Cleaning Symbiosis Among California Inshore Fishes

Home , Brachyistius, Cleaning symbiosis, Gut (coastal geography), Kelp perch

CLEANING SYMBIOSIS AMONG CALIFORNIA INSHORE FISHES

EDMUNDS. HOBSON'

ABSTRACT Cleaning symbiosis among shore fishes was studied during 1968 and 1969 in southern California, with work centered at La Jolla. Three species are habitual cleaners: the seAoriF, Ozyjulis californica; the sharpnose seaperch, Phanerodon atripes; and the kelp perch, Brachyistius frenatus. Because of specific differences in habitat, there is little overlap in the cleaning areas of these three species. Except for juvenile sharpnose seaperch, cleaning is of secondary significance to these species, even though it may be of major significance to certain individuals. The tendency to clean varies between individuals. Principal prey of most members of these species are free-living organisms picked from a substrate and from midwater-a mode of feeding that favors adaptations suited to cleaning. Because it is exceedingly abundant in a variety of habitats, the seiiorita is the predominant inshore cleaning fish in California. Certain aspects of its cleaning relate to the fact that only a few of the many seiioritas present at a given time will clean, and that this activity is not centered around well-defined cleaning stations, as has been reported for certain cleaning fishes elsewhere. Probably because cleaners are difficult to recognize among the many seiioritas that do not clean, other fishes.generally do not attempt to initiate-cleaning; rather, the activity is consistently initiated by the cleaner itself. An infested fish approached by a cleaner generally drifts into an unusual attitude that advertises the temporary existence of the transient cleaning station to other fish in need of service, and these converge on the cleaner. Although seiioritas, as a group, clean a number of different fishes, a given individual tends to initiate cleaning with members of just one species. The fishes cleaned most often are those which are most abundant and, at the same time, are most heavily infested with external parasites. The most numerous ectoparasites are caligid copepods, the most abundant and widespread of which is Caligwr hobsoni. These particular parasites, along with gnathiid isopod larvae, are the major prey of the cleaning fishes. Cleaning is essentially limited to the external body surface; ectoparasites of the oral and branchial cavities are not ordinarily taken. Clean- ing effectively reduces the number of parasites on fishes that are cleaned, and is an important activity for the organisms iwolved. However, there is no basis for the contention that many good fishing grounds in southern California exist because fishes have congregated in these locations for cleaning.

It has been suggested that many of the better reasons that have nothing to do with cleaning. inshore fishing spots are, in fact, cleaning sta- Regardless of which view is correct in a given tions (Limbaugh, 1961; Feder, 1966). The situation, one having witnessed fishes crowded contention is that fishes congregate at these lo- around a cleaner, vigorously soliciting its ser- cations so that ectoparasites and other deleteri- vices, can only conclude that this activity is in- ous material can be removed from their bodies deed important to the organisms involved. by resident cleaning organisms. Critics of this Cleaning symbiosis has been widely described hypothesis might well suggest instead that clean- in the literature (Longley and Hildebrand, 1941; ers simply are especially active where fishes are Eibl-Eibesfeldt, 1955 ; Limbaugh, 1955, 1961; most abundant, or that the cleaners as well as Randall, 1958, 1962; and others) and was re- those they clean occur at these locations for viewed by Feder (1966). Youngbluth (1968) studied activity of the Hawaiian cleaning labrid Contribution of Scri ps Institution of Oceanogra hy. Labroides phthirophagus in some detail, and ' National Marine F?sheries Service, Tiburon gort Losey (1971) analyzed the communicative sig- Fisheries Marine Laboratory, Tiburon, Calif., and Scripps Institution of Oceanography, Universit of Cal- nals between this same species and the fishes that ifornia, San Diego, Calif. Mailin address: Kational it cleans. But most other reports on cleaning Marine Fisheries Service Fishery-gceanography Center, P.O. Box 271, La Jolla, calif. 92037. have been simple treatments based largely on

Manuscript accepted March 1971. FISHERY BULLETIN: VOL. 69. NO. 3, nil. 491 FISHERY BULLETIN: VOL. 69, NO. 3

incidental observations. In this report, I de- SPECIES STUDIED scribe cleaning symbiosis among inshore fishes of southern California and attempt to relate ob- Most of the cleaning observed during this served activity with the incidence of specific study was performed by the seiiorita (Figure 1) , ectoparasites. which by virtue of its great abundance in a va- Conrad Limbaugh, Scripps Institution of riety of habitats is the predominant cleaner in- Oceanography, was among the first to report shore. The sharpnose seaperch (Figure 2) was cleaning symbiosis among California fishes. In frequently observed cleaning, but its activity is a study of fishes of the kelp beds, Limbaugh centered in deeper water. The kelp perch (Fig- (1955) described cleaning by the seiiorita, Ox- ure 3) may be an important cleaner in the can- yjulis californica, a fish of the family Labridae, opy region of the kelp forests, where it concen- and also by several seaperches of the famiIy Embiotocidae: the kelp perch, Brachyistius frenatus; the black perch, Embiotoca jacksoni; and the pile perch, Rhacochilus vacca. Subse- quent observers have described cleaning by the rainbow seaperch, Hypsurus caryi (Gotshall, 1967) ; the sharpnose seaperch, Phunerodon atripes (Clarke, Flechsig, and Grigg, 1967; Gotshall, 1967; Hobson, 1969a) ; and the blacksmith, Chromis punctipinnis (Turner, Ebert, and Given, 1969). FIGURE1.-Seiiorita.

FICUKE2.-Sharpnose seaperch among branches of a gorgonian.

