HELGOLA.NDER MEERESUNTERSUCHUNGEN Helgol/~nder Meeresunters. 52, 59-64 (1998)
"Cleaner" shrimps?
Stephen Spotte
Marine Sciences & Technology Center, The University of Connecticut at A v e r y Point; Groton, Connecticut 06340-6097, USA
[860] 572-0202 (telephone); [860] 572-7700 (fax) e - m a i h s t e p h e n . s p o t t e @ s n e t . n e t
ABSTRACT: In the western North Atlantic, some shrimps of the genus Peridimenes interact with fishes. According to prevailing wisdom, these shrimps "clean" the fishes (i. e. they remove parasites, diseased tissue, or detritus from their exposed surfaces). With one exception, the numerous litera- ture entries recite anecdotal evidence. The only report based on empirical studies has dismissed the notion that "cleaner" shrimps perform the services attributed to them, leaving the nature of the relationship unresolved.
I N T R O D U C T I O N
T h e s c e n e is a coral reef. A fish a p p r o a c h e s a s h a l l o w l e d g e o c c u p i e d by a sea a n e m - one. S t a n d i n g a m o n g the a n e m o n e ' s t e n t a c l e s is a shrimp. T h e shrimp starts to w a v e its a n t e n n a e . H a v i n g r e a c h e d the ledge, the fish rolls p a r t w a y onto its side a n d r e m a i n s mo- tionless. Q u i c k l y the shrimp a b a n d o n s the a n e m o n e a n d climbs onto the fish, r o a m i n g o v e r its sides a n d back, e v e n d i s a p p e a r i n g b e n e a t h a flared operculum. T h e shrimp soon e m e r g e s into the fish's o p e n mouth, t e e t e r s m o m e n t a r i l y on the fish's lower lip, a n d ab- ruptly e n d s the association by flipping b a c k w a r d a n d settling on the a n e m o n e . After r i g h t i n g itself, the fish swims away. What has j u s t h a p p e n e d ?
A c c o r d i n g to p o p u l a r wisdom, t h e shrimp p e r f o r m e d n e e d e d services by r e m o v i n g parasites, d i s e a s e d tissue, a n d p e r h a p s e v e n detritus particles from the fish's surfaces. Both parties h a v e b e n e f i t e d , the fish by r e c e i v i n g a " c l e a n i n g " , the shrimp by g a i n i n g a meal. An o p e n a n d shut case of mutualism, or so it seems. In this brief essay [ t r a c e the p u b l i s h e d history of " c l e a n i n g symbiosis" as it r e l a t e s to " c l e a n e r " shrimps of the w e s t e r n North Atlantic, s u m m a r i z e existing e v i d e n c e in s u p p o r t or refutation of " c l e a n i n g " , a n d s p e c u l a t e on w h y w e find the c o n c e p t of o n e a n i m a l s p e c i e s " c l e a n i n g " a n o t h e r so com- pelling.
HISTORY OF " C L E A N I N G SYMBIOSIS"
E i b l - E i b e s f e l d t (1955) first o b s e r v e d small fishes " c l e a n i n g " l a r g e r ones. H e p r o p o s e d the t e r m " P u t z s y m b i o s e n " ( " c l e a n i n g s y m b i o s i s " ) to d e s c r i b e the r e m o v a l of parasitic c r u s t a c e a n s by " c l e a n e r s " from host fishes. E i b l - E i b e s f e l d t did not actually s e e p a r a s i t e s b e i n g r e m o v e d a n d m a d e no direct test of his h y p o t h e s i s .
Its l e a d i n g p r o p h e t a n d provisor w a s C o n r a d L i m b a u g h . E i b l - E i b e s f e l d t ' s m o d e s t "Putz- s y m b i o s e n " w a s s w e p t a s i d e as L i m b a u g h et al. (1961:237) b o l d l y d e c l a r e d : " C e r t a i n s p e - cies of small, brightly c o l o r e d s h r i m p s h a v e b e e n o b s e r v e d to r e m o v e a n d e a t p a r a s i t e s , i n j u r e d tissue, a n d p o s s i b l y u n d e s i r a b l e food p a r t i c l e s from a l a r g e v a r i e t y of c o o p e r a t i n g reef fishes." A l t h o u g h d a t a w e r e not p r e s e n t e d , this s t a t e m e n t - simple a n d d i r e c t - left no room for doubt. In t h e brief t i m e a l l o t t e d t h e m - a few m i n u t e s at m o s t - " c l e a n e r s " h a d to c a r r y out the g a r b a g e , d i s t i n g u i s h p a r a s i t e s a n d f o r e i g n items from h e a l t h y tissue, m a k e e m e r g e n c y m e d i c a l decisions, a n d p e r f o r m d e l i c a t e surgery. S u c h r e s p o n s i b i l i t i e s r e q u i r e d s t r o n g m u t u a l i s t i c b o n d s b e t w e e n " c l e a n e r s " a n d hosts, a fact n o t lost on Lim- b a u g h et al. (1961) w h o p r o n o u n c e d " c l e a n e r s " to b e e x e m p t from p r e d a t i o n .
