tickell 's leaf warbler ( phylloscopus affinis ) is a leaf warbler found in asia in the countries of bangladesh , bhutan , china , india , myanmar , nepal , pakistan and thailand .

the species has a yellowish underside and super-cilium .

like other leaf warblers it feeds mostly on insects by gleaning and short sallies .

an active bird , it prefers the canopy and low shrubbery and can be difficult to track as it moves actively from branch to branch , acrobatically exploring the underside of leaves and twigs .

the clear yellowish undersides and lack of a wing bar can be used to tell it apart from similar species .

it has slim dark legs with largely pale lower mandible and grayish wing panel .

the name commemorates the british ornithologist samuel tickell who collected in india and myanmar .

tickell ' s leaf warbler

tickell ' s leaf warbler ( phylloscopus affinis ) is a species of bird in the phylloscopidae family .
10–11 cm ; 5·5–7·75 g . a small to medium - sized leaf - warbler with yellowish supercilium and underparts . long supercilium is pale yellow , becoming . . .
clement , p . ( 2018 ) . tickell ' s leaf - warbler ( phylloscopus affinis ) . in : del hoyo , j . , elliott , a . , sargatal , j . , christie , d . a . & de juana , e . ( eds . ) . handbook of the birds of the world alive . lynx edicions , barcelona . ( retrieved from urltoken on 9 july 2018 ) .
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– high - altitude ranges in c china ( e qinghai , gansu , sichuan , n yunnan ) ; recorded in non - breeding season in s china ( yunnan ) .
not globally threatened . common and widespread in breeding season in pakistan , nepal , bhutan and n india ; locally common in s china . uncommon non - breeding visitor in myanmar . . .
martens et al in 2008 showed that the population breeding in qinghai , gansu and sichuan is better treated as a separate species alpine leaf warbler phylloscopus occisinensis . this treatment is followed here but no attempt has been made ( so far ) to identify the birds here which were photographed on their wintering grounds as to whether they should be moved to p . occisinensis or remain here . ref : martens , j . ; sun , y - h . & päckert , m . 2008 .
intraspecific differentiation of sino - himalayan bush - dwelling phylloscopus leaf warblers , with description of two new taxa ( p . fuscatus , p . fuligiventer , p . affinis , p . armandii , p . subaffinis )
. vertebrate zoology 58 ( 3 ) : 233 - 265 .
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del hoyo , j . , collar , n . j . , christie , d . a . , elliott , a . , fishpool , l . d . c . , boesman , p . and kirwan , g . m . 2016 . hbw and birdlife international illustrated checklist of the birds of the world . volume 2 : passerines . lynx edicions and birdlife international , barcelona , spain and cambridge , uk .
justification : this species has an extremely large range , and hence does not approach the thresholds for vulnerable under the range size criterion ( extent of occurrence < 20 , 000 km2 combined with a declining or fluctuating range size , habitat extent / quality , or population size and a small number of locations or severe fragmentation ) . the population trend appears to be stable , and hence the species does not approach the thresholds for vulnerable under the population trend criterion ( > 30 % decline over ten years or three generations ) . the population size has not been quantified , but it is not believed to approach the thresholds for vulnerable under the population size criterion ( < 10 , 000 mature individuals with a continuing decline estimated to be > 10 % in ten years or three generations , or with a specified population structure ) . for these reasons the species is evaluated as least concern .
the global population size has not been quantified , but the species is reported to be locally common ( baker 1997 ) . trend justification : the population is suspected to be stable in the absence of evidence for any declines or substantial threats .
( amended version of 2017 assessment ) . the iucn red list of threatened species 2017 : e . t22715270a118853090 .
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in past , often treated as conspecific with p . subaffinis , but differs in morphology , voice and habitat ; molecular study # r indicates not closely related . recently described form occisinensis # r was originally given species rank , but is virtually identical in song to nominate and less divergent morphologically from nominate than is simultaneously described perflavus # r . three subspecies recognized .
song , from tops of low bushes and boulders , mostly apr to end jul but also on passage in sept , a . . .
food mostly small insects , including weevils ( curculionidae ) and other small beetles ( coleoptera ) , aphids ( aphidoidea ) , flies ( diptera ) , . . .
may–aug ; fledglings first week jul ; one brood . nest , built by both sexes , a ball of dry grasses , plant fibres ( including of juniper ) . . .
migratory . altitudinal migrant , moving short to medium distances to lower levels . passage through . . .
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formerly included in a broad sylviidae . recent review # r indicates that previous internal arrangement , with all taxa of present family split between seicercus and phylloscopus , was paraphyletic . as a result some authors have split phylloscopus into several smaller genera , with some movement of taxa from phylloscopus to seicercus , but accuracy of this debatable on present knowledge . one of these versions # r involves groups containing species as listed below : rhadina ( species 1–3 ) ; abrornis ( species 4–13 ) ; phylloscopus ( species 14–28 ) ; and seicercus ( species 29–78 ) . another version # r divides family into nine genera . more cautious alternative involves merging seicercus into phylloscopus ; adopted herein , pending results of a comprehensive study currently in progress # r .
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this species has an extremely large range , and hence does not approach the thresholds for vulnerable under the range size criterion ( extent of occurrence < 20 , 000 km2 combined with a declining or fluctuating range size , habitat extent / quality , or population size and a small number of locations or severe fragmentation ) . the population trend appears to be stable , and hence the species does not approach the thresholds for vulnerable under the population trend criterion ( > 30 % decline over ten years or three generations ) . the population size has not been quantified , but it is not believed to approach the thresholds for vulnerable under the population size criterion ( < 10 , 000 mature individuals with a continuing decline estimated to be > 10 % in ten years or three generations , or with a specified population structure ) . for these reasons the species is evaluated as least concern .
recommended citation birdlife international ( 2018 ) species factsheet : phylloscopus affinis . downloaded from urltoken on 09 / 07 / 2018 . recommended citation for factsheets for more than one species : birdlife international ( 2018 ) iucn red list for birds . downloaded from urltoken on 09 / 07 / 2018 .
