape ( ref .
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picture of carapus boraborensis has been licensed under a creative commons attribution - noncommercial . original source : fishbase permission : some rights reserved
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lady elliot island ' s shallow coral lagoon , in the coral sea at the south end of the great barrier reef .
i know . it lives in a sea cucumber bottom ! from what i ' ve read the sea cucumber is not getting anything out of the
relationship
. nature , weirder than anything we can imagine . the video i put up at youtube is a too cropped . i ' ll see if i can fix that so you can see the fish better .
marine ; demersal ; depth range 1 - 150 m ( ref . 34024 ) . tropical , preferred ?
confused by a class within a class or an order within an order ? please see our brief essay .
to cite this page : myers , p . , r . espinosa , c . s . parr , t . jones , g . s . hammond , and t . a . dewey . 2018 . the animal diversity web ( online ) . accessed at https : / / animaldiversity . org .
disclaimer : the animal diversity web is an educational resource written largely by and for college students . adw doesn ' t cover all species in the world , nor does it include all the latest scientific information about organisms we describe . though we edit our accounts for accuracy , we cannot guarantee all information in those accounts . while adw staff and contributors provide references to books and websites that we believe are reputable , we cannot necessarily endorse the contents of references beyond our control .
this material is based upon work supported by the national science foundation grants drl 0089283 , drl 0628151 , due 0633095 , drl 0918590 , and due 1122742 . additional support has come from the marisla foundation , um college of literature , science , and the arts , museum of zoology , and information and technology services .
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these fish are unique in that the adults normally live inside invertebrates like clams , sea squirts , and starfish in a commensal relationship ( not harming their host ) . this trait is common throughout the carapidae family .
this pairing behavior is not often seen in our reef aquariums but occasionally members of various reefkeeping forums will report that they have one in their tank .
watch the video below to see this relationship . if you ' re short on time , skip ahead to the 6 minute mark for the re - entry . . .
shane has kept saltwater tanks for the last 12 years , is a research scientist , lives in northern indiana , and is a proud advanced aquarist staffer .
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what is your favourite australian fish @ firstdogonmoon ? ! i ' m curious . . . . and often impressed by your use of cartoonal binomial nomenclature .
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) : 23 . 6 - 28 . 9 , mean 27 . 5 ( based on 920 cells ) .
phylogenetic diversity index ( ref . 82805 ) : pd 50 = 0 . 5078 [ uniqueness , from 0 . 5 = low to 2 . 0 = high ] .
bayesian length - weight : a = 0 . 00102 ( 0 . 00046 - 0 . 00225 ) , b = 3 . 06 ( 2 . 88 - 3 . 24 ) , in cm total length , based on all lwr estimates for this body shape ( ref . 93245 ) .
trophic level ( ref . 69278 ) : 3 . 4 ±0 . 3 se ; based on size and trophs of closest relatives
vulnerability ( ref . 59153 ) : low vulnerability ( 16 of 100 ) .
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conceived and designed the experiments : oh fl . performed the experiments : oh . analyzed the data : oh fl . contributed reagents / materials / analysis tools : fl . wrote the paper : oh fl . obtained permission for animal experiments : fl .
this is an open - access article distributed under the terms of the creative commons attribution license , which permits unrestricted use , distribution , and reproduction in any medium , provided the original author and source are properly credited .
data on sex - specific differences in sound production , acoustic behaviour and hearing abilities in fishes are rare . representatives of numerous catfish families are known to produce sounds in agonistic contexts ( intraspecific aggression and interspecific disturbance situations ) using their pectoral fins . the present study investigates differences in agonistic behaviour , sound production and hearing abilities in males and females of a callichthyid catfish .
current data demonstrate that both male and female m . thoracata produce aggressive sounds , but the behavioural contexts and sound characteristics differ between sexes . sexes do not differ in hearing , but it remains to be clarified if this is a general pattern among fish . this is the first study to describe sex - specific differences in agonistic behaviour in fishes .
a wealth of information is available on sound - generating mechanisms , sound production during agonistic and reproductive behaviour , and hearing in fishes ( for reviews see [ 1 – 5 ] ) . despite this knowledge , data on sex - specific differences in sonic organs , sound production and in hearing are very limited [ 6 ] .
