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JOURNAL OF MORPHOLOGY 253:166-175 (2002)

Clibanarius

(Crustacea, Anomura, D iogenidae)

aymond T. Bauer*

tment of Biology, University of Louisiana at Lafayette, Lafayette, Louisiana 70504-2451

Al though mat ing has been desc r ibed in sev

v e n o t p r e v i o u sl y b ee n d e m o n s t r a t e d . E v i d e n c e

Clibanat h e m a l e a p p l i e s a s p e r m a t o p h o r i c m a s s d i

ma ny o th e r decapo ds . Th e s ing le second p l eopod o fC. vittatus has a s imple endopod wi th no appar

I n d e c a p o d c r u s t a c e a n s , t h e im m o t i l e s p e r m a t o

a r e s u r r o u n d e d b y p r o t e c t i v e a n d a d h e s i v e m a

w h e n t r a n s f e r r e d t o t h e f e m a l e ( S u b r a m o -

, 1 9 9 3) . T h e s e s p e r m - b e a r i n g s t r u c t u r e s

a t o p h o r e s ) , f o r m e d p r i o r t o o r d u r i n g e j a c u l a

v a r y in s i z e , s h a p e , a n d c o m p l e x i t y . T h e p l a c e

e n t o f s p e r m a t o p h o r e s o n t h e e x t e r i o r o f t h e f e

l e o r w i t h i n s p e r m a t h e c a e is o ft en a c h i e v e d w i t h

o r m o r e p a i r s of m a l e g o n o p o d s , w h i c h a r e m o d

e d a n t e r i o r p le o p o d s ( a b d o m i n a l a p p e n d a g e s ) u t i

f or s p e r m t r a n s f e r in m a n y d e c a p o d s ( B a u e r ,

, s u c h a s c a r i d e a n s h r i m p s ( B a u e r , 1 9 7 6 ) ,

a e o i d e a n s h r i m p s ( B a u e r , 1 9 9 1 , 1 9 9 6 a , b ) , c a n i -r i d c r a y f i s h e s ( A n d r e w s , 1 9 1 1 ) , n e p h r o p i d l o b

s ( F a r m e r , 1 9 7 4) , a n d b r a c h y u r a n c r a b s ( C r o n i n ,

R y a n , 1 9 6 7 ) . I n s o m e d e c a p o d s , s u c h a s s t e -

s h r i m p s ( B a u e r , 1 9 8 6 ) a n d p a l i n u r i d l o b

r s ( P h i l l i p s e t a l . , 1 9 8 0 ) , t h e m a l e a n t e r i o r p l e o

s a r e n o t m o d i f i e d fo r s p e r m t r a n s f e r .

M a l e s o f a n o m u r a n s p e c i e s , i n c l u d i n g t h e h e r m i t

o f t h e s u p e r f a m i l y P a g u r o i d e a ( M c L a u g h l i n ,

p r o d u c e c h a r a c t e r i s t i c s p e r m a t o p h o r e s t h a t

p a r e n t l y a r e d e p o s i t e d o n t h e e x t e r n a l s u r f a c e o f

f e m a l e ( T u d g e , 1 9 9 9 a , b ) . T u d g e ( 1 9 9 1 , 1 9 9 5 ,

a n d S u b r a m o n i a m (1 9 9 3 ) d e s c r i b e d t h e

o m i n a n t s p e r m a t o p h o r e t y p e e n c o u n t e r e d i n

r o i d e a n c r a b s a s s t a l k e d o r p e d u n c u l a t e w i t h

e d i s t i n c t c o m p o n e n t s , t h e d i s t a l a m p u l l a , s t a l k .