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synalpheus microneptunus is a species of small snapping shrimp native to the waters off the island of barbados .

it is one of at least seven known species of eusocial shrimp .

they are cryptofauna , living exclusively within the network of tunnels in the sponges neopetrosia proxima and neopetrosia subtriangularis .

they form small colonies of six to fifteen individuals , usually with only a single breeding female .

synalpheus microneptunus

synalpheus microneptunus hultgren , iii & duffy , 2011 , n . sp . - plazi treatmentbank
have a fact about synalpheus microneptunus ? write it here to share it with the entire community .
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synalpheus microneptunus , hultgren , kristin m . , iii , kenneth s macdonald & duffy , emmett , 2011
order decapoda latreille alpheidae rafinesque synalpheus bate synalpheus ankeri n . sp . figs . 1 - 2
synalpheus odontophorus is an indo - west pacific snapping shrimp that belongs to the comatularum species group within the genus synalpheus . first described from indonesia , it lives associated with crinoids .
composition of synalpheus shrimp assemblages from the sand bores reefs , belize between 1996 and 2012 .
synalpheus trispinosus is an indo - west pacific and indian ocean snapping shrimp first described from indonesia .
synalpheus demani was first placed in the neomeris species group within the genus synalpheus by banner and banner ( 1975 ) . for additional descriptions , see banner and banner ( 1975 ) , chace ( 1988 ) .
morphologically similar to synalpheus streptodactylus , but can be differentiated from most other synalpheus species by its long , slender , rostrum , reaching to the middle of the second antennular article ( banner and banner 1985 ) .
synalpheus regalis lives in coral reefs , most commonly in the sponge species xestospongia spp . and hyattella intestinalis .
synalpheus
rathbunae c
( duffy 1996c , bjls ) ; zuzalpheus regalis ( rios and duffy 2007 ) .
synalpheus somalia is an indo - west pacific snapping shrimp first described from somalia ( banner and banner 1979 ) .
synalpheus modestus is an indo - west pacific snapping shrimp first described from banda , indonesia ( de man 1909 ) .
synalpheus shrimps ( crustacea : decapoda : alpheidae ) . i . the gambarelloides group , with a description of a new species
synalpheus regalis is one of at least six described eusocial synalpheus species in the gambarelloides species complex , making this group a model system for examining the evolution of eusociality in the sea ( duffy et al . 2000 , morrison et al . 2004 ) .
alpheus triunguiculatus ( sensu de man 1888 ) ; alpheus spiniger ( sensu bate 1888 ) ; synalpheus brockii ( nobili 1901 ) .
synalpheus cayoneptunus is currently known from sponges in the genus neopetrosia , and other unidentified white sponges found in the matrices of coral rubble .
16s bayesian consensus gene tree of the synalpheus paraneptunus species complex . taxon names , node numbers and outgroup as in fig . a1 .
the species name is derived from the type locality ( the florida keys ) and its affinity with other species of the synalpheus paraneptunus - complex .
synalpheus regalis belongs to the gambarelloides species complex ( duffy , 1996 ) within the genus synalpheus . the species name is derived from the latin
regalis ,
meaning royal , referring to the social structure of this species in which large colonies are headed by a single
queen
.
synalpheus duffyi is currently known from sponges in the genus neopetrosia , and other unidentified white sponges , presumably closely related to neopetrosia , in coral rubble .
synalpheus demani is an indo - west pacific snapping shrimp that lives associated with crinoids . for more details , see abrs ( 2009 ) : urltoken .
j . emmett duffy ( 1996 ) .
synalpheus regalis , new species , a sponge - dwelling shrimp from the belize barrier reef , with comments on host specificity in synalpheus
( pdf ) . journal of crustacean biology 16 ( 3 ) : 564–573 . doi : 10 . 2307 / 1548748 .
synalpheus cretoculatus is an indo - west pacific snapping shrimp first described from andaman sea , off the southern tip of burma ( banner and banner 1979 ) .
s . regalis belong to the gambarelloides species group in the genus synalpheus , and molecular work suggests that eusociality evolved independently at least three times in this group .
synalpheus curacaoensis was named after the country from which this species was first described ( curaçao ) . type locality : spanish bay , curaçao ( schmitt 1924 ) .
figure 5 . synalpheus microneptunus n . sp . paratype , non - ovigerous individual , cl 2 . 44 mm ( usnm 1154072 , original vims br 08 - 7002 - 2 ) from xestospongia proxima , cement factory , barbados : a , third pereopod ; b , same , distal region ; c , fourth pereopod ; d , same , distal region ; e , fifth pereopod ; f , same , distal region . scale bar = 1 mm for a , c , e ; 0 . 27 mm for b , d , f .
figure 4 . synalpheus microneptunus n . sp . paratype , non - ovigerous individual , cl 2 . 44 mm ( usnm 1154072 , original vims br08 - 7002 - 2 ) from xestospongia proxima , cement factory , barbados : a , minor first pereopod ; b , same , distal region of fingers ; c , second pereopod , setae not drawn ; d , same , distal region . scale bar = 0 . 33 mm for a , 0 . 16 mm for b , 1 mm for c , 0 . 4 mm for d .