" C l e a n i n g symbiosis" - or r a t h e r its a b s e n c e - w a s b e l i e v e d to h a v e h u g e e c o l o g i c a l c o n s e q u e n c e s . L i m b a u g h et al. (1961:237) d e s c r i b e d the effect of r e m o v i n g " c l e a n e r " fishes a n d s h r i m p s from sections of a B a h a m i a n reef: "The o b s e r v e d r e s u l t w i t h i n a few w e e k s w a s a r e d u c e d n u m b e r of reef fishes a n d a h i g h i n c i d e n c e of fishes w i t h f r a y e d fins a n d u l c e r a t e d sores." A l t h o u g h this s t a t e m e n t w a s p u r e l y a n e c d o t a l , the " c l e a n i n g " sta- tion as s w i m - i n clinic n o n e t h e l e s s b e c a m e d o g m a . Sefton (1977:37), for e x a m p l e , wrote: "For the c l e a n e r s it is a c o n t i n u i n g b a n q u e t , a n d for the c l e a n e d it is a n e s s e n t i a l visit; ex- p e r i m e n t s s h o w that without the b e n e f i t of c l e a n e r s , fishes m a y s i c k e n a n d e v e n t u a l l y die from u n c h e c k e d p a r a s i t e s . " No s u c h e x p e r i m e n t s , of course, h a d b e e n p e r f o r m e d . Lim- b a u g h (1961:45) s u m m e d up his proof w i t h o u t e v i d e n c e w i t h this s t a t e m e n t : " A m o n g the o r g a n i s m s I h a v e n o t e d in t h e s t o m a c h c o n t e n t s of c l e a n e r s [ p r e s u m a b l y b o t h fishes a n d shrimps] are c o p e p o d s a n d i s o p o d s . . . . "
F o l l o w i n g L i m b a u g h ' s p u b l i c a t i o n s , s i g h t i n g s of " c l e a n i n g symbiosis" i n c r e a s e d . In the w e s t e r n North Atlantic s e v e r a l s p e c i e s of s h r i m p s w e r e p u r p o r t e d l y at w o r k "clea- n i n g " fishes. Literature e n t r i e s a c c u m u l a t e d as n e w e y e w i t n e s s a c c o u n t s w e r e d e s c r i b e d a n d l a t e r c i t e d uncritically. Putative " c l e a n e r s " e v e n t u a l l y i n c l u d e d
Periclimenes
an tho-philus
Holthuis & Eibl-Eibesfeldt, 1964 ( S a r g e n t & W a g e n b a c h , 1975); P.pedersoni
C h a c e , 1958 (Chace, 1958; Collette & Talbot, 1972; Colin, 1972; Criales, 1979; C r i a l e s & Corredor, 1977; Feder, 1966; Holthuis & E i b l - E i b e s f e l d t , 1964; J o n a s s o n , 1987; J o h n s o n & Ruben, 1988; L i m b a u g h , 1961; L i m b a u g h et al., 1961; M a h n k e n , 1972; R o e s s l e r & Post, 1972; Ross, 1983; S a r g e n t & W a g e n b a c h , 1975; Sefton, 1977; S m i t h & Tyler, 1973; Wick- sten, 1995; Williams, 1984; Williams & Williams, 1979); P.yucatanicus
(Ives, 1891) (Feder, 1966; J o n a s s o n , 1987; L i m b a u g h et al., 1961; M a h n k e n , 1972; Roessler & Post, 1972; Ross, 1983; S p o t t e et al., 1991; W i c k s t e n , 1995);Lysmata grabhami
(Gordon, 1935) (Criales, 1979; C r i a l e s & Corredor, 1977; Feder, 1966; J o n a s s o n , 1987; L i m b a u g h et al., 1961; Roes- sler & Post, 1972; Ross, 1983; Wicksten, 1995);Stenopus hispidus
(Olivier, 1811) (Criales & Corredor, 1977; Feder, 1966; J o n a s s o n , 1987; L i m b a u g h et al., 1961; R o e s s l e r & Post, 1972; Ross, 1983; Wicksten, 1995); S.scutellatus
Rankin, 1898 (Criales & C o r r e d o r , 1977; Feder, 1966; L i m b a u g h et al., 1961; Ross, 1983; W i c k s t e n , 1995); a n dBrachycarpus biun-
guiculatus
(Lucas, 1849) (Corredor, 1978; C r i a l e s & Corredor, 1977).THE E V I D E N C E
" C l e a n e r " shrimps? 61
r e m o v e d c r u s t a c e a n parasites (juveniles of
Anflocra
sp.) from a live fish u n d e r laboratory conditions, b u t p r o v i d e d no data. L i m b a u g h et al. (1961:245) wrote: "Parasites are remo- v e d as the s h r i m p m o v e s rapidly over the fish. In this o p e r a t i o n it pulls directly at the parasite or o p e n s the tissue s u r r o u n d i n g it." F. A. C h a c e Jr., o n e of L i m b a u g h ' s coauthors, later a d m i t t e d that this s t a t e m e n t was conjectural: the r e m o v a l of parasites h a d not b e e n o b s e r v e d (Tumbull, 1981).Factors that elicit a n d direct the " c l e a n i n g " r e s p o n s e are poorly described. A c c o r d i n g to Colin (1972:2),