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- HOBSON: CLEANING SYMBIOSIS trates, but this was not determined in this study all specimens and will be reported in detail else- because observations in the kelp-canopy habitat where in collaboration with R. F. Cressey, U.S. were infrequent. Nevertheless, observations National Museum. These collections also pro- were sufficient to recognize the kelp perch as a vided the material for descriptions of 11 species habitual cleaner. The only other fish seen clean- of copepods formerly new to science (Cressey, ing was the white seaperch, Phanerodon fur- 1969a, 1969b, 1970; J. Ho, California State Col- catus, in which cleaning seemed to be only an lege, Long Beach, unpublished manuscript). Ad- occasional incidental activity. ditional undescribed species may occur among a number of copepods from these collections METHODS presently under study by Z. Kabata, Biological Station, Nanaimo, British Columbia. During 1968 and 1969, I spent more than 103 In addition to a survey of the ectoparasites, hr underwater directly observing cleaning and gut contents of known cleaning species, including related activity in California inshore waters. material from 53 seiioritas, 29 sharpnose sea- Also contributing to the study are many inci- perch, and 3 kelp perch, were analyzed. dental observations of cleaning made during Many ectoparasites leave their host when it other work with California fishes between 1961 is in difficulty, and some fishes regurgitate their and 1970. stomach contents under stress. To reduce this Supplementing the observations, 421 speci- loss, all specimens were individually sealed in mens of 39 species were collected with spear. plastic bags immediately upon capture, and while These represent most of the species common in still underwater. the study area that exceed a length of 100 mm To acquire detailed data on the cleaning in- (all lengths of fishes in this report are standard teraction, a number of individuals of cleaning length). The ectoparasites were collected from species were kept under surveillance for periods

FIGURE%-Kelp perch next to giant kelp.

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__-- - FISHERY BULLETIN: VOL. 69, NO. 3 up to 15 min, and a verbal account of their ac- in comparison to some areas nearby to the south tivity was recorded on tape. The attempted and elsewhere in California. Other details of standard of 15 min could not be maintained for the principal study area will be introduced as all these observations because sometimes con- they become pertinent. tact with the fish being watched was lost as the During all observation periods at the La Jolla fish swam among vegetation or other fishes. In- stations a record was kept of water temperatures dividuals followed included known cleaners as from surface to bottom, horizontal visibility, and well as others that had not shown evidence of surge conditions. cleaning. In monitoring the activity of known cleaners, a record was kept of the time during OBSERVATIONS which they showed an apparent cleaning interest in other fish and also the number of cleaning GENERAL ECOLOGY bouts in which they became involved. A cleaning bout is defined here as any cleaning activity Seiiotita involving a discrete group of fishes, whether this The seiiorita, which attains a length of about group includes one cleaner attending a single 250 mm, is one of the most abundant fishes in fish, or several cleaners attending a cluster of the inshore waters of southern California, in- 40 to 50 fish. On various occasions I also re- cluding the Channel Islands. It occurs from the corded the number of times that the cleaner shoreline to depths exceeding 40 m and is re- actually “picked” at the body of another fish, and corded from central California south to central precisely at what point on the body this action Baja California, Mexico (Roedel, 1953). An in- was directed. habitant of water over rocky substrates and among sea weeds, the seiiorita sometimes swims Study Areas singly, but more often in groups of from a few to many hundreds of individuals. Like other Observations of cleaning symbiosis were made labrids, it is strictly a diurnal fish, taking shelter at many locations throughout southern Califor- under cover at night. nia, including the Channel Islands, and at the Coronado Islands, Mexico. However, most of the data were collected during concentrated work Food habits.-The sefiorita feeds on a variety at La Jolla, Calif. Here, three study sites were of benthic organisms from the surface of both established, each including an area of about algae and rocks. It also feeds heavily in the mid- 100 m2, that lie on a line running northwest off- waters, taking small organisms in the plankton, shore from La Jolla Point. Moving away from as well as forms that are attached to or encrusted the beach along this line, the first station lies in 3 on drifting algal fragments. All this feeding to 10 m of water about 200 m offshore, the sec- is accomplished in a characteristic picking man- ond is in 20 to 25 m of water about 700 m off- ner, a mode of feeding well suited to its pointed shore, and the third in 30 to 35 m of water about snout and the several long, curved canine teeth 1000 m offshore. The sea floor at all three sta- that project forward at the front of each jaw. tions is rocky and irregular, with many crevices To determine the food habits of this fish in and caves. Algae are not conspicuous at the two the study area, 26 specimens, 110 to 195 mm deeper stations, which are similar, but the rocks long, were speared randomly from the population support a heavy growth of gorgonians. On the at large. None of these were cleaning when other hand, the nearshore region of the 3- to 10-m collected. Food items in their stomachs, ranked station is richly carpeted with surfgrass, PhyL as percentage of each item in the entire sample, lospadix, and other parts of the inshore station were as follows: bryozoans encrusted on algae, are forested by large kelps, particularly giant 43 % ; caprellid amphipods, 32 % ; fish eggs, 3%; kelp, Macrocystis, and feather-boa kelp, Egre- gammarid amphipods, 2.5 % ; unidentified crus- gia. However, these large kelps are sparse here tacean fragments, 4%; and pelecypod mollusks,