figure 4 . synalpheus microneptunus n . sp . paratype , non - ovigerous individual , cl 2 . 44 mm ( usnm 1154072 , original vims br 08 - 7002 - 2 ) from xestospongia proxima , cement factory , barbados : a , minor first pereopod ; b , same , distal region of fingers ; c , second pereopod , setae not drawn ; d , same , distal region . scale bar = 0 . 33 mm for a , 0 . 16 mm for b , 1 mm for c , 0 . 4 mm for d .
synalpheus brachyceros was first described from tuamoto islands , french polynesia by nobili , 1906 ( recorded from poupin 2008 ) ; it has not been recorded since its original description .
synalpheus crosnieri is an indian ocean snapping shrimp that belongs to the gambarelloides species group within the genus synalpheus ( banner and banner 1983 ) . banner and banner ( 1983 ) reported highly skewed sex ratios in this species ( one or a few females collected and often hundreds of non - ovigerous individuals ) . as such , this species is thought to be eusocial , like many species of synalpheus in the gambarelloides species group ( duffy 1998 ) . like many species in the gambarelloides species group , s . crosnieri also lives in sponges .
synalpheus brachyceros is a indo - west pacific snapping shrimp first described from tuamoto islands , french polynesia by nobili , 1906 . for more details , see poupin ( 2008 ) : urltoken
synalpheus crosnieri belongs to the gambarelloides species group within the genus synalpheus ( banner and banner 1983 ) . the species is named after dr . alain crosnier , office de la recherche scientifique et technique outre - mer , paris . type locality : madagascar ( banner and banner 1983 ) , types stored at the muséum national d’histoire naturelle , paris , france ( mnhn ) .
a new species of snapping shrimp from the gulf of mexico and bahama islands , synalpheus agelas , is described , illustrated , and compared to other species of the genus . notes on its association with the orange demosponge , agelas dispar , and other invertebrate associates are given . a key to the species of synalpheus with the carpus of the second pereiopod composed of four articles is presented .
specimen count 1 record last modified 16 oct 2014 nmnh - invertebrate zoology dept . common name snapping shrimps taxonomy animalia arthropoda malacostraca decapoda alpheidae collector kristin hultgren dr . kenneth s . macdonald iii ocean / sea / gulf north atlantic ocean , caribbean sea depth ( m ) 11 - 12 preparation alcohol ( ethanol ) sex female stage ovigerous see more items in invertebrate zoology place cement factory , barbados , north atlantic ocean collection date 21 oct 2008 type status holotype type citation [ article ] hultgren , k . , et al . 2011 . sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species . zootaxa . 2834 : 1 - 16 . other numbers collector number : br08 - 7001 usnm number 1154070 published name synalpheus microneptunus macdonald et al . , 2011
specimen count 1 record last modified 16 oct 2014 nmnh - invertebrate zoology dept . common name snapping shrimps taxonomy animalia arthropoda malacostraca decapoda alpheidae collector kristin hultgren dr . kenneth s . macdonald iii ocean / sea / gulf north atlantic ocean , caribbean sea depth ( m ) 11 - 12 preparation alcohol ( ethanol ) stage non - ovigerous see more items in invertebrate zoology place cement factory , barbados , north atlantic ocean collection date 21 oct 2008 type status paratype type citation [ article ] hultgren , k . , et al . 2011 . sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species . zootaxa . 2834 : 1 - 16 . other numbers collector number : br08 - 7002 - 7 usnm number 1154077 published name synalpheus microneptunus macdonald et al . , 2011
anker , arthur ; toth , eva ( 2008 ) .
a preliminary revision of the synalpheus paranuptunus coutiere , 1909 species complex ( crustacea : decapoda : alpheidae )
. zootaxa 1915 : 1–28 .
synalpheus is a genus of snapping shrimp of the family alpheidae , presently containing more than 100 species ; new ones are described on a regular basis , and the exact number even of described species is disputed .
the species - complex of synalpheus paraneptunus coutière , 1909 is one of the most behaviorally and sexually diverse groups of sponge - dwelling shrimp in synalpheus , containing both eusocial and pair - living species . accurate resolution of this taxonomically challenging group is crucial to examining the evolution of social behavior in the genus . new collections from the us florida keys and cuba , along with examination of previous collections from jamaica , panama and belize , have yielded two new species : the eusocial synalpheus cayoneptunus n . sp . ( described from type material from the florida keys ) , and synalpheus ankeri n . sp . ( described from type material from belize ) . synalpheus duffyi anker and tóth , 2008 is reported from new locations in cuba and the florida keys . a phylogenetic analysis of six of the nine species in the s . paraneptunus - species - complex indicates that eusociality likely arose only once in this complex but was secondarily lost in the pair - living species s . ankeri . a key to the nine known species in the complex is presented based on morphological characters .
like several other species in the genus synalpheus , s . regalis exhibits eusocial population structure ( defined here as living in large colonies with a single breeding female ) . this species undergoes direct development , with embryos hatching into crawling larvae .
maximum body size is 9 mm ( carapace length ) ( chace 1988 ) . morphologically similar to synalpheus triacanthus , but can be separated by various characters of the major chela and the merus of the third pereopod ( chace 1988 ) .
synalpheus iphinoe is a indo - west pacific snapping shrimp first described from multiple localities in indonesia ( de man 1909 ) . little is known about the habitat requirements of this species ; it has been reported as living in association with the gorgonian solenocaulon sp .
synalpheus somalia was first described from somalia by banner and banner ( 1979 ) . this species is named after the type locality ( somalia ) . types stored at the national museum of natural history , smithsonian institution ( usnm ) . holotype : usnm 181357 .