P. pedersoni
d e m o n s t r a t e s " c l e a n i n g b e h a v i o r towards a n e s t h e t i z e d fish, p a p e r fish models, p a p e r fish shapes, a n d p a p e r rectangles." W h e n the s h r i m p were satiated with food, " c l e a n i n g " b e h a v i o r was not seen. A m o d e l m a d e of white p a p e r with i n k e d features elicited the greatest n u m b e r of " c l e a n i n g " responses, e v e n m o r e t h a n a n a n e s t h e t i z e d fish, i n d i c a t i n g that olfaction m i g h t not be important. S a r g e n t & W a g e n b a c h (1975) dissected b e h a v i o r a l aspects of the " c l e a n i n g " s e q u e n c e .Others h a v e tried to q u a n t i f y " c l e a n i n g " activity by r e c o r d i n g the n u m b e r of "clean- ing" e v e n t s or the n u m b e r of host fishes (individuals or species) that are " c l e a n e d " (e.g., Criales, 1979; Criales & Corredor, 1977; J o h n s o n & Ruben, 1988; Jonasson, 1987; M a h n - ken, 1972; Wicksten, 1995). J o n a s s o n (1987) tested " c l e a n i n g " efficacy in three species of shrimps a n d e v e n d e v i s e d a " C l e a n i n g Efficiency Index" to c o m p a r e scores. Like others before him, he p r o v i d e d no direct m e a s u r e of w h a t was monitored.
O n l y T u r n b u l l (1981) has properly assessed " c l e a n i n g symbiosis" by a shrimp. His u n p u b l i s h e d d i s s e r t a t i o n d e s c r i b i n g i n t e r a c t i o n s of
P. pedersoni
with four species of ser- ranids in the B a h a m a s set a n empirical s t a n d a r d in the a t t e m p t to m e a s u r e a n y costs or benefits d e r i v e d from " c l e a n i n g symbiosis."T u r n b u l l s p e n t more t h a n 5 years on the project, i n c l u d i n g 343 hours of direct obser- v a t i o n u n d e r w a t e r . He collected s e r r a n i d s by spear, s u r v e y e d a n d identified their exter- n a l parasites, a n d m a d e "infestation m a p s " to d e t e r m i n e w h e r e o n the fishes parasites were most p r e v a l e n t . By p h o t o g r a p h i n g
P. pedersoni
in the act of " c l e a n i n g " he w a s able to m a k e " f e e d i n g m a p s " for c o m p a r i s o n with his "infestation maps". In other experi- m e n t s i n v o l v i n g P.pedersoni,
T u r n b u l l tested i m m u n i t y to predation, d e t e r m i n e d which foods were e a t e n u n d e r different conditions, a n d e x a m i n e d physical characteristics of the principal f e e d i n g structures of the s h r i m p to e v a l u a t e " c l e a n i n g " capability.T u r n b u l l also p l a c e d a n acrylic h e m i s p h e r e perforated with tiny holes over a n as- s e m b l a g e of 18
P. pedersoni
o c c u p y i n g a single a n e m o n e , p r e v e n t i n g the s h r i m p from p o t e n t i a l " c l e a n i n g " activities for 42 days. F o r e g u t contents of these " n o n - i n t e r a c t i v e " shrimp were c o m p a r e d with those of "interactive" shrimp collected d u r i n g " c l e a n i n g " activities or i m m e d i a t e l y afterward. O t h e r fishes were captured, s t a i n e d i n situ with a l c i a n blue (selective for mucins), a n d r e l e a s e d to b e " c l e a n e d " by shrimp.sites, p e r h a p s as a direct result of i n f l a m m a t i o n i n d u c e d by parasitism. T h e s h r i m p were t r a p p i n g this m a t e r i a l u s i n g c h e l a e of the first a n d second p e r e o p o d s or the flagella. T h e shrimp also a p p e a r e d to feed on tiny detritus clusters p r e s e n t on the skin of host fishes. Despite visible a b r a s i o n s on m a n y of the fishes, tissue f r a g m e n t s were n e v e r r e m o v e d by shrimp.