494 HOBSON: CLEANING SYMBIOSIS

2.4%. A number of items each made up less ditions. These comments on temperature effects than 1% of the sample, including crab frag- are based entirely on casual evaluations of rel- ments, gastropod mollusks, pycnogonids, and a ative abundance under varying conditions. gnathiid isopod larva. Unidentified material constituted 16% of the sample. The gnathiid Sharpnose Seaperch larva, a single individual from one seiiorita, was the only evidence of ectroparasites among this The sharpnose seaperch is not regarded as a material. common species (e.g., Limbaugh, 1955), but was Limbaugh (1955) stated that seiioritas are relatively abundant during this study over rocky omnivorous carnivores which feed on almost any substrates below 20 m in the La Jolla area. It animal material. Quast (1968) concluded that grows to over 200 mm long and is recorded from the principal foods of the seiiorita are small Bodega Bay, central California (Miller, Gotshall, gastropods and crustaceans associated with al- and Nitsos, 1965), south to the San Benito gae. Because he found no crabs or pistal shrimps Islands, Mexico (Roedel, 1953). Most of those in the diet, Quast suggested that bottom feeding observed during this study were juveniles less is infrequent; however, having seen seiioritas than about 125 mm long that swam singly or, frequently picking on the bottom, I believe there more often, in small groups of less than 10 indi- must be some other reason why these prey are viduals. Adults were seen only occasionally but not taken more often. Size may be a factor, as sometimes swam in larger aggregations. All crabs and pistal shrimps generally are larger and activity observed in these fish occurred during more heavily shelled than most prey of the daylight. After dark they hover above the sub- seiiorita. strate and are alert, but their activity at this time, if any occurs, was not determined. Movements.-Although individual seiioritas may range widely over the bottom in a given Food habits.-This seaperch takes a variety locality, they seem to operate within a restricted of benthic organisms from the surface of rocks, range. Individual fish, when followed, always algae, gorgonians, and other benthic substrates. criss-cross back and forth within a defined area. Prey are taken off the bottom in a characteristic Twelve individuals, selected randomly from the picking manner similar to that of the seiiorita. population at large and kept under surveillance However, the seaperch's dentition would seem for 11 to 15 min each, showed no evidence of less specialized for picking than that of the cleaning. seiiorita; its conic teeth are relatively short and Seiioritas are most abundant at the 3- to 10-m straight, and those at the front of the jaws are station and become progressively fewer with in- not notably longer than those on the sides, nor creasing depth offshore. Nevertheless, even at do they project forward. the 30- to 35-m station the species was among To investigate the food habits of this fish in the most numerous present. Fluctuations in the study area, 13 individuals, 76 to 170 mm numbers were often apparent with changes in long, were speared randomly from the popula- water temperature. Some of the movement is tion at large. None of these were cleaning when vertical. When a layer of colder water moved collected. Food items in their stomachs, ranked in over the bottom-a frequent phenomenon at as percentage of each item in the entire sample, the 20- to 25-m station-seiioritas were especially were as follows: caprellid amphipods, 56%; abundant up in the water column above the chitons, 9 o/c ; planktonic copepods, 9%; isopods, thermal interface. Seasonal and other longer 8 % ; limpets, 2 % ; pelycypod mollusks, 1 % : and term changes may induce inshore/offshore move- sponges, 1%. Unidentified material made up ments in certain members of the population. The 14% of the sample. There was no evidence of numbers present fall off noticeably when temper- ectroparasites in this material. One individual atures drop much below 13" C, but at least some had fed heavily and exclusively on plankton- seiioritas were present no matter what the conic copepods, showing that this fish is not

495 FISHERY BULLETIN: VOL. 49. NO. 3 limited to benthic prey. I have found no refer- with kelp. Attaining a maximum length of about ences to food habits of this fish in the litera- 150 mm, the kelp perch is recorded from Van- ture. couver Island, Canada, south to central Baja California, Mexico (Roedel, 1953). The kelp Movements.-On the basis of limited obser- perch occurs near the rocky bottom at the base vations, these fish do not seem to move around in of giant kelp, as well as adjacent to the rising their habitat as much as sefioritas do. Never- kelp stipes, but is most abundant just under the theless, they do show marked inshore/offshore kelp canopy, near the water's surface. Typi- movements that may relate to changing water cally, this fish occurs in aggregations of a dozen temperatures. Unlike the ubiquitous seiiorita, or more, but larger individuals frequently are this fish occurred in limited numbers that al- solitary, especially those near the rocky sea floor. lowed assessing relative abundance through ac- Most of my observations of kelp perch were made tual counts. It was never seen at the 3- to 10-m outside the La Jolla study area, the majority station but was reasonably abundant (10-20 in- around the Channel Islands. dividuals were counted during 15-min periods) on all visits to the 30- to 35-m station. At the 20- to 25-m station its appearance was irregular Food habits.-This perch feeds in a picking and closely followed temperature fluctuations. manner, similar to that employed by the seiiorita Generally it was rare or absent at the 20- to 25-m and sharpnose seaperch. It preys on a variety station when bottom temperatures rose much of organisms from the surface of the surrounding above 13" C, and was present (a maximum of kelp and also feeds extensively on material sus- 10 was seen during a 20-min period) when the pended in the current. Its pointed snout and temperature dropped much below this level. As, small, upturned mouth, together with a number most of the individuals seen were juveniles, a of relatively long, curved canine teeth that pro- seasonal factor independent of temperature was ject forward at the front of each jaw, are well probably operating here. Nevertheless, short- suited to its mode of feeding. The dentition of term temperature changes over the critical range this fish is similar to that of the seiiorita, a fact (approximately 12"-14" C at the 20- to 25-m sta- also noted by Hubbs and Hubbs (1954). I did tion) were consistently accompanied by the not sample kelp perch from the population at presence or absence of this fish. I emphasize large for food-habit analysis; all those collected that these assessments of abundance are relative were from known cleaning stations. However, to the numbers of the species regularly present. Limbaugh (1955) stated that they feed on small The sefiorita was always more abundant than crustaceans, particularly those that occur on the seaperch at all stations and under all con- giant kelp. Quast (1968), who also reported a ditions. Thus whereas the seaperch was con- predominantly crustacean diet, with a prepon- sidered abundant during a period in which 15 derance of amphipods, noted that some mollusks individuals were seen, at no time did I find so few and bryozoans are taken as well. sefioritas present at any of the three La Jolla stations. Movements.-Limited observations indicate that aggregations of kelp perch in the canopy, Kelp Perch and close to large rocks, remain relatively stable. Several aggregations that were observed over The kelp perch was not abundant in the La 2 to 3 months did not change appreciably in lo- Jolla study area, where it was seen only at the in- cation or in numbers of individuals. Data on shore station. Its distribution is essentially lim- this point are scanty, however. ited to the kelp beds, which were not well de- At night they hover in the same areas in veloped in the study area at the time of this which they are active in daylight, but their ac- work. Nevertheless, it is very numerous in Cal- tivity at this time, if any occurs, was not deter- ifornia inshore waters that are heavily forested mined.