figure 3 . synalpheus microneptunus n . sp . holotype , ovigerous female , cl 2 . 72 mm ( usnm 1154070 , original vims br08 - 7001 ) from xestospongia proxima , cement factory , barbados : a , carapace , anterior region , and cephalic appendages , dorsal view ; allotype , non - ovigerous individual , cl 2 . 44 mm ( usnm 1154072 , original vims br08 - 7002 - 2 ) from xestospongia proxima , cement factory , barbados : b , anterior carapace and cephalic appendages , dorsal view ; c , chela of major first pereopod , ventral view ; d , same , dorsal view ; e , same , anterior region ; f , third maxilliped . scale bar = 1 mm for a , d ; 1 . 33 mm for b , 1 . 5 mm for c , e ; 0 . 4 mm for f .
synalpheus regalis is a unique species of sponge - dwelling snapping shrimp , and the first described example of eusociality in the sea ( duffy 1996a ) . like social insects such as ants and honeybees , synalpheus regalis lives in large colonies consisting of one breeding female
queen
and typically 100 or more non - breeding workers that jointly defend the sponge against intruders ( duffy 1996b , 2007 ) . allozyme work has confirmed that most colonies consist of full - sibs produced by the queen and possibly a single male
king .
figure 3 . synalpheus microneptunus n . sp . holotype , ovigerous female , cl 2 . 72 mm ( usnm 1154070 , original vims br 08 - 7001 ) from xestospongia proxima , cement factory , barbados : a , carapace , anterior region , and cephalic appendages , dorsal view ; allotype , non - ovigerous individual , cl 2 . 44 mm ( usnm 1154072 , original vims br 08 - 7002 - 2 ) from xestospongia proxima , cement factory , barbados : b , anterior carapace and cephalic appendages , dorsal view ; c , chela of major first pereopod , ventral view ; d , same , dorsal view ; e , same , anterior region ; f , third maxilliped . scale bar = 1 mm for a , d ; 1 . 33 mm for b , 1 . 5 mm for c , e ; 0 . 4 mm for f .
kenneth macdonald , kristin hultgren , & j . emmett duffy ( 2009 ) .
the sponge - dwelling snapping shrimps ( crustacea , decapoda , alpheidae , synalpheus ) of discovery bay , jamaica , with descriptions of four new species
. zootaxa 2199 : 42 .
like most members of the synalpheus gambarelloides species group , synalpheus regalis has a streamlined body adapted to living in sponge canals and a thick brush of setae on the minor chela ( claw ) . maximum body size ( carapace length , or cl ) of males is 3 . 2 mm ; females , 4 . 14 mm ( macdonald et al . 2009 ) . color : body translucent to faint translucent - orange ; distal tips of major chela brighter orange , ovaries and embryos pale green ( duffy 1996b , rios and duffy 2007 ) .
hultgren , k . , k . s . iii macdonald & j . e . duffy , 2011 . sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species . — zootaxa 2834 : 1 - 16 .
coi bayesian consensus gene tree of the synalpheus paraneptunus species complex . taxon names include species , voucher number and collection location ; species in bold are eusocial . numbers above or below each node indicate bayesian posterior probability values ( bpp ) . s . goodei is the out - group .
w . w . l . au & k . banks ( 1998 ) .
the acoustics of the snapping shrimp synalpheus parneomeris in kaneohe bay
. journal of the acoustical society of america 103 ( 1 ) : 41–47 . doi : 10 . 1121 / 1 . 423234 .
hultgren , kristin m . ; macdonald iii , kenneth s ; duffy , j . emmett ( 2011 ) .
sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species
. zootaxa 2834 : 1–16 .
figure 6 . synalpheus microneptunus n . sp . paratype , non - ovigerous individual , cl 2 . 49 mm ( usnm 1154071 , original vims br 08 - 7002 - 1 ) from xestospongia proxima , cement factory , barbados : a , abdomen , right side ; paratype , non - ovigerous individual , cl 2 . 44 mm ( usnm 1154072 , original vims br 08 - 7002 - 2 ) from xestospongia proxima , cement factory , barbados : b , telson , dorsal view ; c , distolateral margin of left uropodal exopod , dorsal view ; paratypes , non - ovigerous individual , cl 2 . 44 ( usnm 1154073 , original vims br 08 - 7002 - 3 ) from xestospongia proxima , cement factory , barbados : d , distolateral margin of right uropodal exopod , dorsal view . scale bar = 1 mm for a , 1 . 4 mm for b , 0 . 25 mm for c , d .
margarita hermoso - salazar , mary wicksten & juan j . morrone ( 2008 ) .
phylogenetic analysis of the paulsoni species group ( decapoda : alpheidae ) from the american pacific , with implications for the phylogenetic classification of the genus synalpheus
( pdf ) . zootaxa 1744 : 19–30 .
kristin m . hultgren , kenneth s . macdonald iii & j . emmett duffy ( 2011 ) .
sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species
( pdf ) . zootaxa 2834 : 1–16 .
hultgren , kristin m . , iii , kenneth s macdonald & duffy , emmett , 2011 , sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species , zootaxa 2834 , pp . 1 - 16 : 8 - 10
kristin m . hultgren , kenneth s . macdonald iii , & j . emmett duffy ( 2011 ) .
sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species
( pdf ) . zootaxa 2834 : 1–16 .
hultgren , k . , k . s . iii macdonald & j . e . duffy , 2011 . sponge - dwelling snapping shrimps ( alpheidae : synalpheus ) of barbados , west indies , with a description of a new eusocial species . — zootaxa 2834 : 1 - 16 . [ details ]
anker , arthur , pachelle , paulo p . g . ( 2014 ) : taxonomic notes on some brazilian species of synalpheus spence bate , 1888 , with new records and description of a new species ( decapoda , alpheidae ) . zootaxa 3815 ( 2 ) : 215 - 232 , doi : urltoken
synalpheus odontophorus was first described from three locations in southern and eastern indonesia by de man ( 1909 ) . for more details , see banner and banner ( 1978 ) , chace ( 1988 ) . types stored at the zoölogisch museum , universiteit van amsterdam , amsterdam , the netherlands ( zma ) .