apposed to t he ven t r a l cepha lo tho rax o f t he f emale . Ama ss ive am ou n t o f sem ina l sec r e t ion con ta in ing spe r m a t o p h o r e r i b b o n s , t e r m e d h e r e t h e s p e r m a t o p h o r i c m a s sand descr ibed for the f i r s t t ime in a hermi t crab species ,was obse rved cover ing the s t e rn i t e s and coxae o f pe r eo -pod s 1-5 of a rece nt ly copu lated fem ale . I t i s sug ges tedtha t du r ing copu la t ion the ma le emi t s t he con ten t s o f t hee j acu la to ry duc t s d i r ec t ly on to the f emale wi thou t t he a ido f gonopods o r gen i t a l pap i l l ae . A l though spe rmatophoret ransfer i s s imple in C. vittatus, the presence of modif ied

an te r io r p l eopods o r e longa te gen i t a l pap i l l ae ( sexua ltubes) i n o the r paguro idean spec i es sugges t s t he poss ib i l i t y o f a more complex insemina t ion p rocess i n t hese o the rh e r m i t c r a b s . J . M o r p h o l . 2 5 3 : 1 6 6 - 1 7 5 , 2 0 0 2 .

© 2002 Wiley-Liss. Inc.

KEY WORDS: gonopods ; gonopores : he rmi t c r ab ; spe r m a t o p h o r e : s p e r m t r a n s f e r

a n d p r o x i m a l p e d e s t a l . T h e s p e r m a t o z o a a r e s t o r e d

w i t h i n t h e a m p u l l a , w h i c h i s c o m p o s e d o f t w o h a l v e s

j o i n e d a l o n g t h e i r l a t e r a l r i d g e s ( T u d g e , 1 9 9 9 a ) . T h e

d i s t a l a m p u l l a r e s t s a t o p t h e s t a l k , w h i c h i s u n d e r

l a i n b y t h e p e d e s t a l o r b a s e o f t h e s t a l k . T h e p e d e s

t a l a p p e a r s t o f u n c t i o n a s t h e p o i n t o f a t t a c h m e n t fo r

t h e s p e r m a t o p h o r e t o t h e e x t e r n a l s u r f a c e of t h e

f e m a l e d u r i n g c o p u l a t i o n ( T u d g e , 19 9 9 b ). M o u c h e t

( 1 9 3 0 , 1 9 3 1 ) a n d H a m o n ( 1 9 3 7 , 1 9 3 9 ) s u g g e s t e d t h a t

t h e a m p u l l a s p l i t s a l o n g t h i s r i d g e , t e r m e d t h e l i n e

o f d e h i s c e n c e ( T u d g e 1 9 9 9 a ) o r "ligiie de suture"

( H a m o n , 1 9 3 7 ) , t h e r e b y r e l e a s i n g t h e s p e r m a t o z o a

( T u d g e 1 9 9 1 , 1 9 9 5 , 1 9 9 9 a , b ) . H a m o n ( 1 9 3 7 ) s u g g e s t e d t h a t m e c h a n i c a l o r o s m o t i c f o rc e s m i g h t

c a u s e t h e a m p u l l a t o f r a c t u r e a n d r e l e a s e t h e s p e r

m a t o z o a .

Contract grant sponsors: the Graduate Student Organization, University of Louisiana at Lafayette I DLL), and the Neptune Foundation.

'Correspondence to: Raymond T. Bauer, Department of Biology,University of Louisiana at Lafayette. Lafayette, Louisiana 70504-

2451. E-mail: [email protected]

Published online 20 May 2002 inWiley InterSeience (www.interscience.wiley.com) DOI; 10.1002/jmor.lll8

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G.S. HE SS AND R.T. BAUER

t h e r s t r u c t u r e s i n a v a r i e t y o f o t h e r d e c a p o d sue r , 1979 , 1998 , 1999) . Th i s b r i s t l i ng a r r a y o f

The gonopores of male Clibanarius vittatus a r er em ar k ab l e ap e r t u r e s gua r ded by f l ap - li ke ope r -

ns ion s of th e e jacula tory duc t s ) , as in se vera l

I n t he penaeo i d sh r i m p Sicyonia dorsalis,

en t o f t h e com pl ex gonopods ( pe t a sm a)ue r , 1996b) . T he lack of gen i ta l pa pi l l ae in m alesC. vittatus i nd i ca t e s t ha t e j acu l a t ed m a t e r i a l s i m