496 HOBSON: CLEANING SYMBIOSIS

CLEANING ACTIVITY OF seven instances were sefioritas seen cleaning THE SE~~ORITA members of a mixed-species group. The tabu- lation of species cleaned (Table 1) does not in- Unlike some other cleaners (see Feder, 1966), clude the mixed-species groups because in the seiioritas do not establish well-defined stations mixed groups it was not determined whether at which they receive other fishes seeking to be representatives of all species present were ac- cleaned. Rather, the seiioritas, as they move tually cleaned. All seven mixed groups included over the local area, approach and clean fishes halfmoons, Medialuna californiensis, and one or wherever they encounter them. more fish of other species. In four of these, Despite their great abundance, only a small halfmoons were mixed with blacksmiths, in one segment of the seiiorita population seems pre- they were mixed with opaleyes (Girella nigric- disposed to clean at a given time. The cleaning ans) , in one with rubberlip perch (Rhucochilus habit is not limited to any particular stage in toxotes), and in one with both rubberlip perch their life history: cleaning seiioritas have in- and pile perch. All of these were incidental cluded some of the smallest individuals seen observations. The compilation does not include (< 40 mm) as well as some of the largest data obtained on other occasions when the ac- (> 225 mm). In cleaning material from the tivity of individual cleaners was recorded for bodies of fishes, seiioritas employ the same pick- extended periods. ing technique they use to take small prey from The data clearly indicate that blacksmiths, and a rock or algal substrate. This mode of feeding, to a lesser extent topsmelt (Atherinops affinis), along with their pointed snout and long, for- predominate as recipients of the seiiorita's clean- ward-projecting canine teeth, are well suited to ing efforts in the areas where the observations the cleaning habit. were made. Table 1 is not a definitive list of Individuals that clean are numerous where species cleaned by the seiiorita ; nevertheless, it there are many resident fishes, especially of is evident that many species which co-occur with certain species (as discussed below), but I found the seiiorita are not cleaned. At other times, no evidence that residents of other areas come in addition to all species noted in Table 1, I have to these locations to have parasites removed. seen Seriola dorsalis and Trachurus symmet- Occasionally a migrating species, such as the ricus being cleaned. But the ratio of species California yellowtail, Serioh dorsalis, will pause listed here generally is consistent with observa- to be cleaned while passing through areas where tions made on other occasions and at many dif- cleaners are active, but this is not the same as ferent locations. a resident of a particular area habitually swimming elsewhere to be cleaned and then returning its home ground. to TABLE1.-Fishes observed being cleaned by seiioritas during 62 observation periods between June 1968 and Cleaned by the Seiiorita January 1969 at La Jolla, Calif. (exclusive of seven Fishes mixed-species groups).

Percent of Casual observation alone show that some fish Species total bouts species are cleaned far more often than others, I -. , and that many species do not seem to interact Blacksmith. Chromir punrtipinnir 231 60 Topsmelt, Athrrinops afinir 81 21 with cleaners at all. Gariboldi, Hyprypopr rubicunda 22 6 To obtain data on this point, a record was kept Halfmoon, Mtdinlunn rolilornirnrir 19 5 Seiiorita, Oxyiulir rolilorniro IO 3 of the species seen being cleaned by sefioritas Rubberlip perch, Rharorhilur toxotrr a 2 during 62 observation periods (15 min to 2 hr Opaleye, GirrNn nigrirnnr 5 1 Kelpfish, Httrrostirhur roitratur 3 1 long) from June 1968 to January 1969. During Block perch, Embiotora iorkroni 1 1 this period, 392 cleaning bouts were witnessed, Pile perch, Khncochilur vocra 1 1 Sargo, Anirotrcmus dovidsoni I 1 385 of which involved seiioritas cleaning one or Blue rockfish, Sfbnttrr myrtinur I 1 more individuals of a single species; in only Olive rockfish, Srbortrr rrrranoidrs 1 1

497 FISHERY BULLETIN: VOL. 69, NO. 3

Reports in the literature present a comparable Generally the first sign of an interaction oc- picture. Most published accounts of cleaning by curs when a sefiorita swims up alongside a black- seiioritas describe the way blacksmiths cluster smith in midwater and closely inspects its body. around this cleaner to solicit its attentions (Lim- The blacksmith may then immediately stop swim- baugh, 1955, 1961; Feder, 1966; and others). ming and, holding its fins motionless and erect, Limbaugh (1955) observed the following fish drift into an awkward-appearing posture. Usu- being cleaned by seiioritas: Myliobatis califor- ally the blacksmith is head-down, but sometimes nica, Stereolepis gigas, Paralabrax cluthratus, turns on its sides or is tail-down. On some occa- Trachurus symmetricus, Atherinops affinis, sions the blacksmith presents a particular part Anisotremus davidsoni, Hyperprosopon argen- of its body to the inspecting seiiorita. The seii- teum, Rhmochilus vacca, Chromis punctipinnis, orita swims about this fish, usually pausing Hypsypops rubicunda, Girellu nigricans, Medi- briefly to pick at its body. Immediately follow- dwnu californiensis, and Mola mola. Turner et ing the first sign of this activity other black- al. (1969) observed the following fish being smiths converge on the spot, so that very quickly cleaned by seiioritas: Sebastes spp., Atherinops 10 or more crowd around the cleaner (Figure 4). affinis, Atherinopsis californiensis, Trachum The seiiorita soon leaves the original blacksmith symmetricus, Seriola dorsalis, Chromis punctip- and may then move on to one of the others. It innis, and Molu molu. Neither of these reports may also swim slowly away, whereupon the gives data on the relative frequency with which group of blacksmiths follows along, each attempt- these different species were cleaned, but it is ing to position itself in the seiiorita’s path. Al- significant that many of the same species con- though the seiiorita shows progressively less in- sistently appear in the reports of independent terest in the blacksmiths, they continue to crowd observers, while at the same time many other in its way. Soon the seiiorita shows no further species that frequent these waters in large num- interest in cleaning, and all but a few black- bers are not mentioned. No doubt many species smiths leave the group. The remaining few not yet reported are occasionally cleaned by doggedly continue attempting to present them- seiioritas, but there seems little doubt that a selves to the now-unresponsive cleaner. Even- certain few species, the blacksmith in particular, tually, however, these last blacksmiths lose con- predominate in this activity. tact with the cleaner as it swims off among the kelp or the many other seiioritas in the sur- Specific Cleaning Interactions rounding water. Once they have lost contact with the cleaner the blacksmiths do not attempt The fishes cleaned by the seiiorita vary mark- to solicit cleaning from any of the many other edly in their habits and habitat, as well as in seiioritas around them. their relative numbers. These fishes do not seek On only two occasions did I note blacksmiths out cleaning at a “station” established by the soliciting cleaning from a seiiorita that did not seiiorita, but rather receive the seiiorita on their seem to have made an ipitiating gesture. Once own grounds during the course of their regular the blacksmiths were very small, about 40 mm activity. Cleaning interactions often proceed long, and in the other observation, at a depth differently with one of these species than with of 27 m, little cleaning had been.seen and rela- another. Some of these variations in cleaning tively few seiioritas were present. However, activity are characterized below. in both instances the seiioritas were known by me on the basis of earlier observations to be Sefiorita-blacksmithinteractions.-The black- individuals that clean. It is possible that the smith is one of the most abundant fish over rocky fishes soliciting attention recognized these seii- substrates in California inshore waters, where oritas as cleaners through some cue not noted it swims in large stationary aggregations in mid- by me. Sometimes when a seiiorita incidentally water. It feeds largely on zooplankton (Quast, passes close to a blacksmith, the blacksmith no- 1968) and attains a length of about 250 mm. ticeably pauses in its swimming and looks as