arthur anker & sammy de grave ( 2008 ) .
zuzalpheus ríos and duffy , 2007 : a junior synonym of synalpheus bate , 1888 ( decapoda : alpheidae )
( pdf ) . journal of crustacean biology 28 ( 4 ) : 735–740 . doi : 10 . 1651 / 07 - 2969 . 1 .
banner and banner ( 1983 ) reported highly skewed sex ratios in this species ( one or a few females collected and often hundreds of non - ovigerous individuals ) . as such , this species is thought to be eusocial , like many species of synalpheus in the gambarelloides species group ( rios and duffy 2007 ) .
arthur anker & sammy de grave ( 2008 ) .
zuzalpheus ríos and duffy , 2007 : a junior synonym of synalpheus bate , 1888 ( decapoda : alpheidae )
( pdf ) . journal of crustacean biology 28 ( 4 ) : 735–740 . doi : 10 . 1651 / 07 - 2969 . 1 .
j . emmett duffy , cheryl l . morrison & kenneth s . macdonald ( 2002 ) .
colony defense and behavioral differentiation in the eusocial shrimp synalpheus regalis
( pdf ) . behavioral ecology and sociobiology 51 ( 5 ) : 488–495 . doi : 10 . 1007 / s00265 - 002 - 0455 - 5 .
synalpheus modestus was first described from banda , indonesia by de man , 1909 ( de man 1909 ) . for more details , see banner and banner ( 1985 ) . type locality : banda , indonesia ( de man 1909 ) , types stored at the zoölogisch museum , universiteit van amsterdam , amsterdam , the netherlands ( zma ) .
paratype for synalpheus curacaoensis schmitt , 1924 catalog number : usnm 57555 collection : smithsonian institution , national museum of natural history , department of invertebrate zoology preparation : alcohol ( ethanol ) collector ( s ) : c . van der horst year collected : 1920 locality : curacao , spanish bay , netherlands antilles , caribbean sea , north atlantic ocean
j . emmett duffy , cheryl l . morrison & rubén ríos ( 2000 ) .
multiple origins of eusociality among sponge - dwelling shrimps ( synalpheus )
( pdf ) . evolution 54 ( 2 ) : 503–516 . doi : 10 . 1111 / j . 0014 - 3820 . 2000 . tb00053 . x . pmid 10937227 .
phylogenetic tree of synalpheus paraneptunus - species - complex , shown as a bayesian consensus tree based on 16s and coi . taxon names include species , voucher number , and collection location ; species in bold are eusocial . numbers above or below each node indicate bayesian posterior probability values ( bpp ) . s . goodei is the out - group .
morrison , cheryl l ; rios , ruben ; duffy , j emmett ( may 2004 ) .
phylogenetic evidence for an ancient rapid radiation of caribbean sponge - dwelling snapping shrimps ( synalpheus )
. molecular phylogenetics and evolution 31 ( 2 ) : 810–813 . doi : 10 . 1016 / s1055 - 7903 ( 03 ) 00252 - 5 .
synalpheus iphinoe was first described from multiple localities in indonesia by de man ( 1909 ) : sapeh strait , madura bay , banda anchorage , and rumah - kuda - bay , and roma - island . for more details , see banner and banner ( 1985 ) . types stored at the zoölogisch museum , universiteit van amsterdam , amsterdam , the netherlands ( zma ) .
synalpheus trispinosus was first described from the southern part of selat moro , indonesia by de man , 1910 ( reported in chace 1988 ) . for more details , see chace ( 1988 ) . type locality : southern part of selat moro , indonesia ( chace 1988 ) , types stored at the zoölogisch museum , universiteit van amsterdam , amsterdam , the netherlands ( zma ) .
paratype for synalpheus regalis duffy , 1996 catalog number : usnm 280095 collection : smithsonian institution , national museum of natural history , department of invertebrate zoology preparation : alcohol ( ethanol ) collector ( s ) : j . duffy year collected : 1993 locality : carrie bow cay , belize , caribbean sea , north atlantic ocean microhabitat : outer reef ridge depth ( m ) : 15 to 15
banner and banner ( 1983 ) reported highly skewed sex ratios in this species ( one or a few females collected and often hundreds of non - ovigerous individuals ) . as such , this species is thought to be eusocial , like many species of synalpheus in the gambarelloides species group ( duffy 1998 ) . like many species in the gambarelloides species group , s . crosnieri also lives in sponges .
funding : the authors are grateful to the smithsonian institution’s caribbean coral reef ecosystem program and to the national science foundation , most recently via grants ios - 1121716 ( jed ) and ios - 1121435 ( drr ) , for supporting the authors’ research on sponge - dwelling synalpheus . the funders had no role in study design , data collection and analysis , decision to publish , or preparation of the manuscript .