a previous study on the callichthyid armoured catfish megalechis thoracata ( formerly hoplosternum thoracatum ) showed that , corresponding to the behavioural contexts , males and females uttered different types of pectoral sounds [ 27 ] . this differs considerably from investigations on the callichthyid c . paleatus , in which males produced trains of sounds during dyadic contests , whereas no stridulation sounds could be recorded from females during social interactions [ 13 , 28 ] .
acoustic communication is defined as transmission of information by a sender to a receiver with benefits for the receiver or mutual potential benefits for both [ 36 ] . accordingly , a match of spectral contents of sounds and best hearing sensitivity of the intended receiver , and vice versa , should be preferred by natural selection [ 33 , 35 ] . auditory sensitivity was found to match the characteristics of sounds produced in the frequency domain in some species [ 35 , 37 – 41 ] , but mismatch was observed in others [ 33 , 42 ] .
the aims of the present study were to investigate sex - specific differences in ( 1 ) sound - generating mechanisms , ( 2 ) agonistic behaviour , ( 3 ) sounds produced and their characteristics , ( 4 ) the auditory abilities , and finally ( 5 ) to determine if the dominant frequencies of sounds correlate with the best hearing sensitivity in the callichthyid catfish m . thoracata .
experiments were performed with permission of the austrian federal ministry of science and research ( bundesministerium für wissenschaft und forschung , gz 66 . 006 / 0023 - ii / 10b / 2008 ) . the permission covered all experimental procedures . no animal was sacrificed during this study . according to the austrian law on experiments in animals ( tierversuchsgesetz 1989 / 2005 ) an institutional animal care and use committee ( or ethics committee ) was not mandatory and did not exist at the university of vienna when experiments were carried out .
seventeen specimens of m . thoracata were used for the study : seven subadult males ( 93–104 mm total length , tl , 12 . 2–19 . 1 g body mass ) , nine subadult females ( 84–102 mm , 9 . 8–17 . 1 g ) and one adult male ( 126 mm , 32 . 9 g ) . fish were obtained from a local pet shop and a fish farmer . we assume that 16 of the 17 fish were subadult because they were one year old during our experiments and mayr [ 27 ] stated that first reproductive behaviour in this species is shown at the age of two years . moreover , we observed no reproductive behaviour in the present study when sexes were kept together in community tanks . this species is a bottom - dwelling fish from slowly flowing rivers , pools , drainage ditches and swampy areas in south america [ 43 ] .
the sex of the fish was determined by inspecting the genital papillae , the distance between coracoids and the size of pectoral fins . males possess genital papillae , a narrower gap between coracoids and longer , thicker and orange pectoral spines [ 43 ] . due to the individually spotted body pattern , the subjects could be easily distinguished from each other .
fish were kept in three community tanks ( 110 x 30 x 55 cm ) whose bottom was covered with fine sand and which were similarly equipped with half flower pots , tubes , plants and roots as shelters . the tank of the adult male measured 90 x 30 x 30 cm . four males and four females and three males and five females , respectively , were kept together . a 12 : 12 hour light : dark cycle was provided and the water temperature was kept at 25 ± 1°c . the aquaria were filtered by external filters in order to reduce noise . fish were fed frozen chironomid larvae and occasionally artificial food ( flakes and tablets ) five to six times a week .
after behaviour and sound recordings , body mass , total length and length of the pectoral spine of each contestant were measured . the pectoral spine length ( psl ) was measured from the juncture of the spine with the outer body surface to its tip using digital callipers . the relative pectoral spine length ( rpsl ) was calculated using the formula rpsl = psl / tl , where tl is the total length .
all agonistic experiments were performed from august to november 2011 . fish were kept for three months in holding tanks before the start of behavioural experiments . the video and sound recordings were carried out in a walk - in soundproof room , which was constructed as a faraday cage . the experiments were conducted in a test tank ( 70 x 40 x 35 cm ) . the resonant frequency of the tank is 3042 hz according to akamatsu et al . [ 44 ] . the water temperature was maintained at 25 ± 1°c . the test tank was placed on a table that rested on a vibration - isolated concrete plate .