" N o n - i n t e r a c t i v e " shrimp fed e x t e n s i v e l y on detritus, algae, a n d their o w n a n e m - ones. Their foreguts c o n t a i n e d calcareous s e d i m e n t a n d algae from the s u b s t r a t u m in ad- dition to n e m a t o c y s t s a n d z o o x a n t h e l l a e from a n e m o n e tissues. T h e s e s h r i m p w e r e n e v - er o b s e r v e d to p u r s u e or seize free-living crustaceans. Foregut c o n t e n t s of "interactive" shrimp c o n t a i n e d only fish skin m u c u s or small a m o u n t s of detritus.
Shrimp w e r e occasionally s w a l l o w e d by their host fishes, which r e f u t e d the i m m u - nity-to*predation hypothesis. Shrimp i m p r i s o n e d inside the acrylic h e m i s p h e r e s u r v i v e d without a p p a r e n t harm, d e m o n s t r a t i n g that their livelihood was not d e p e n d e n t on food o b t a i n e d d u r i n g " c l e a n i n g . " As T u r n b u l l (1981:37) stated, " . . . the r e m o v a l of m u c u s a n d detrital particles from the surfaces of s e r r a n i d s r e p r e s e n t s only one facet of the overall tro- phic position of
Peridimenes pedersoni
as a n omnivore." S c a n n i n g e l e c t r o n microscopy i n d i c a t e d a structural basis for n o n p r e h e n s i l e feeding, p e r h a p s by e n t r a p m e n t of food items ( i n c l u d i n g fish mucus) in setae of the principal f e e d i n g a p p e n d a g e s . From Turn- bull's findings, P.pedersoni
a p p e a r s to lack a m e c h a n i s m for c a p t u r i n g a n d t h e n g r a s p i n g prey, a n d its first two p e r e o p o d s s e e m i n c a p a b l e of p e r f o r m i n g "surgery."Turnbull therefore rejected the n o t i o n that " c l e a n i n g symbiosis" is c o m m e n s a l (i. e., host fishes n e i t h e r shelter the shrimp nor share food with them). T h e q u a n t i t i e s of m u c u s r e m o v e d w e r e minimal, c a u s i n g no d i s c e r n i b l e i n j u r y to the hosts. Parasitism on host fishes could therefore b e e l i m i n a t e d , a l t h o u g h the shrimp were clearly p r e y i n g on their a n e m o n e s . Without direct e v i d e n c e of b e n e f i t to the host, m u t u a t i s m could be rejected too. T u r n b u l l w a s left with de Bary's original definition of symbiosis (de Bary, 1879:5); that is, " . . . des Z u s a m m e n l e b e n s u n g l e i c h n a m i g e r O r g a n i s m e n " (the living t o g e t h e r of two dissimilarly n a m e d organisms). This is symbiosis d e f i n e d in an u n r e s t r i c t e d s e n s e with- out costs or benefits (Saffo, 1992). As Saffo (1992:18) noted, de Bary's d e f i n i t i o n " . . . is a n association b y i n t i m a c y of interaction, rather t h a n by the c o n s e q u e n c e s of that inter- action."
DISCUSSION
Ross (1983:193) wrote, " C l e a n i n g symbiosis is surely one of the most r e m a r k a b l e of all ecological a n d b e h a v i o r a l a d a p t a t i o n s . " W h e r e "cleaner" shrimps are c o n c e r n e d , the c o n c e p t s e e m s all the more a s t o n i s h i n g for h a v i n g e n d u r e d so long w i t h o u t a n e m p i r i c a l foundation. We tell ourselves that s o m e t h i n g must be going on. W h y else does a s h r i m p climb onto a fish? A n d w h y does the fish p e r m i t this to h a p p e n ? T h e s e are r e a s o n a b l e questions. As M a y r (1992:131) p o i n t e d out, "More t h a n a n y t h i n g else it is the e x i s t e n c e of a d a p t e d features that l e d biologists to ask 'why?' questions." For e x a m p l e , w h e n a s k e d h o w he c a m e u p o n the discovery that blood circulates, Sir W i l l i a m H a r v e y a n - s w e r e d b e c a u s e he w o n d e r e d w h y v e i n s h a d valves (see Mayr, 1992:131-132).