Dur ing the br ie f copula t ion of Clibanarius vittath e gonopo res of th e m ale a re ne ar to or in

tac t wi th th e ve nt r a l sur face of th e female cepha-O u r i n t e r p r e t a t i on i s t h a t w hen e j acu l a

r m a t op hor es i s em i t t ed fr om bo t h m a l e gono

T h e ro w s of s p e r m a t o p h o r e s , n e a t l y a r r a n g e d

ina l secre t ion i s spew ed out onto the fem ale

f e g g s w i t h s p e r m a t o p h o r e s d u r i n g s p a w n i n g

y cause t h e sp l i t t i ng o f t he i r l a t e r a l r i dges sub qu en t re lea se of spe rm atoz oa for fe r t i l i za t ion . Th e

t he m a j o r c l ean i ng and g r oom i ng appendage o f

A l t hough w e conc l ude t ha t t r ans f e r o f spe r m a t o Clibanarius vittatus i s a morphological ly

ods beca use of th e i r comp lex modi f ica t ions

of th e type see n in o th er decap od spec ies in

add i t i on , m any o t he r pagur o i dean spec i e s have p r o nounced gen i t a l pap i l l a e , t e r m ed " sexua l t ubes"( McL augh l i n , 1980; Lem a i t r e and Mc Laug h l i n ,1995) t ha t m i gh t be used t o p l ace spe r m a t ophor i cm asses o r spe r m a t ophor es d i r ec t l y on t he f em a l e i na more complex fashion than tha t observed in C.vittatus. S p e r m a t o p h o r e t r a n s f e r in h e r m i t c r a b s

spec i e s w i t h "gonopods" and s exua l t ubes need s t o bei nves t i ga t ed t o de t e r m i ne i f and how t hese s t r uc t u r e s a r e i nvo l ved i n i n sem i na t i on .

A C K N O W L E D G M E N T S

We t hank D r . F r ank Tr uesda l e f o r g r an t i ng acces sto and ass i s tance a t the col lec t ing s i t e in GrandeTer r e , Lou i s i ana . O ur spec i a l t hanks t o D r s . R a f ae lLem a i t r e and C hr i s t ophe r Tudge f o r sha r i ng t he i rexpe r t i s e i n t he sys t em a t i c s and r ep r oduc t i ve m or pho l ogy o f he r m i t c r abs . We t hank D r s . D a i r y ]Fe l de r , Lew i s D ea t on , and t he anonym ous r ev i ew er so f t he m an usc r i p t fo r he l p fu l co m m ent s and sugges t i o n s . Th i s i s C on t r i bu t i on 80 of t he U LL Lab or a t o r yof C r u s t a c e a n R e s e a r c h .

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Bauer RT. 1976 . Mat i ng behav i o r and spermat ophore t r ans fer i nt h e s h r i m p Heplacarpus piclus (S t i mpson) (Decapoda: Car i dea :Hi ppo l y t i dae) . J Na t Hi s t 10 : 415-4 40 .

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Ba ue r RT. 1986 . Phy l oge ne t i c t r en ds i n sperm t r ans fer and s t o r age compl ex i ty i n decapod crus t ace ans . J C rus t ac ean B io l6 : 3 1 3 - 3 2 5 .

B a u e r R T . 1 9 9 1 . S p e r m t r a n s f e r a n d s t o r a g e s t r u c t u r e s i n p e n a e o i d sh r i mps : a func t i ona l and phy l ogene t i c per spec t i ve . In :Bauer RT and Mar t i n JW. ed i t o r s . C rus t acean Sexual B i o l ogy .New York and Oxfo rd : Co l umbi a Un i ver s i t y , p .18 3 -207 .

B a u e r R T . 1 9 9 3 . S p e r m a t o p h o r e s a n d p l u g s u b s t a n c e o f t h e m a r i n e s h r i m p Trachypenaeus sirnilis ( C r u s t a c e a : D e c a p o d a :Peuae i dae l : fo rmat i on i n t he mal e r ep roduct i ve t r ac t and d i s pos i t ion in t he i n sem i na t e d f emal e . B io l Bu ll 18 5 : 174 -18 5 .

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and f emal e mo l t i ng i n decapod sh r i mp , u s i ng Sicyonia dorsalis( D e c a p o d a : P e n a e o i d e a ) . J C r u s t a c e a n B io l 1 6 : 4 2 9 - 4 3 6 .