the behaviour and acoustic signals were recorded using a hydrophone ( brüel & kjaer 8101 , sensitivity −184 db re 1 v μpa −1 ) , which was connected to a power supply ( brüel & kjaer 2804 ) and placed in the centre of the aquarium close to the back wall . both the hydrophone and video camera ( sony ccd - vx1e ) were connected to a hifi s - vhs video cassette recorder ( jvc hr - s4700 eg / e ) . hifi audio and s - video signals were stored simultaneously on s - vhs hifi videotapes ( fujifilm super vhs pro se - 240 ) . sound pressure levels ( rms fast time weighting , linear frequency weighting ) were measured in parallel with the sound recordings using a sound level meter ( brüel & kjaer mediator 2238 ) connected to the power supply . the observer was always hidden behind a curtain during recordings . external filters of the test tank were switched off before the start of experiments .
as the intention of this study was to record acoustic displays during agonistic behaviour dyadic interactions were not allowed to proceed to a phase , where biting might have occurred . no biting or injuries were observed in any of the experiments .
each sound was digitized using a sampling rate of 11 khz ( 16 bit resolution ) and analysed using cool edit 2000 ( syntrillium software corporation , phoenix , usa ) and st x soundtools 3 . 7 . 8 . ( institute of sound research at the austrian academy of sciences , vienna ) . only sounds with a good signal - to - noise ratio were analysed . the following acoustic variables were measured from sounds recorded during dyadic contests :
sound duration ( sd ) : the total length between the onset and the end of a single call or a series of sounds . dominant frequency ( df ) : the frequency with the highest amplitude within a power spectrum . the dominant frequency of sounds was determined from cepstrum - smoothed power spectra . harmonic sounds are characterized by several regularly spaced peaks , in which the frequencies of the harmonic peaks are multiples of that of the fundamental frequency . the harmonic content of a sound was controlled by overlaying a harmonic grid .
sound pressure level ( spl ) : measured in db re 1μpa ( rms fast , linear weighting ) . in order to compensate the varying distances of vocalizing fish to the hydrophone , a correction factor was calculated . therefore , the test tank was divided into 21 sectors ( each measuring 10 x 10 cm ) by using a grid applied on the front glass of the aquarium . the sector in which a fish emitted sounds was noted . because sounds of m . thoracata were of low energy , pink noise was chosen for calculating a correction factor . short tone bursts were played back at a constant spl from a small loudspeaker ( fuji 7g06 , 8 ohm , 0 . 8 w ) , in each of the 21 sectors , and the spls were noted . the relative difference of the spl measured in the sector nearest to the hydrophone ( 3 cm away ) and the other sectors were calculated and added to the spl values of fish sounds measured before . thus , a distance - independent absolute spl value could be determined for each sound emission .
the aim of the behavioural analyses was to describe all behavioural patterns ( elements ) occurring during the male - male and female - female agonistic contests . all behavioural patterns shown during a total of 24 agonistic encounters were classified according to the description presented in
. the number of acoustic signals and visual displays such as attack , circling and head nodding was counted for each experiment and individual .
description of the behavioural repertoire shown during dyadic male - male and female - female interactions of m . thoracata .
fin displaying or approaching another fish , stopping suddenly before forcefully hitting the other with its tail .
two females swam in an anti - parallel ( head - to - tail ) orientation .
two males moved towards each other , in a parallel , anti - parallel position or various angles spreading all their fins . additionally , at high intensities the caudal part of the body was erected in a distinct angle .
continued escape reaction in response to a chase . fish swam rapidly away from the aggressor .
females showed serial vertical up and down movements of their heads in different positions to each other .
males moved their heads rapidly away and towards the opponent while bending their body c - like .
one female following the opponent by a snake - like movement on the bottom .
definitions followed mayr [ 27 ] except for fin beating , jerks and sneaking . m—males , f—females .
auditory sensitivity was determined using the non - invasive auditory evoked potential ( aep ) recording technique , originally reported by kenyon et al . [ 45 ] and modified by wysocki and ladich [ 46 – 47 ] .