paratype for synalpheus regalis duffy , 1996 catalog number : usnm 280093 collection : smithsonian institution , national museum of natural history , department of invertebrate zoology sex / stage : male ; preparation : alcohol ( ethanol ) collector ( s ) : j . duffy year collected : 1993 locality : carrie bow cay , belize , caribbean sea , north atlantic ocean microhabitat : outer reef ridge depth ( m ) : 15 to 15
holotype for synalpheus regalis duffy , 1996 catalog number : usnm 280092 collection : smithsonian institution , national museum of natural history , department of invertebrate zoology sex / stage : male ; preparation : alcohol ( ethanol ) collector ( s ) : j . duffy year collected : 1993 locality : carrie bow cay , belize , caribbean sea , north atlantic ocean microhabitat : outer reef ridge depth ( m ) : 15 to 15
paratype for synalpheus regalis duffy , 1996 catalog number : usnm 280094 collection : smithsonian institution , national museum of natural history , department of invertebrate zoology sex / stage : female ; ovigerous preparation : alcohol ( ethanol ) collector ( s ) : j . duffy year collected : 1993 locality : carrie bow cay , belize , caribbean sea , north atlantic ocean microhabitat : outer reef ridge depth ( m ) : 15 to 15
vouchers of most sponge species were kindly identified by dr . klaus ruetzler at the us national museum of natural history . provisional identification of synalpheus species in the field was based on observations of the color , host associations , body size , and social structure of living shrimp , and confirmed by careful microscopic examination of morphology according to the latest taxonomy of the group [ 11 ] , [ 13 ] – [ 17 ] , as well as molecular sequence data in some cases [ 18 ] .
we thank klaus ruetzler , mike carpenter , valerie paul , and zach foltz of the smithsonian institution for facilitating our work at carrie bow cay in belize ; anthony downes , peter gayle , and dayne buddo for help in jamaica ; and cheryl morrison , eva tóth , rubén ríos , james douglass , and sally bornbusch for collaboration as members of team synalpheus in various years . our research and collections were approved by the belize department of fisheries and the national environment and planning agency of jamaica .
in jamaica we made two collections , one in january 2008 and one in january 2012 . in 2008 our collections were exploratory and intended to capture as much of the synalpheus diversity as possible [ 11 ] . in 2012 our primary goal was to locate colonies of eusocial shrimp species . because we have data from only two collections , and since sampling was not quantitative in either year , we focus here on changes in the structure of jamaican eusocial shrimp colonies rather than trends in sponge or shrimp community composition .
synalpheus cretoculatus was first described from andaman sea , off the southern tip of burma by banner and banner ( 1979 ) . the species sname is derived from
creta
( chalk ) and
oculatus
( to bear eyes ) , and refers to a distinguishing character of this species - - the unpigmented , chalk - like condition of the eyes . type locality : andaman sea , off the southern tip of burma ( banner and banner 1979 ) , types stored at the national museum of natural history , smithsonian institution ( usnm ) . type : usnm 181358 .
the one partial exception to the trend of declining eusocial shrimp in belize was synalpheus chacei , which remained present in 2012 , albeit less frequent ( fig . 2 , table s1 ) . s . chacei is a comparative generalist that uses several species of sponges as hosts in belize [ 5 ] and elsewhere . s . chacei showed no clear change in either abundance or colony size between 2012 and prior years ( fig . 2 , 3 ) . although the trend in s . chacei was also toward smaller colonies in the later collections , this was not as marked as in the other eusocial species .
our results show that eusocial shrimp have declined greatly , and that three of the four eusocial species have apparently disappeared , from shallow reefs in the central belize barrier reef after dominating these habitats for at least two decades . prior to 2012 eusocial species were found on each of the nine sampling trips that spanned 14 years , and comprised 53–99 % ( median 87 % ) of the total numbers of shrimp collected in each year . yet in 2012 , only seven of 60 samples contained eusocial shrimp , all specimens of the host generalist synalpheus chacei , which accounted for only 8 % of shrimp collected in that year . similar declines of eusocial species appear to be occurring in jamaica .
most sponges in the sand bores were cryptic , filling spaces among eroded branches of dead coral . in the field , pieces of dead coral rubble were collected , placed in mesh bags , transported back to the station at carrie bow cay , and retained in flowing seawater until they could be processed . rubble was broken apart and all sponges were provisionally identified . sponges were then dissected and macrofauna was removed from the internal canals of the sponge . synalpheus shrimps were sorted by species , counted , then preserved in davidson’s fixative , 10 % formalin in seawater , 70 % etoh , or 95 % etoh . representative samples of each sponge species were preserved in 70 % etoh for later identification .
our analysis is based on specimens of shrimp ( synalpheus spp . ) and sponges collected in belize and jamaica . in belize , we sampled cryptic reef sponges and associated shrimp from dead coral rubble in 1–3 m depth in the sand bores region , a collection of small reefs and banktops that rise from the sand - bottomed lagoon behind the barrier reef in the vicinity of the smithsonian institution’s field station at carrie bow cay ( 16°48 . 155′n , 088°04 . 896′w ) . between 1996 and 2009 , samples of reef rubble were collected on 21 separate days ; in 2012 we sampled the sand bores region systematically and intensively to compare the communities with those of prior years , collecting ten bags of coral rubble ( 1 . 2–7 . 1 liters each , median 3 . 6 l ) from each of six reefs spanning the geographic extent of the sand bores complex ( see [ 5 ] for more detailed methods ) .
animal social organization varies from complex societies where reproduction is dominated by a single individual ( eusociality ) to those where reproduction is more evenly distributed among group members ( communal breeding ) . yet , how simple groups transition evolutionarily to more complex societies remains unclear . competing hypotheses suggest that eusociality and communal breeding are alternative evolutionary endpoints , or that communal breeding is an intermediate stage in the transition towards eusociality . we tested these alternative hypotheses in sponge - dwelling shrimps , synalpheus spp . although species varied continuously in reproductive skew , they clustered into pair - forming , communal and eusocial categories based on several demographic traits . evolutionary transition models suggested that eusocial and communal species are discrete evolutionary endpoints that evolved independently from pair - forming ancestors along alternative paths . this ‘family - centred’ origin of eusociality parallels observations in insects and vertebrates , reinforcing the role of kin selection in the evolution of eusociality and suggesting a general model of animal social evolution .