Ba uer RT. 1996b . Ro l e o f t he pe t a sm a and a ppend i ce s m ascu l i naedur i n g copu l a t i on and i n sem i na t i on i n t he penaeo i d sh r i m p .Sicyonia dorsalis ( C r u s t a c e a : D e c a p o d a : D e n d r o b r a n c h i a t a ) .I n v e r t e b r R e p r o d D e v 2 9 : 1 7 3 - 1 8 4 .



SPERMATOPHORE TRANSFER IN A HERMIT CRAB 17 3

Fig . 6 . Clibanarius vittatus. S E M o f t h e s p e r m a t o p h o r i cm a s s o n c o p u l a t e d f e m a l e s ( H M D S d r i e d ) . A , C , E : F e m a l eprese rve d jus t a f te r copula t ion . B , D: Fem ale tha t h ads p a w n e d b e t w e e n c o p u l a t i o n a n d p r e s e r v a t i o n . A : S p e r m a t o

phor i c mass sur rounding the gonopores (gp) and cove r ing thes t e rn i t e s and coxae of pe reopods 1-4 . Note s emina l s ec re t ion( s sl a n d s p e r m a t o p h o r e s ( s p ) w i t h i n t h e s p e r m a t o p h o r i c m a s s .B : R e m n a n t s o f a s p e r m a t o p h o r i c m a s s ( u n l a b e le d a r r o w s ) o na recen t ly spawn ed female , gp , gonopo re . C: H ighe r magni f ica t ion of spe r ma toph or i c m ass f rom A. Note rup tur ing ofs p e r m a t o p h o r e s . s p . s p e r m a t o p h o r e ; s s , s e m i n a l s e c r e t i o n s . D :High er magni f i ca t ion of B show ing rem na nt s o f t he spe rm a top h o r i c m a s s a n d r u p t u r e d s p e r m a t o p h o r e s ( s p ). s s , s e m i n a ls ec re t ion . E : H ig he r magni f i ca t ion of spe rm a top hor e f rom Cshowin g ru p t ur e a long the l i ne of deh i s cence (com pare to Fig .3 E ) . Scale ba r = 1 mm in A and B, 200 urn in C, 100 y.m in Da n d E .

p leo p o d sh o ws n o o b v io u s mo d i f i ca t i o n for t h e ro l e o f f emale p l eo p o d s in i n c u b a t io n o f em -e r m a t o p h o r e t r a n s f e r . A l t h o u g h t h e s e c o n d b r y o s . T h e p l e o p o d s o f f e m a l e s , r e l a t i v e l y l a r g e r

C. vittatus i s s e x u a l l y d i m o r p h i c , t h e a n d m o r e s e t o s e t h a n t h o s e o f m a l e s , s e r v e a sb e t w e e n t h e s e x e s c a n b e a t t r i b u t e d t o a t t a c h m e n t s i t e s fo r e m b r y o s . T h e s e t a e of f e m a l e

"1 ^

-• ' ••' $ > J



G.S. HE SS AND R.T. BAUER

5. Clibanarius uittatus. P o s i t i o n o f t h e s p e r m a t o p h o r i con the fema le . A : Pho togra ph of a fema le prese rv ed j u s t

spin, s p e r m a t o p h o r i c m a s s . B : D r a w i n g of t h eA d e p i c ti n g s p e r m a t o p h o r i c m a s s ( sp m ) c o v e ri n g t h e

pi—5, pereopods 1—6. C:

ra luc ida dra wi ng of a fema le th a t had copula t e d 2 .5 h

o n a n d p r e s e r v a t i o n . N o t e t h e r e m n a n t s of t h e s p e r m a t o

and 4 (p4) . Scale b ar = 1 cm for B and C.

r o f t h e s p e r m a t o p h o r i c m a s s f ro m t h e m a l e

pos i t ion of the spe rm a top ho r ic ma ss on the fe

the m a le gonopores ra t he r tha n wi th th e a id of go n o p o d s o r o t h e r i n t r o m i t t e n t s t r u c t u r e s .