for each test condition , the stimuli were presented at opposite polarities ( 180° phase shifted ) and the corresponding aeps were averaged in order to eliminate stimulus artefacts . at spls close to the threshold , this procedure was performed at least twice and the aep traces were overlaid to examine if they were repeatable . the spl values of tone burst stimuli were reduced in 4 db steps . by overlaying replicate traces , the lowest spl in which an identifiable and repeatable aep trace could be obtained was regarded as threshold . the method developed by kenyon et al . [ 45 ] gives auditory thresholds very similar to behavioural thresholds ( for discussion see [ 4 , 48 ] ) .
additionally , a one - way analysis of variance ( anova ) was performed , followed by a bonferroni post - hoc test , in order to determine differences in sound characteristics of each aggressive sound type . differences in relative pectoral spine length between sexes were tested using a paired t - test . a total of 244 sounds were analysed .
mean hearing thresholds were determined for both sexes at each frequency . thresholds obtained for males ( n = 6 ) and females ( n = 6 ) were compared by a two - way anova using a general linear model , where one factor was sex and the other was frequency . the sex factor alone should reveal differences in sensitivity between sexes and , combined with the frequency factor , if different tendencies exist at different frequencies of the audiograms .
all statistical tests were conducted using pasw 18 . 0 ( spss inc . , chicago , usa ) . the significance level was set at p ≤ 0 . 05 .
produced sounds by vibrating pectoral fins . the first pectoral fin rays were orange in males in contrast to females . pectoral spines were longer and thicker in males . the relative length of pectoral spines ( pectoral spine length / total length ) was on overage 1 . 7 - fold higher in males than females ( t - test , t = 44 . 27 , df = 15 , p ≤ 0 . 01 ) (
different letters indicate statistically significant differences between sexes . psl—total length of pectoral spine , tl—total fish length .
aggressive interactions usually started after removal of the separating sheet and as soon as opponents detected each other visually . the agonistic behavioural sequences were interrupted by air gulping , digging , resting close to each other or withdrawal into the shelter . for the description of behavioural patterns observed during thirteen male - male and eleven female - female encounters see
generally , one or both males started to approach each other and erected their fins ( threatening fin display ) . occasionally , this posture was followed by fin beating , which could last for several seconds . head jerking followed and was accompanied by the production of two sound types , namely barks or thumps , indicating high levels of aggression . jerking could occur without sound emission , in which case maximally three jerks were observed .
in 12 out of 13 encounters ( 92 % ) , barks and thumps were produced during aggressive interactions . furthermore , in 10 out of 13 contests ( 78 % ) , sound emission occurred in both contestants . barks were emitted at various distances from a few centimetres up to a maximum of 40 cm away from the opponent . before abduction of pectoral fins , a single adduction was observed . barks were often produced during approaching and swimming (
) . the individual producing a sound mostly swam away and then again approached the conspecific . the latter could react by fin displays or moving away from the other .
the illustration shows the right male approaching the opponent , shortly before uttering a bark .
in contrast to barks , thumps occurred only in direct proximity ( within one body length ) to the opponent . typically , opponents showed fin displays in a parallel , anti - parallel position or at various angles to each other (
) , or swam close and emitted thumps . typically , thumps were produced in an oblique position towards the opponent . opponents responded by producing a thump , by attacking or by fleeing .
this screen shot shows the typically threatening fin display with fins spread and the caudal part of the right male erected in a distinct angle . the right fish produced a thump in this oblique anti - parallel position relative to the conspecific .
during all experiments , we counted a total of 40 attacks , often preceded by fin display and fin beating . attacks were mainly performed by sound producers , occasionally accompanied by thumps . besides these behavioural elements , chasing was observed . during chasing , barks were emitted by the pursuer .
in five out of seven experiments , barks were even emitted after separating both fishes by the plastic sheet , i . e . after they lost visual contact . barks were recorded mainly in males , which produced numerous sounds during the dyadic contests . just in one case did both opponents emit barks . after separation by the plastic sheet , males generated barks during swimming or when approaching the separating sheet .