we characterized community structure , separately for synalpheus shrimps and sponges , using non - metric multidimensional scaling ( nmds ) , a non - parametric ordination approach , implemented in primer [ 19 ] . for nmds analysis of shrimp communities , we used relative abundances ( % of total shrimp in sample ) rather than raw abundance as input to control for differences in sampling effort among days ; relative abundances were square - root transformed prior to analysis to reduce the influence of dominant species . for analysis of sponge community composition , we used presence / absence data as input because ( i ) some species of sponges enmeshed in the coral rubble could rarely be collected without breaking them into several pieces , such that abundance could not be accurately estimated , and ( ii ) sponge sizes were not measured in most collections . for each analysis we constructed a resemblance matrix among samples based on bray - curtis similarity measures , and generated the nmds plots using 100 random starts and the best 2d solution . to estimate the goodness of fit of the nmds ordination to the data , we calculated stress , i . e . , the mismatch between the observed rankings in similarity among samples and the distance rankings estimated from the ordination ; stress values < 0 . 20 are generally considered “useful” [ 19 ] . we tested differences among groups ( time period : before 2012 vs . 2012 ) using the analysis of similarity ( anosim ) procedure in primer , and the simper procedure to identify the contributions of individual species to differences between groups . analyses used 999 permutations ; significance values are pseudo - p values .
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citation : duffy je , macdonald iii ks , hultgren km , chak tcs , rubenstein dr ( 2013 ) decline and local extinction of caribbean eusocial shrimp . plos one 8 ( 2 ) : e54637 . urltoken
copyright : © 2013 duffy et al . 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 credited .
competing interests : co - author dustin rubenstein is a plos one editorial board member . his contribution as a co - author does not alter the authors’ adherence to all the plos one policies on sharing data and materials .
tropical reefs are widely recognized as centers of marine biodiversity [ 1 ] . the corals that build them have therefore been well studied , as have the charismatic and ecologically important fishes they support . but within the porous reef structure of dead corals , algae , mollusks , and other organisms lives a rich variety of largely invisible organisms of every phylum . although most of these species are poorly known they comprise the bulk of marine biodiversity .
in 2012 we revisited carrie bow cay , belize as part of a long - term research program [ 7 ] , [ 12 ] , [ 13 ] . to our surprise the eusocial shrimp species that have dominated reefs at this site for > 20 years had apparently disappeared . here we document this temporal change by assembling data on the changing species composition and abundance of cryptic sponges and their associated shrimps . we also document changes in the structure of eusocial shrimp colonies in belize over the past 16 years , and present preliminary evidence for similar patterns in jamaica .
analysis of temporal change in sponge - dwelling shrimp communities is constrained by the highly heterogeneous nature of the coral rubble habitat , which makes quantitative sampling challenging , and by the haphazard nature of sampling this material during the early years . however , the sand bores collections prior to 2012 were intended to maximize shrimp diversity , and the cryptic sponges were often not visible prior to collection , hence we have no reason to suspect that our collections were strongly biased relative to natural abundances or species composition . nevertheless , to minimize the influence of haphazard collections or variation in sampling effort , we pooled all specimens collected on a given day for the pre - 2012 collections , treating the aggregated specimens from a given day as a single sample . in 2012 we collected larger , more systematic samples consisting of bags of rubble and sponges ; each such bag is considered a separate sample in 2012 .
changes in ( a ) shrimp and ( b ) sponge community composition through time .
non - metric multidimensional scaling ( nmds ) was performed on square - root transformed relative abundances of shrimp , and on presence / absence data for sponges . light blue symbols and lines represent samples from pre - 2012 , whereas dark blue symbols and lines are samples from 2012 .
changes in relative abundance of ( left ) eusocial and ( right ) nonsocial , pair - forming shrimp through time in belize .
the left part of each panel shows the percentage of the total sampled shrimp made up by the focal species in collections from that year ; gray bars at right show the percentage of samples in which the species was found before 2012 versus in 2012 . the top panels shows relative abundance of all eusocial ( left ) and non - social ( right ) species aggregated together ; remaining panels show individual species . sample sizes ( number of days sampled in collections before 2012 , number of sampled bags in 2012 ) were : 1996 ( 1 ) , 1998 ( 1 ) , 1999 ( 3 ) , 2001 ( 3 ) , 2002 ( 2 ) , 2003 ( 2 ) , 2004 ( 2 ) , 2005 ( 2 ) , 2009 ( 5 ) , 2012 ( 60 ) .
other strong contributors to temporal change in the shrimp assemblage were pair - forming and species and species that live in small , non - eusocial groups , which showed the opposite pattern ( fig . 2 ) : s . ruetzleri , s . yano , and s . “ longicarpus small” were relatively rare prior to 2012 , but were dominant species in 2012 . s . bousfieldi , a socially plastic species that usually lives in pairs or small groups , fluctuated strongly among dates with little discernible pattern in abundance or group size . the trend of several pair - forming species increasing in abundance as eusocial species declined partly reflects the fact that percentages are not independent of one another . however , frequencies of occurrence , which are not correlated in this way , show a similar pattern , namely increased commonness of the pair - forming species s . ruetzleri , s . yano , and s . “longicarpus small” in 2012 as the eusocial species disappeared ( fig . 2 right - hand panels , table s1 ) .
in contrast to the shift in shrimp assemblages , composition of sponge assemblages showed little change in 2012 compared with prior years ( fig . 1 , p = 0 . 125 , anosim ) . nmds of the sponge community produced an ordination with relatively low stress ( 0 . 11 ) , indicating a good fit . despite the lack of significant change in overall composition of the sponge assemblage , however , our extensive collections from 2012 located no specimens of the favored hosts of eusocial shrimp s . regalis and s . filidigitus in the sand bores reefs , namely neopetrosia ( formerly xestospongia ) proxima , n . cf . subtriangularis , or oceanapia sp . these sponges collectively occurred in 11 of 21 samples prior to 2012 but were completely absent in 2012 ( table s2 ) .