T he use of modif ied f irst a nd seco nd pleop ods a sg o n o p o d s f or s p e r m a t o p h o r e t r a n s f e r h a s b e e nd e m o n s t r a t e d i n d e c a p o d g r o u p s s u c h a s c a r i d e a ns h r i m p s ( B a u e r , 1 9 7 6 ; B e r g a n d S a n d i f e r , 1 9 8 4 ),

p e n a e o i d e a n s h r i m p s ( B a u e r , 1 9 9 1 , 1 9 9 6 b ) , c a m -b a r i d c r a y f i sh e s ( A n d r e w s , 1 9 1 1 ), n e p h r o p i d l ob s t e r s ( F a r m e r , 1 9 7 4 ) , a n d b r a c h y u r a n c r a b s ( C ro -n in , 1947 ; Ry an , 1967) . M a le s o f Clibanariusvitlatus do no t have f i r s t p l eopods and the s ing le



S P E RMA T OP HORE T RANS F E R IN A HE RM IT CRAB 171

Fig. 4. Clibanarius vi.ttatus. Copula to r y pos i t ion m ode led f r om v ideo r ecor d ings o f copula t ionand f r om pr ese r v ed spec im e ns p laced in m a t in g pos tu r e . The m a le ( unsha ded , above f em a le ) hasthe gonopor e a r ea n ea r the ven t r a l su r face o f the pos te r io r ceph a lo tho r ax o f the f em a le ( d a r ks h a d i n g ) , a b , a b d o m e n : p l - p 5 , per eopods 1 - 5 .

f th e female in i t s gas t r opo d she l l , a s desc r ibed

t ra l s u r fa c e s o f th e c e p h a lo th o r a x o f

e pos te r io r ve n tr a l su rface of th e pe reopod 1-4e n t s (F ig. 4 ) . T h e m a le a n d fe ma le w a lk in g l e g s

—5 a r e he ld ou tw ard f rom th e ceph a lo th orax a t

c o n ta c t w i th th e f e ma le . In th e th r e e m a t in g

but on ly fo r 5 sec in the th i rd . One of the th reeles f rom the se pa i r s wa s p re se rv ed 2 .5 h a f te r

fem ales , p re se rv ed a t leas t 6 h a f te r co pula t ion ,

S p e r m a t o p h o r i c M a s s

Th e s ing le fema le p res e rve d ju s t a f te r copula t ionh a d a l a rg e o p a q u e g e la t in o u s ma s s c o v e r in g th ev e n t ra l s u r fa c e o f th e c e p h a lo th o ra x f ro m p e re o p o d s1-4 , inc lu d ing the gonopore s (F ig . 5A,B) . Th e adhes iv e s e m in a l s e c re t io n s a t t a c h e d th e s p e rm a to -pho res to th e s te rn i te s and coxae of th e fem ale .Mic ro s c o p ic e x a min a t io n o f th e ma s s p r io r to S E Mre v e a le d lo n g r ib b o n s o f u n ru p tu re d s p e rm a to -p h o re s e mb e d d e d w i th in a m a s s o f s e min a l s e c re t ion . The dehydra t ion p rocess fo r SEM caused theses p e rma to p h o re s to ru p tu re (F ig . 6 A ,C ,E ) . De h y d ra t io n a l s o c a u s e d s o me s h r in k a g e in b o th th e s e min a ls e c r e t i o n a n d s p e r m a t o p h o r e s .

In a n o th e r c o p u la t e d f e ma le , p re s e rv e d 2 .5 h a f t e rc o p u la t io n , s p a wn in g h a d o c c u r re d b u t r e mn a n t s o fa s p e r m a t o p h o r i c m a s s r e m a i n e d , c o v e r i n g t h ecoxae o f pe reo pod s 4 - 5 a s we ll a s th e s te rn i te s ofp e re o p o d s 3 -5 (F ig s . 5 C , 6 B ,D) . Ob s e rv a t io n s ma d ef i r s t w i th a s t e re o mie ro s c o p e a n d th e n S E M s h o we dt h a t r u p t u r e d s p e r m a t o p h o r e s w e r e s t i l l p r e s e n t o nthe coxae o f pe reopods 3 as we l l a s the coxae ands te rn i te s o f pe reopods 4 (F ig . 6B,D).