) close to the bottom . this sneaking behaviour toward the opponent was occasionally accompanied by the emission of crackles . sounds were recorded in all female - female experiments . in four out of eleven contests , both females vocalized during agonistic interactions . sounds were produced close to the opponent ( within one to two body lengths ) (
) and were generated by rapid pectoral fin movements . shortly before uttering a crackle , the vocalizing fish may strike towards the opponent . crackles were most frequently emitted when one female chased the other . swimming after each other or pursuing could continue into circling behaviour (
) , which lasted up to 3 s . sounds were uttered before , during or at the end of circling .
head nodding was either performed by one female or simultaneously by both . two to 18 head nods per individual were observed within a series . we counted a total of 736 head nods during eleven agonistic interactions , and the vocalizing female exhibited a higher rate . this visual threatening display could be elicited by the movement of one fish , when swimming by or when above the other , before and after circling , and when resting close to each other . furthermore , interactions were characterized by a high rate of body contacts such as touching with barbels . attacks occurred only four times : three were accompanied by crackles and one was exhibited shortly after head nodding .
in contrast to male - male encounters , in which both males vocalized , crackles were mainly produced by one female , seldom by both . female - female contests were characterized by circling behaviour and the lack of jerks . head nodding could not be observed in any male - male interaction . while males beat their fins during fin displays , females did it during circling . females undulated only their dorsal and caudal fins , whereas in males all fins were involved . furthermore , females attacked less frequently than males , indicating a lower level of aggressivity .
three types of sounds were recorded during dyadic encounters . males produced barks and thumps , and females emitted crackles . barks and thumps were recorded in seven out of eight males and crackles in eight out of nine females . the fish produced 376 barks , 66 thumps and 739 crackles during 24 interactions . acoustic signals were not audible to human listeners . video analysis revealed that barks were produced during abduction of the pectoral fin . we could not unequivocally determine the movement of the pectoral fins ( adduction and / or abduction ) during the emission of thumps and crackles .
barks were low - frequency harmonic sounds showing frequency modulation ; they only occurred singly . they consisted of one to three parts and were therefore classified as being mono - , bi - or tripartite (
) . sound duration ranged from 159 to 317 ms , and the spl ranged from 101 . 2 to 125 db re 1 μpa at a distance of 3 cm . the main energies were found in the first , second or third harmonic . the dominant frequency of bipartite barks varied in the first part from 110 to 600 hz , and in the second from 170 to 730 hz .
the spectrum shows three harmonics ( 1st , 2nd , 3rd ) with the highest energy found in the second harmonic . sampling rate 22 khz . hanning filter , overlap 75 % , ( a ) filter bandwidth 20 hz , ( b ) filter bandwidth 1 hz , number of coefficients 350 .
the spectrum reveals three harmonics ( 1st , 2nd , 3rd ) within the second sound part ( white arrow ) with the highest energy found in the second harmonic . the oscillogram shows lower amplitude in the first part ( light blue arrow ) . sampling rate 11 khz . hanning filter , overlap 75 % , ( a ) filter bandwidth 20 hz , ( b ) filter bandwidth 1 hz , number of coefficients 170 .
thumps were produced singly and showed no harmonic structure . they were mostly mono - , seldom bipartite (
) . bipartite thumps were recorded only in the one examined adult subject . sound duration ranged from 116 to 446 ms and the spl ranged from 107 . 07 to 137 . 5 db re 1 μpa . the dominant frequency varied from 70 to 210 hz .
the dominant frequency is indicated in ( b ) . sampling rate 11 khz . hanning filter , overlap 75 % , ( a ) filter bandwidth 20 hz , ( b ) filter bandwidth 1 hz , number of coefficients 80 .
female crackles differed from male sounds in their complex structure and frequency content . they were of higher frequency and always consisted of series of sound elements (
) . crackles were built up mostly by four sound elements ( range : 2–8 elements ) . these series were characterized by a main element featuring the highest peak - to - peak - amplitude and several elements of lower amplitude before and after the main element (
) . elements could be separated by intervals from each other and could consist of a substructure such as a train of pulses ( = one element ) .
the oscillogram shows five sound elements . the white arrow indicates the main element , followed by a train of pulses . the dominant frequency is indicated in the cepstrum - smoothed power spectrum in ( b ) . sampling rate 11 khz . hanning filter , overlap 75 % , ( a ) filter bandwidth 100 hz , ( b ) filter bandwidth 1 hz , number of coefficients 20 .
the duration of crackles ranged from 81 to 394 ms . single elements ( including train of pulses ) ranged from 5 . 6 up to 192 . 9 ms and main elements varied from 15 . 3 to 57 . 6 ms in duration . spls were between 101 . 5 and 128 . 1 db re 1 μpa . dominant frequencies of crackles varied from 370 to 830 hz .