" C l e a n e r " shrimps? 63 tivity lies not in the future (in w h i c h c a s e it w o u l d be teleological) but w i t h i n the c o d e of the p r o g r a m itself. A d a p t e d f e a t u r e s s u c h as c l e a n i n g symbiosis should b e p r e d i c t a b l e a n a l o g s of H a r v e y ' s v a l v e s a n d veins. A n y such p r o g r a m must be c o m p a t i b l e with Mayr's f r a m e w o r k , d i v e s t e d as it is not just from t e l e o l o g y but from a n t h r o p o m o r p h i s m , t e l e o l o g y ' s p h i l o s o p h i c a l d e r i v a t i v e .
Does " c l e a n i n g " b e h a v i o r by a shrimp qualify? A shrimp in the process of " c l e a n i n g " a fish p r e s u m a b l y displays certain e l e m e n t s of its b e h a v i o r a l repertoire in this direction. A program, if present, r e q u i r e s it. But e v e n if " c l e a n i n g " is t e l e o a o m i c , its a d a p t e d features in t e r m s of costs a n d b e n e f i t s r e m a i n unclear, e s p e c i a l l y from the s t a n d p o i n t of the host. Tactile stimulation from the " c l e a n e r " m i g h t b e a fish's only r e w a r d ( S a r g e n t & W a g e n b a c h , 1975).
Early reports of " c l e a n i n g " symbiosis s u g g e s t e d n u a n c e s of interspecific c o o p e r a t i o n a n d ecological utility t h a t w e r e difficult to resist from a t e l e o l o g i c a l p e r s p e c t i v e . T h e im- a g e s c o n v e y e d w e r e of n a t u r e in b a l a n c e , of animals c o o p e r a t i n g to k e e p it so. It w a s a s c e n e of g o a l - d i r e c t e d b e h a v i o r r e f l e c t i n g b a c k the future instead of the p r o g r a m : with the naturalist as provocateur, life in coral seas was u n a b a s h e d l y teleological. L i m b a u g h (1961:42), for e x a m p l e , w r o t e of P e r i c l i m e n e s pedersoni: " T h e fish usually p r e s e n t s its h e a d or a gill c o v e r for c l e a n i n g , but if it is b o t h e r e d by s o m e t h i n g out of t h e ordinary, such as an injury n e a r its tail, it p r e s e n t s its tail first. T h e s h r i m p . . , w a l k s rapidly o v e r the fish, c h e c k i n g irregularities, t u g g i n g at p a r a s i t e s with its claws a n d c l e a n i n g i n j u r e d areas. T h e fish r e m a i n s almost m o t i o n l e s s d u r i n g this i n s p e c t i o n and allows the shrimp to m a k e m i n o r incisions in o r d e r to g e t at s u b c u t a n e o u s parasites."
Such a p p e a l i n g i n t e r p r e t a t i o n s of n a t u r e are usually sticky q u a g m i r e s c l e v e r l y dis- guised. " C l e a n i n g symbiosis" m i g h t b e t t e r h a v e b e e n s e e n as discontinuous activity with no p r e d e t e r m i n e d endpoint, just as the milling of p e o p l e on a street corner infers n o t h i n g a b o u t ultimate destinations. It m i g h t h a v e b e e n p r u d e n t , in o t h e r words, to a c c e p t initially the null h y p o t h e s i s of no association. A d m i t t i n g that falsification of the null m u s t p r e c e d e a c c e p t a n c e of the a l t e r n a t i v e h y p o t h e s i s has always b e e n difficult. C a m p b e l l (1993:93) wrote: "As social animals, w e a c q u i r e c o n f i d e n t beliefs t h r o u g h the reports of others. T h e layers of e q u i v o c a l i t y are t h e n m o r e n u m e r o u s . . . . " In science, as in o t h e r e n d e a v o r s , a l a y e r called "objectivity" is a l w a y s the t h i c k e s t a n d most uncertain.
Acknowledgements. I thank R. Bruce Gillie, Robin M. Overstreet, and Robert S. Prezant for re-
viewing the manuscript. This is contribution 293 of the Marine Sciences & Technology Center.
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Bary, A. de, 1879. Die Erscheinung der Symbiose. Trtibner, Strassburg, 30 pp.
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