498 HOBSON: CLEANING SYMBIOSIS

FIGURE4.-SeRorita cleaning the caudal peduncle of one of a group of blacksmiths that hover to solicit service. though it is beginning to assume a soliciting at a number of different locations-always with posture; however, when the seiiorita swims on blacksmiths. I have no explanation for the fact past, the blacksmith immediately resumes its that a seiiorita which becomes unresponsive and original activity. Occasionally members of other leaves one group of blacksmiths that still vigor- species were seen responding similarly to passing ously solicits its service may soon initiate ac- sefioritas. In most observations of cleaning, my tivity again with another blacksmith. attention was drawn to activity already in prog- The three individuals whose cleaning activity ress, so that it was not possible to determine was monitored for 15 min joined in a mean of whether cleaner or client had initiated the ac- 4 separate bouts (range 2-6), For a mean of 11 tivity. min of this time (range 6.75-13.25 min) they Individual seiioritas that cleaned blacksmiths showed an apparent cleaning interest in black- during many short-term observations were not smiths, or were accompanied by blacksmiths with seen cleaning any other species. This same which they had earlier initiated a cleaning inter- situation held true for three individuals, known action. When not thus engaged with black- to have been cleaning blacksmiths, whose ac- smiths, they swam in midwater showing no tivity was monitored in detail on tape for 15 apparent interest in the fishes around them but min. When observed for extended periods, occasionally picked at drifting scraps of debris, sefioritas were found to become involved in usually algal fra-gments. During much of the a succession of separate cleaning bouts. This time that they swam in consort with blacksmiths, activity was not restricted to one location but they closely inspected these fish and actually continued at various points over a relatively picked at their bodies a mean of 26 times (range wide area. Periodically they joined cleaning al- 14-33). Of these picks, 27% were made at the ready underway, or initiated cleaning themselves base of the blacksmith's anal fin, 25% on the

499 FISHERY BULLETIN: VOL. 69, NO. 3 caudal peduncle or caudal fin, 22% at the base of group of topsmelt more readily than they do the pectoral fin, 10% somewhere on the body with blacksmiths, as they need only swim down exclusive of a fin-base or head, 8% on the head, to the substrate below, where the topsmelt seem 5% at the base of the pelvic fins, and 3% at the reluctant to follow. base of the dorsal fin. These shallow areas are frequently swept by Clearly, the bases of the fins receive most of surge, and the load of drifting debris in mid- the attention from the seiioritas. These data water is frequently heavy. In this area cleaning are consistent with the many more general ob- seiioritas frequently leave the groups of topsmelt servations made on other occasions. At no time they are attending to inspect an object drifting during this study were seiioritas seen to clean in the water nearby. Sometimes they take the within the oral or branchial cavities of black- object into their mouths, sometimes not. Often smiths: all cleaning was directed at the body when taken it is quickly rejected. surface. Attempts at extended observations on individual sefioritas that had been cleaning topsmelt Sefiorita-topsmelt in t erac t ions.-The top- were largely unsuccessful. Too often before the smelt, which attains a length of about 200 mm, is observation had progressed far the seiioritas abundant in many inshore regions of California disappeared among the surfgrass or other vege- coastal waters, but its distribution is more spotty tation carpeting the sea floor in this area. How- than that of the ubiquitous blacksmith. Like ever, two individuals were followed for 10 min the blacksmith, it feeds largely on zooplankton, each, during which time one entered into four, which it takes while swimming in large schools the other two, separate cleaning bouts. Between at the water’s surface. Quast (1968) noted the cleaning bouts these two swam over a wile area similarity in diet between topsmelt and black- alone in aidwater, occasionally picking at drift- smiths, and while acknowledging that their feeding debris. On several occasions they picked at ing areas may overlap, he pointed out that top- benthic algae. Neither individual showed clean- smelt normally swim higher in the water column. ing interest in species other than topsmelt, which In the La Jolla study area, topsmelt are con- was consistent with observations of other seii- centrated at the inshore station over extensive oritas that cleaned topsmelt. fields of surfgrass that grow in 3 to 5 m of water. They are never far from the substrate Seiioritn-gwibaldi int eructions.-The gari- in this relatively shallow water, even though baldi, which attains a length of about 250 mm, they swim in large schools at the water’s sur- is a solitary, highly territorial fish that lives face. They are more abundant than blacksmiths close to the substrate. Especially during the re- in this area, and here they predominate in the productive season, when the males aggressively seiiorita’s cleaning activity. guard their nests among the rocks, these bright The cleaning interaction proceeds in much the orange pomacentrids normally drive away all same way as it does with blacksmiths: the ac- other fish that come near. They feed on sessile tivity is initiated when a seiiorita swims up to benthic invertebrates and are abundant at the an individual topsmelt and begins to inspect it 3- to IO-m station. closely. Immediately other topsmelt converge Garibaldis frequently are cleaned by seiioritas. on this pair to place themselves in the seiiorita’s Most of the garibaldis seen being cleaned were path, thus soliciting its attention. When pre- swimming a meter or so above the bottom; I senting themselves motionless before seiioritas, did not observe cleaners active around the gari- topsmelt frequently hover tail-down, in contrast baldis guarding nests among the rocks. All of to the head-down posture most often assumed the garibaldis seen being cleaned were solitary, by blacksmiths. I saw seiioritas clean only the which reflects their territorial nature. The seii- external body surfaces of topsmelt. In the rel- orita swims up to a garibaldi and closely inspects atively shallow water where most of this activity its body, thus initiating the action. Usually the was observed, seiioritas break off contact with a garibaldi hovers motionless in a normal hori-