) . thumps were significantly louder than barks and crackles , but no such difference was found between barks and crackles ( bonferroni post - hoc test ) . furthermore , the dominant frequencies varied between sound types ( one - way anova : f
) . mean dominant frequencies of crackles were much higher than of other sound types . the first part of barks and thumps did not differ significantly in dominant frequency ( bonferroni post - hoc test ) .
mean ( + se ) sound duration of male barks and thumps ( n = 7 ) and of female crackles ( n = 8 ) .
mean ( + se ) sound pressure level of male barks and thumps ( n = 7 ) and of female crackles ( n = 8 ) .
mean ( + se ) dominant frequency of male barks and thumps ( n = 7 ) and of female crackles ( n = 8 ) .
sound characteristics of male barks and thumps and female crackles were significantly correlated to morphological measures when males and females were pooled . duration of male thumps and female crackles combined increased with mean total length and pectoral spine length (
correlations between mean sound characteristics ( sound duration , dominant frequency , sound pressure level ) of male and female sound types and morphological variables ( total length , pectoral spine length , relative pectoral spine length ) .
n = 15 . b—bark , bp—bark part , c—crackles , t—thumps . pearson’s correlation coefficients are given . asterisks indicate statistically significant differences .
) . individuals with larger pectoral spines emitted sounds of lower frequency . mean dominant frequencies of the first part of barks ( or the second part of barks ) , or of thumps and females crackles combined , were negatively correlated to pectoral spine lengths (
thus , mean sound characteristics were always correlated to relative pectoral spine lengths , except for spls of male barks . in contrast , only sound duration and spls of thumps and crackles combined were correlated to total length (
all fish detected tone bursts between 100 hz and 4 khz . hearing curves of both sexes were u - shaped with best auditory sensitivities between 0 . 2 and 1 khz (
) . hearing abilities decreased rapidly above 1 khz . thresholds increased by 41 db between 1 and 4 khz in males and females . overall , hearing thresholds did not differ between sexes ( two - way anova : f
= 1 . 2 , n . s . ) . females had better hearing between 0 . 1 and 1 khz ( two - way anova : f
= 0 . 007 , n . s . ) . no significant interaction was found between sex and frequency . thus , the difference in auditory sensitivity between 0 . 1 and 1 khz was not frequency - dependent .
mean ( ± se ) auditory sensitivities of male ( n = 6 ) and female ( n = 6 ) m . thoracata .
) . the greatest energy of sounds was concentrated from 180 to 620 hz in male barks , from 100 to 540 hz in male thumps and from 470 to 750 hz in female crackles . main energies of male and female sounds were much lower than the resonant frequency of the test tank ( see energy peak at 3 khz in
( solid lines ) in relation to spectral characteristics of sounds ( dotted lines ) .
power spectra of sounds were averaged of sounds of all individuals and are shown in relative amplitude values ( right y - axis ) .
video analysis revealed that both sexes of m . thoracata produced sounds during rapid pectoral fin movements . therefore , we assume that sound production is based on a stridulatory mechanism , well known in numerous catfish families [ 50 ] . while we observed that male barks were produced during abduction of pectoral fins , the movement of pectoral spines during generation of thumps and crackles remains unclear due to faster movements of fins and technical limitations of a standard video recording system . pruzsinszky and ladich [ 13 ] mentioned that c . paleatus produced sounds by abducting the pectoral fins alternately . similarly , heyd and pfeiffer [ 51 ] reported that in the callichthyid catfish d . urostriatum sounds were produced during abduction , and all members of the family callichthyidae probably generate sounds during abduction of pectoral fins . we assume that barks and thumps are generated by a single pectoral fin abduction and crackles by several fin abductions depending on the number of elements within a crackle sound .