D I S C U S S I O N

Ha zle t t (1996) f irst no ted th e p rese nce o f a spe rma to p h o r i c ma s s o n re c e n t ly c o p u la t e d f e ma le s o fClibanarius vittatus. In th e p re s e n t s tu d y , we d e s c r ib e th e s p e rm a to p h o r i c m a s s o f a h e rm i t c ra bspecies in deta il for the firs t t ime. I t is composed of



0 G.S. HESS AND R.T. BAUER

Fig. 3 . Clibanarius vittatus. A: Light micrograph of a r ibbon ofs p e r m a t o p h o r e s ( s p ) s u r r o u n d e d w i t h s e m i n a l s e c r e t i o n s ( s s )wi t h i n t he d i s t a l mo s t r eg i on o f t he va s deferens , ed , e j acu l u t o ryduct . B : En l arg em en t o f A t o show de t a i l of t he sper ma t opho res( sp) and t h e i n t e rcon nec t i ng ba sa l r eg i on (b ) be t we en t wo sper ma t opho res . sz , sperm at ozo a wi t h i n a spe rma t oph ore . C : Confo-ca l mi crog raph o f s i ng l e sper ma t oph ore con t a i n i ng spe rmat o zoa( sz) . D: SEM of t wo HM DS-d r i ed sp erm at oph ores ( sp ) d i s sec t edf rom t he e j acu l a t o ry duc t , s s , semi na l secre t i on . E : SEM of acr i t i ca l -po i n t -d r i ed spe rma t oph ore wi t h cha rac t e r i s t i c l i ne o f dehiscence ( Id) . Scale bar = 500 \t.m in A, 100 |j.m in B, 50 (xm in C,40 |xm in D, and 30 |o.m in E.

en s o f t he va sa de f e r en t i a and e j acu l a t o r y duc t s t hem se l ve s cause d t he l a t t e r t o r u p t u r e a long t he i r

i n a l s e c re t io n or t h e s p e r m a t o p h o r e s

l a t e r a l r i dges .

D e s c r i p t i o n o f C o p u l a t i o n

U pon con t ac t w i t h a r ecep t i ve f em a l e , t he m a l ebeg an p r ecop u l a t o r y behav i o r , a t ap p i n g and r o t a t -



S P E R M A T O P H O R E T R A N S F E R I N A H E R M I T C R A B 1 69

Fig. 2. Clibanarius villains. Sexua l d imorp hi sm in reproduc t ive morphology of gonop ores and s econd p leopods . A : SEM of ma lepores (gp) and o perc ulum (o) located on the coxae of th e f i fth pere opo ds (HM DS dried ! . B : SE M of female gon opo res (gpl on coxae

th i rd pe reopods (H MD S dr i ed) . C: Ante r io r v i ew of s econd p leopod of ma le ( sh i e ld l eng th = 10 .5 mm ) wi th s e t a e removed , en ,pod; ex, exopod. D: Anterio r view of second pleopod of fema le (shie ld leng th _ 6.3 mm) wi th s e t ae removed , en , endopod; ex ,

SEM of ma le pleopod seta (s t ) and s etu les (su) (cr i t ica l -p oint -d ried) . F : SEM of den se ar ray of female pleo podal 2 se tules ;ind ica t e s m ul t id i g i t a t e s ca l e subse tu l e ( s c ) on s e tu l e (HM DS dr i ed) . G : SE M of a s ing le ma le p l eopod 2 s e tu l e w i th s imp le s ca l e

se tu l e s ( s c) (c r i t ica l -po in t -dr i ed) . H : SEM of fema le s e tu l e w i th mu l t id ig i t a t e s ca l e subse tu l e s ( s c ) (HM DS dr i ed) . Sca le ba r - 1 m m\xm in E, 40 pjm in F, 2 p.m in G, and 4 p.m in H.