500 HOBSON: CLEANING SYMBIOSIS zontal attitude, its fins sometimes erect. The not particularly abundant in the principal study seiiorita may pick at a few places on the gari- areas. Still, they were frequently seen being baldi’s body-most often around the caudal re- cleaned by seiioritas during this study. When gion-but usually its attentions are brief, and many halfmoons were present, cleaning by the soon it swims away. With blacksmiths and top- seiiorita progressed much as described above for smelt, each cleaning bout is prolonged by the blacksmiths. Yet when just one halfmoon was many other individuals that join at the cleaning present, a frequent occurrence, the cleaning site to crowd in the seiiorita’s path. Nothing of bouts were brief like those described above for this sort happens with the solitary garibaldi, the garibaldi. At least one halfmoon was pres- which usually makes no attempt to follow the ent in all the mixed-species groups that I re- seiiorita when it leaves, so that each cleaning corded when collecting the data presented in bout is relatively brief. After leaving one gari- Table 1. I saw seiioritas clean only the external baldi, however, often the seiiorita quickly ap- body surface of halfmoons. proaches another. In agreement with their One seiiorita, seen cleaning a halfmoon, was cleaning of blacksmiths and topsmelt, seiioritas kept under surveillance for 12 min before con- known to have cleaned garibaldis were subse- tact was lost. As the observation period began, quently seen cleaning only other members of that the seiiorita picked at the halfmoon once and same species. This was true during several then moved away, swimming slowly and alone, short-term observations, and also when one in- 2 or 3 m over the substrate. After an unevent- dividual was followed for 15 min, and a record ful 3 min, the seiiorita approached a second half- of its activity was taped; this particular seiiorita moon, which promptly hovered in a head-down initiated cleaning activity with 26 different gari- attitude. For 15 sec the seiiorita closely in- baldis during the observation period as it swam spected this halfmoon and picked at its body over an irregular course among the rocks in an three times before swimming away. It then area where blacksmiths, topsmelt, and other spe- continued on alone for the remaining 8+ min cies also were present. Each cleaning bout lasted that it was under observation, still swimming a mean of 10 sec (range 7-25 sec) ,totaling 4 min slowly over a wide semicircular course 2 or 3 m 15 sec of the 15-min period. In nine of these above the rocks. During this time it passed bouts, the sefiorita inspected the garibaldi but many different fish without showing interest, did not pick at its body. In the other 17 bouts, but it did not pass another halfmoon. It did the seiiorita picked at the garibaldi’s body a pick at three different pieces of floating debris total of 42 times, or a mean of about 2.5 times but rejected all three immediately. per bout. All cleaning of garibaldi that I observed was Sefio r i t a-s e Eorit a interactions.-Seiioritas directed at the external body surface. themselves are cleaned by other members of their own species. Despite the large numbers Seiiorita-halfmoon interactions.-Halfmoons, of sefioritas that usually are present, I saw no which may exceed a length of 250 mm, usually groups converging on cleaning individuals, as swim high in the water column, frequently in regularly occurs with blacksmiths, topsmelt, and large aggregations, but just as often in small other abundant species. In most of the seiio- groups or as solitary individuals. They are often rita’s intraspecific cleaning interactions, the abundant among rising stands of giant kelp. cleaner attends just a single individual, which Their omnivorous diet, which includes a variety usually hovers motionless in a normal horizontal of benthic algae, along with bryozoans, sponges, attitude, except that its fins are erected; some- and crustaceans (Limbaugh, 1955 ;Quast, 1968), times the mouth is open wide and gill covers indicates bottom feeding; however, much of this are distended, but I saw seiioritas clean only material is taken in midwater as drifting debris. the external body surface of these fish. There Considering their large numbers in many was no indication that seiioritas which clean southern California coastal areas, halfmoons are other seiioritas also clean other species. I fol-

501 FISHERY BULLETIN: VOL. 69, NO. 3

lowed one individual for 10 min after having passed by without responding to the kelpfish, and seen it clean another seiiorita. After this ini- each time the kelpfish returned to the cover be- tial activity, the individual under surveillance low, where it waited until the next approach. swam over a wide area, showing interest only Finally a passing sefiorita paused briefly and in other seiioritas, even though blacksmiths, top- picked at the kelpfish’s side before continuing on smelt, and other species were present. Swim- its way. After this brief encounter, the kelp- ming alone, 2 or 3 m over the rocks, it would fish did not rise from concealment again even assume a position alongside another seiiorita and though several more seiioritas subsequently follow it for a short distance. Usually these passed overhead. other fish showed no interest, but some stopped During the present study this sequence of swimming and erected their fins, whereupon the events involving kelpfish and seiioritas was wit- cleaner picked at their bodies-usually once, but nessed several times at a variety of locations; occasionally several times. Between cleaning indeed, every instance of a kelpfish being cleaned encounters this seiiorita passed through a school followed this pattern-obviously it is a regular of very small (< 40 mm) blacksmiths, several pattern in the behavior of the species. of which hovered head-down in its path; however, the cleaner showed no interest in these fish. Other interactions-Observations are too few On two occasions it picked at a piece of drifting to recognize distinctive aspects in cleaning in- debris. teractions involving the many other species that occasionally are cleaned by seiioritas. Usually such activity is noted simply as occasional sight- Sefiorita-kelpfish interactions.-At least one ings of small clusters of fish, or individual fish, species regularly initiates cleaning bouts with hoveriig before a seiiorita. In all such en- seiioritas. Earlier (Hobson, 1965a) I reported counters, however, only the external body surface observing a kelpfish, Heterostichus rostratus, was cleaned. repeatedly soliciting cleaning from unresponsive Notes follow regarding two other species that seiioritas. The kelpfish was concealed among are cleaned by sefioritas. benthic algae, which is the typical habitat of this A single seiiorita was observed cleaning a pile fish. But each time a seiiorita approached in perch, after which its activity was noted for the water overhead, the kelpfish rose up into 15 min. Pile perch are not abundant where these the sefiorita’s path, where it hovered motionless, observations were made, and after leaving the fins erect (Figure 5). A succession of seiioritas first individual, the seiiorita swam alone in midwater for 14 min. It moved over a wide semicircular course during this time and showed no interest in any of the many fish that it passed, although none were pile perch. It did pick at three small items drifting in midwater. After 14 min it made an abrupt course change and, with slightly accelerated swimming, went directly to a solitary pile perch that was in midwater about 10 m away. The seiiorita swam about the pile perch, which now hovered head- down, but after a close inspection lasting about 10 sec it moved on without picking at the pile perch’s body. Many of the fishes cleaned by seiioritas occasionally start, as if nipped too vigorously. Some- FIGURE5.-Kelpfish hovering in midwater, fins erect, times such fish dart away, thus terminating the to solicit cleaning from a passing seiiorita. cleaning. Other times they actively turn on the