the declining trend in commonness of eusocial shrimp colonies in belize coincided with parallel strong declines in average colony sizes and increases in the frequency of queenless colonies ( fig . 2 ) . the trend is dramatically illustrated by s . filidigitus ( fig . 3 ) : between 1996 and 2005 we collected 23 colonies of s . filidigitus with a median size of 42 individuals , all but three of which ( 87 % ) included a queen , whereas in 2009 we found only two colonies , each with two individuals and neither with a queen . in 2012 , our extensive search of the sand bores region yielded no s . filidigitus . the highly social species s . regalis was uncommon in the shallow sand bores , having been historically more common on deeper reefs , but showed a similar pattern : prior to 2009 , we collected two s . regalis colonies of 19 and 374 individuals from the sand bores , the smaller of which was queenless , whereas in 2009 we collected only two colonies , each with nine individuals and no queen . we found no s . regalis in the 60 samples collected from the sand bores in 2012 . the eusocial species s . elizabethae was not found in 2009 or 2012 so we could not compare colony sizes through time for this species .
changes in shrimp colony size and frequency of queenless colonies in belize through time .
queenless colonies are shown as the black portion of each bar . c med = median colony size ( number of individual shrimp per sponge ) , % q = the percentage of colonies that contained a breeding queen .
in jamaica , we made collections in only two years but these produced a larger number of colonies than for several of the eusocial species in belize . although based on only two collections , the pattern of declining colony size and increasing frequency of queenless colonies in jamaica is strikingly similar to that observed in belize ( fig . 4 ) . s . regalis colony size declined from a median of 30 individuals in 2008 to five individuals in 2012 , with about half the colonies queenless during both time periods . for s . duffyi , the pattern was similar : median colony size declined from 52 to four , and the percentage of colonies with a queen declined from 83 to 30 between 2008 and 2012 .
changes in shrimp colony size and frequency of queenless colonies in jamaica through time .
changes in shrimp community composition through time . nmds was performed on presence / absence data . symbols as in fig . 1
composition of sponge assemblages from the sand bores reefs , belize between 1996 and 2012 .
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duffy je 1 , macdonald ks 3rd , hultgren km , chak tc , rubenstein dr .
virginia institute of marine science , the college of william and mary , gloucester point , virginia , united states of america . jeduffy @ urltoken
pmid : 23418429 pmcid : pmc3572134 doi : 10 . 1371 / journal . pone . 0054637
research support , u . s . gov ' t , non - p . h . s .
hultgren , macdonald & duffy , 2011 . accessed at : urltoken ; = 588964 on 2018 - 07 - 09
de grave , s . & c . h . j . m . fransen . ( 2011 ) . carideorum catalogus : the recent species of the dendrobranchiate , stenopodidean , procarididean and caridean shrimps ( crustacea : decapoda ) . zool . med . leiden . 85 ( 9 ) : 30 . ix . 2011 : 195 - 589 figs 1 - 59 . ( look up in imis ) [ details ] available for editors [ request ]
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de grave , s . & c . h . j . m . fransen . ( 2011 ) . carideorum catalogus : the recent species of the dendrobranchiate , stenopodidean , procarididean and caridean shrimps ( crustacea : decapoda ) . < em > zool . med . leiden . < / em > 85 ( 9 ) : 30 . ix . 2011 : 195 - 589 figs 1 - 59 .
type material . holotype : ovigerous female , cl 2 . 73 mm ( usnm
, 21 . x . 2008 . paratypes : 1 non - ovigerous individuals , cl 2 . 16–2 . 49 mm ( usnm
08br 7002 – 1 to 7002 – 12 ) , same collection data as holotype .
08br5103 , 5703 ) , brandon’s beach , no host recorded . 8 ovigerous females , 31 non - ovigerous individuals ( vims
08br 6301 ) , breach reef , no host recorded . 1 ovigerous female , 3 non - ovigerous individuals ( vims
08br 6710 ) , cement factory , no host recorded . 1 ovigerous female , 11 non - ovigerous individuals ( vims
. largest ovigerous female , cl 2 . 86 mm , largest non - ovigerous individual , cl 2 . 55 mm .
description : body subcylindrical ; carapace smooth , sparsely setose , posterior margin with distinct cardiac notch . rostrum longer and narrower than ocular hoods ( fig 3
) , latter dorsally convex ; blunt distally , separated from rostrum by adrostral sinus . stylocerite acute , with blunt tip reaching beyond midpoint of first segment of antennular peduncle . basicerite with blunt projection on dorsomesial corner , with longer ventrolateral spine , latter not reaching third segment of antennular peduncle and about 3 / 4 length of scaphocerite . scaphocerite with short blade ranging from vestigial to < 1 / 4 length of distolateral spine , latter robust , acute , reaching almost to distal end of third segment of antennular peduncle ; lateral margin concave . third maxilliped ( fig . 3
) massive , with fingers clearly shorter than half - length of palm ; fixed finger slightly shorter than dactyl . palm of chela with distodorsal protuberance tapering to acute point , curved toward dactyl . minor first pereopod ( fig . 4
) with palm less than two times longer than high ; fingers clearly shorter than palm ; dactyl with flexor margin concave , blade - like , with three distinct distal teeth , latter subequal in length ; fixed finger with flexor margin excavate , trowel - like , and with single distal tooth . second pereopod ( fig . 4