G.S. HESS AND R.T. BAUER

gPvd

Fig. 1. Clibanarius vittatus. Tes tes and vasa de i ' e ren t ia t e rmina t ing wi th in the pereopod 5coxae as e jaeu la to ry d uc t s th a t open to the ex te r io r th ro ugh the gonopores . c, coxa; gp . gonopore ;t , t es t i s ; vd , vas defe rens . Sca le bar = 1 nn t i .

g . 2 B ) . T h e s t e r n u m b e t w e e n t h e t h i r d

ina t io ns o f th e exosk e le ton o r ape r s s u g g e s t i v e of t h e f e m a l e s p e r m - s t o r a g e s t r u c

a n d s p e r m a t h e c a e of p e n a e o i d e a n s h r i m p s

e r , 19 91 , 1993 , 1996a ,b ) , c am bar id c ray f i shesnd rew s , 1905, 1906, 1908; Ho bbs , 1974) , and ne-

( F a r m e r , 1 9 74 ; A i k e n a n d W a d d y ,

st two pair s of pleopod s are modified as go nopodsClibanarius vittatus, as in many

of th e abdo m en. Th e firs t abdo m inal som ite oflacks a p leopod in both males and females

The pleopods ai-e bi ramous , wi th both an endopod

of m ales an d females

and wid th to th e endopod, whi le in male s the exopod islonger and bro ader th an the endopod (Fig . 2C,D). Bothth e endopod an d exopod of fem ale pleopod 2 possess agrea ter number and proport iona l ly longer se tae andse tule s tha n th ose of th e mal e (Fig . 2E,F) . The se tu lesof p leopod 2 se ta e of the ma le a re sparse ly equippedwith s imple scale subsetules (Fig. 2G), wlii le those of

the female a re dense ly covered wi th mul t id ig i ta tesca le subse tules (Fig . 2F.H).

S p e r m a t o p h o r e s a n d S e m i n a l S e c r e t i o n

Sp erm a to ph ore s of th i s spec ie s a re fo rmed p r io r toe jacu la t ion and can be obse rved wi th in the lumensof the vasa d e fe ren t i a a nd e jaeu la to ry duc t s (F igs . 1,3 A , B ) . E a c h n o n p e d u n c u l a t e s p e r m a t o p h o r e i s c o m posed o f two ha lv es me e t in g a t a ra i s e d l ine t e rm edthe " l a t e ra l r idge" o r " l ine o f deh i s cence" (Tudge ,1991 , 1 9 9 9 a ) , f o r m i n g t h e a m p u l l a o f t h e s p e r m a t o phore (F ig . 3D,E) . Spe rma tozoa can be obse rvedwi th in the am pu l l a (F ig . 3B ,C) . Be low the am pu l l ais a basa l region (Fig . 3B) tha t ac ts as a connect ingc o r d a t t a c h i n g a d j a c e n t s p e r m a t o p h o r e s w i t h i n t h e



SPERMA TOPHORE TRANSF ER IN A HERMIT CRAB 167

Mouche t (1931) . Hamon (1937 , 1939) , Ma thewsG r e e n w o o d ( 1 9 72 ) , a n d U m a a n d S u b r a m o -

Dardanus asper (Diogenidae) form a con

c o n t r a c t i o n s of t h e s u r r o u n d i n g m u s c u l a r

c s h a p e o f t h e s p e r m a t o p h o r e .

A l t h o u g h a s p e c t s of s p e r m a t o p h o r e f o r m a t i o n

; M a th ew s , 1953), the me cha m b y w h i c h s p e r m a t o p h o r e s a r e t r a n s m i t t e d

ma laven i , 1949 ; M a the ws , 1956 ; Haz le t t , 1966 ,Am eyaw-Ak fumi . 1975). The purpo se of th i s

C/ibanarius vittatun.t he an te r io r p leopods of the m a le ,

, s p e r m a t o p h o r e s , a n d s p e r m a t o p h o r i c

A N D M E T H O D S

Live spec imens o f Clibanarius vittatus (Bosc ,w ere col lec ted in Ju ly and A ug us t 1999 from

m a t i n g o b s e r v a t i o n s . T h e h e r m i t c r a b s w e r e

w a t e r t a b l e s y s t e m w i t h w a t e r t e m p e r a t u r e

T e s t e s a n d v a s a d e f e r e n t i a c o n t a i n i n g s p e r m a t o

The crabs were f i rs t anes the t ized by chi l l ing ,

s t r a ig hte n th e abd om ens for ease of d issecan d the n f ixed in 10% form al in . Eja cula tory

the d i s t a lm os t po r t ions o f the vasa de fe ren t i a

g e lec t ron m icroscopy (SEM ). Th e freshly d is rent i a of one m ale wer e p laced in

enated s ea w ate r for 1 h and then placed in 10%

by wa sh i ng wi th s eaw a te r fo r 30 m in , s t a ined wi thFM 464* (Red l ipoph i l i c marke r ) and Sy to 13*(g reen nuc lea r marke r ) fo r 30 min and examinedwith a confoca l microscope (Biorad® MRC 1024 ES).