502 HOBSON: CLEANING SYMBIOSIS seiiorita and drive it away. The rubberlip perch parasitic copepods, and isopods. He was not was noted taking the latter course of action per- more specific than this, nor did he present data. haps more often than the other species, even Various other cleaners reportedly take not only considering the relatively few times it was ob- ectoparasites but also diseased and necrotic tis- served being cleaned. sue (Feder, 1966, and others.) Although the kelpfish is the only species that To determine just what it is that seiioritas was observed consistently initiating cleaning remove from the bodies of other fishes, I ex- from sefioritas, individuals of several species do amined the gut contents of 27 specimens, 111 to so in at least one situation. This occurs where 175 mm long, that were speared while they were exceptionally large concentrations of seiioritas, cleaning other fishes. Food items in their guts, sometimes thousands, swim above the rocks. ranked as percentage of each item in the entire At various times, garibaldis, pile perch, rubber- sample, were as follows: caligid copepods, 39%; lip perch, olive rockfish, and others were ob- gnathiid isopod larvae, 12%; algae with en- served hovering in the soliciting posture amid crusting bryozoans, 10% ; caprellid amphipods, these concentrations (Figure 6) until one of the 5%; fish scales, 47; and fragments of nonpar- sefioritas approached and cleaned them. asitic crustaceans, 4 ?+. Unidentified material made up 2675 of the sample. Of the 27 speci- Material Removed from Other Fishes by mens, ectoparasites occurred zmong the gut con- the Seiiorita tents of all but two. In most, the ectoparasites predominated. Even though the data are con- Food habits of cleaning seGoritas.-An obvi- vincing, they do not fully reflect the extent to ous question is: What do seiioritas remove from which cleaning obviously dominated the activity the bodies of fishes they clean? Limbaugh of these particular fish for at least several hours (1955) stated that seiioritas remove bacteria, leading up to their capture. This is because the

FIGURE6.-Garibaldi hovering amid a large assemblage of seiioritas.

503 FISHERY BC'LLETIN: VOL. 69, NO. 3 parasites are so small (1-3 mm long) in com- chids, which were found on 12 species of the parison with the size of other food items. For fishes sampled, are mobile forms about 2 mm example, 471 gnathiid isopod larvae were present long (all lengths of parasites here and below do in one sefiorita gut, but being so small they con- not include egg cases) that occurred mostly on stituted only 3574 of the material. On the other the gills of their hosts. The caligids, which in- hand, a few algal fragments, with encrusting fested 29 species of the fishes, are mobile forms, bryozoans, made up 40% of the material in this 2 to 4 mm long, that occurred mostly on the ex- same specimen. However, only seven individ- ternal body surface of their hosts, although two uals contained ectoparasites alone, as compared species were found only in the oral cavity. The with 17 that contained both parasites and free- dichelesthiids are highly modified forms about living prey. In all but one of these, the two 2 mm long that were attached to the gills of two classes of material were sharply divided in the species. The lernaeid is a highly modified form gut, usually with the free-living material poster- about 5 mm long that was attached to the fins iorly in a more advanced stage of digestion. Al- of 12 species. The chondracanthids, which in- though most of the ectoparasites in the gut had fested five species, are highly modified forms, 3 or undergone extensive damage and would not, by 4 mm long, that lived attached in the branchial themselves, have been identifiable to species, this chamber, including the gills, of their hosts. The material usually graded gradually to freshly in- lerneopodids, infesting eight of the fish species, gested specimens that were readily identified. are highly modified forms, 2 to 5 mm long, mostly This fact, coupled with the circumstance that in- living attached in the branchial and oral cavities, dividual sefioritas tend to stay pretty much with although one individual fish carried several at- a single type of food organism during a given tached to its dorsal fin. Finally, the argulid period, greatly aided the task of analyzing this is a mobile form about 2 mm long that was found material. on the outer body surface of one species of fish. The fish species hosting representatives of the Ectoparasites on the fishes.-To assess the sig- different copepod and brachiuran families are nificance of cleaning in removing ectoparasites, listed in Table 2, and examples of the six copepod one must know what parasites occur on the fishes, families are illustrated in Figure 7. as well as the extent of the infestation. Thus Thus a variety of ectoparasitic copepods occur the survey of ectoparasites done in conjunction on the fishes, but only caligids were found among with this work included essentially every fish the gut contents of the cleaners. Further- species exceeding 100 mm long regularly present more, although 13 species of caligids (five spe- in the La Jolla study area, as well as every species of the genus Caligus and eight species of cies that was seen being cleaned there. Ecto- the genus Lepeophtheirus) occur on fishes in this parasites infesting these fishes include 33 spe- area, only a relatively few of these are significant cies of copepods, one species of brachiuran, two as prey of the cleaners, as noted below. species of isopods, one species of leech, and one Of the two isopods, one, Livoneca vulgaris, a species of monogenetic trematode. Following is large parasite, about 20 mm long, was found in a brief summary of the information being com- the branchial chamber of just one species of fish piled on these parasites in collaboration with R. and was not found to be prey of the cleaners. F. Cressey. On the other hand, the highly mobile gnathiid Copepods are the predominant ectoparasites larvae (Figure 8),which are about 2 mm long, on fishes in this area. The 33 species represent are a major prey of the cleaners. Only one form seven families: Bomolochidae (6 species), of gnathiid was readily recognized, but more Caligidae (13 species), Dichelesthiidae (2 spe- than one species may occur among this material. cies), Lernaeidae (1 species), Chondracanthidae Parasites of the body surface of fishes, the gnath- (5 species), and Lerneopodidae (6 species). The iid larvae were taken on 11 of the fish species one species of the closely related brachiurans is sampled, but I suspect that they are actually a member of the family Argulidae. The bomolo- more widespread and abundant than these data

504 HOBSON: CLEANING SYMBIOSIS

TABLE2.-The types of ectoparasites and the fishes they infest, based on a survey of the fishes in the study area. Where more than one species of parasites is included under a heading, the number in parentheses following the name of each fish thereunder indicates how many different species of that type are represented on that fish. For all fish species listed, the number of infested individuals is shown over the number of individuals examined, followed by the range in numbers of individual parasites of that type which were taken from that species of fish.