the current study revealed that agonistic behaviour of male and female m . thoracata differed from each other . male agonistic behaviour mainly consisted of fin displays and jerks , whereas female behaviour was characterized by circling , head nodding , sneaking and striking . agonistic sounds were produced by males and females in different behavioural contexts . while males uttered thumps during threatening displays and barks mostly during approaching and swimming , females , in contrast , emitted crackles mainly during chasing behaviour . threatening displays in males consisted of a sequence of visual displays shown by both opponents , during which both may produce sounds . in contrast , chasing behaviour in females was typically shown in one individual , which vocalized when following or moving toward the other fish .
based on the present data , male m . thoracata seem to be more aggressive than females as revealed by the much higher number of attacks ( 40 in males versus four in females ) observed during a similar number of same - sex contests . the vocalizing behaviour of m . thoracata differs markedly from the closely related callichthyine subfamily member c . paleatus , in which only males produced trains of sounds during courtship and in which aggressive behaviour was absent during dyadic contests [ 13 ] . kaatz and lobel [ 56 ] mentioned that male corydoras spp . emitted agonistic chase sound only before , during and after spawning . this difference between the genera corydoras and megalechis is primarily due to their different mating systems . male megalechis are territorial and defend nest sites , while male corydoras do not build nests or show parental care .
the observation that fin beating and sound production occurred at short distances to the opponent indicates that water movement may be detected by the lateral line . this may constitute a third communication channel besides the visual and acoustic ones . such hydrodynamic cues are potentially involved in all short - distance agonistic and reproductive activities in fishes but seldom unequivocally proven . satou et al . [ 58 ] showed that visual and vibrational ( lateral line detected ) stimuli elicit spawning behaviour in male red salmon oncorhynchus nerka .
our study revealed three different agonistic sound types ( two in males , one in females ) based on physical characteristics of sounds . mean sound duration in m . thoracata differed between sexes , with female crackles ( 167 ms ) being shorter than both male barks ( 219 ms ) and thumps ( 240 ms ) . mean spls of thumps ( 123 db ) were higher than those of barks ( 112 db ) and crackles ( 115 db ) . mean dominant frequency of female crackles ( 562 hz ) was much higher than that of male sounds ( 132–403 hz ) . in contrast , mayr [ 27 ] wrote that aggressive signals ( = thumps ) were shorter than territorial sounds ( = barks ) . nonetheless , there is a lack of information about whether male sounds differ from female sounds because the sound characteristics have not been compared statistically between sexes . differences between the current and the prior study by mayr [ 27 ] may reflect that the present study investigated subadult fish and the former only adult reproductive fish . our fish were most likely immature because we observed no reproductive behaviour in community tanks .
) . all show best sensitivity between 0 . 3 and 1 khz and a step decrease in sensitivity above 1 khz [
] showed that smaller swimbladders and fewer weberian ossicles results in a decrease in sensitivity above 1 kilohertz .
aep - audiograms of all representatives of the family callichthyidae investigated in the recent and in prior studies .
megalechis thoracata ( current study , females and males pooled ) , corydoras paleatus [ 33 ] , corydoras sodalis and dianema urostriatum [ 52 ] .
in summary , this is the first investigation showing sex - specific differences in agonistic behaviour , sound production , sound characteristics and hearing abilities using same - sex agonistic contests . the data reveal clear differences in agonistic behaviour , which have not been shown in any fish species before . this study furthermore indicates that differences in sound characteristics between sexes seem to be due to the dimorphism in the pectoral sonic organs in megalechis .
we want to thank tanja schulz - mirbach , walter lechner , jessica jaxion - harm , angelika zebedin , isabelle maiditsch and jasmin oswald for their help with sound level measurements , isabelle maiditsch for her advice regarding analysis of female sounds and hearing measurements , and sonja windhager for her introduction to camstudio . finally , we want to thanks michael stachowitsch for scientific english proofreading and a reviewer for its helpful comments .
this article was supported by the open access publishing fund of the university of vienna . the funders had no role in study design , data collection and analysis , decision to publish , or preparation of the manuscript .
data will be uploaded in our university’s repository as soon as the paper has been accepted .
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