Dr aw ings of t e s t e s and p leopods were m ad e u s inga camera luc ida moun ted on a s t e reomic roscope .Ma te r i a l pho tographed us ing l igh t mic roscopy wasfirst f ixed in 10% se aw at er form alin for 1 h, wa sh ed

twice wi th seawater for 20 min, s ta ined wi th ac idfuchs in , and c leared wi th CMCP-10 high viscos i tym o u n t a n t .

For obse rva t ion o f morpho logy wi th SE M,fo rm a l in -p re se rved va sa de fe ren t i a , spe rm a to phor es , app end age , and po r t ions of the ceph a lo tho-rax f rom va r ious ind iv idu a l c rabs were wa she d tw icefor 15 min with a 0.2 M PBS (pH 7.2) (Tudge, 1992)to remove re s idua l fo rma l in and then dehydra tedwi th a g raded e thano l s e r i e s (20-100%) . Spec imenswe re e i the r c r i t i c a l -po in t -d r i ed wi th C 0 2 or a i r -dr iedaf te r t rea tment wi th a 1 :1 solut ion of 100% hexam-

e thy ld i s a l i zane (H MD S) and 100% e thano l for 20min fol lowed by im m ers io n in 100% HM DS . Al l specim ens we re spu t t e r -coa te d w i th go ld for 1 -6 minbe fo re v iewing them in a JEOL 6300-FV SEMequipped wi th a d ig i t a l image -cap tu re sys tem.

To a s se s s ova r i an m a tu r i ty for m a t in g obse rva t i o n s , fema le he rmi t c rabs were removed f rom she l l sby gen t ly he a t in g the apex o f the i r ga s t ropod she l l swi t h a bu ta ne c iga re t t e l igh te r . N in e teen fema le sw ith m at ur e ov ar ies ( fu ll of v i te l logenic oocytes ) , butw i t h o u t e m b r y o s or r e m n a n t s of e g g m e m b r a n e s o nthe p leopods , we re ind iv idua l ly pa i red wi th a ma le

in aqu ar ia . Act iv i t ies were recorded for 1 day a t a24-h recording speed (f ive f rames /sec) wi th a t ime-lapse v ideo recor der sys tem a t t ach ed to an infrared -sens i t ive su rve i l l an ce cam era equ ipped wi th a 3 0 -180 m m zoom lens . I l lu m ina t ion cons is ted of two 880nm in f ra red l amps dur ing the n igh t (da rk ) pe r iodan d two 40 -w at t fluorescent lam ps for day (l igh t)obse rva t ions . V ideo tapes were rev iewed da i ly to de t e r m ine if copu la t ion ha d occur red . W hen copu la t ionwa s observe d on a ta pe (3 of 19 pa i r ings ) , th e pa i rswere p re se rved in 10% sea wa te r fo rma l in and th efema le s were l a t e r examined fo r the p re sence o r

absence o f spe rm a top hor es and s em ina l s ec re t ions .One add i t iona l copu la t ion was obse rved on a wa te rt ab le and the ma t ing pa i r was immedia te ly p re s e rved and l a t e r examined a s in the o the r th reep a i r s .

R E S U L T S

G o n o p o r e a n d P l e o p o d M o r p h o l o g y

Th e dis t a l ends of th e va sa deferen t ia , th e e jacula tory du ets , a r e loca ted wi th in the coxae of th e f if th

pereopods of the male and open to the exter ior v iathe gonopores (Figs . 1 , 2A). These openings a regu ard ed by f lap- like oper cula (Fig . 2A). T he femalegonopo res , the e x te rn a l open ings of the ov iduc t s , a r e

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