COPEPODS COPEPODS-Cont. ISOPODS BOMOLOCHIDAE (6 species of 3 genera) CALlGl DAE-Cont. CYMOTHOIDAE (I species) Fishes infested with members of Alhcrinopr afinir (1) 13/13: 1-23 Fish infested with this parasite: this family: Plturonirhthyr focnoiu, (I) 5/10; 1-5 Srbartrr myrtinvr 1/9: 1 Parolnbrax rlathrotur (I) 2/8: 1-2 DiCHELESTHllDAE (2 species of 1 genus) P. ncbulilrr (2) 5/11: 1-20 GNATHIID LARVAE (number of species not Phanrrodon afriprr (I) 1/13: 1 Fishes infested with pararites determined) of this family: Rhacochilur vorrn (1) 3/15: 1 Fishes infested with these parasites: Grmnothorox rnordox (I) 1/1: 9 Mirromrlrui minimur (I) 1/7: 1 Chromir punrtipinnir 1/10: 1 Pnrnlnbrox nrbulilrr (I) 5/11: 2-70 Hypiypopi rubirundn (I) 1/20: 1 HYPJYPOPJrubicunda 4/20: 1-8 Scorparw guttata (1) 6/14: 2-56 LERNAEiDAE (1 species) Pimrlomttopon pulrhrvm 3/14: 1-4 Scbartrs mYJlinuJ (1) 1/9: 1 Fishes infested by this porasite: Stbartrr atrovirrnr 4/16: 1-20 s. Jrrronoidrr (1) 2/1 1: 1-8 Trnchurur rymmrtricur (I) 1/7: I S. carnntur 3/11: 1 Uxylrbivr pirtur (I) 1/8: 1 Anirotrrmur dnvidroni (1) I/& 1 s. rkryramr/ar 1/11: 2 Afhrrinopr afinir (I) 2/13: 1-4 Chtilotrrmo raturnurn (I) 2/16: 1-2 s. COnJtr/htUJ 1/2: 1 Plruronirhthyr cornwur (I) 6/10: 1-1 1 Mrdialuno rolilornirnrir (I) 5/13: 2-7 s. Jlrronoidrr 1 /I 1: 1 Brarhyirtiur (rrnatur (I) 1/5: 1 S. rrrricrpr 3/15: 1-5 CALlGlDAE (13 species of 2 genera) Embiotora jarkroni (I) 2/15: 1-2 Oxylrbiur pirtur 13 Fishes infested with members of 3/8: this family: Hyprurur rnryi (1) 2/11: 1-2 Srorpornirhthyr marmomfur 3/10: 2-5 Pnrnlabrnx clathrotur (2) 4/8: 1-5 Phonrrodon lurmtur (I) 3/12: 1-3 P. nrbulifrr (3) 4/11: 5-27 Rhorochilur toxotri (I) 1/10: 1 MONOGENETIC TREMATODE (1 species) Coulolntilur prinrrpr (I) 1/4: 2 R. varrn (I) 2/15: 1 Fishes infested with this parasite: Antrotrtmur dovidroni (I) 1/8: 1 Mirromrtrur minimur (I) 5/7: 1-6 Mrdioluna calilornirnrir 6/13: 2-16 Chrilotrrms JdUrnYm (I) 2/16: 1 Athirinopr ofinir (I) 2/13: 1-4 Girrlla nigriranr 4/10: 1-4 Rhacochilur toxottr 2/10: 1 Mcdialuma cdilornitnrir (2) 12/13: 1-75 CHONDRACANTHIDAE (5 species of 5 genera) R. noma 2/15: 1-18 Cirrlh nigriconr (3) 1/10: 1-14 Fishes infested with parasites of Embiotora jorbroni (2) 2/15: 1-2 this family: Hyp~yp~prrubirunda 1/20: 1 Phnnrrodon atriprr (I) 5/13: 1-5 Oxyjulir mlilorniro (I) 13/38: 1-4 Pimrlomttopon pulrhrum 10/14: 1-26 Rhncorhilur toxotrr (3) 10/10: 1-10 Srorpoino guttnta (I) 2/14: 1-5 Scorparno guttotn 2/14: 5-8 Srbartrr atrovirrnr 7/16: 1 R. vnccn (2) 4/15: 1-11 Srorpntnirhthyr mnrmorutur (I) 4/10: 1-4 Chromir punrtipinnir (1) IO/ID: 239 Httrrortirhur rortratur (I) 7/13: 1-7 s. conrttllatur 1/2: 1 HYPJYPO~Jrubicund4 (2) 19/20: 1-144 Plcuronirhthyr cornomr (I) 7/10: 1-47 S. miniutur 2/5: 1-2 Pimrlomttopon pulrhrum (3) 13/14: 1-70 s. rcrrnnoidrr 3/11: 1-26 LERNEOPODIDAE (6 species of 4 genera) Oxyjulir colilornica (3) 13/38: 1-59 s. JrWiCtpJ 2/15: 1-3 Fishes infested by parasites of Hrtrrortichur rortratur 6/13: 1-7 SCOrP4CM EUflot4 (1) 7/14: 1-14 this family: Sebnrtrr ntroffirrnr (3) 6/16: I Chrilotrtmn raturnurn (I) 1/16: 1 LEECH (1 species) S. rarnatur (2) 3/11: 1 Girrlln nigriconr (I) 1/10: 1 Fishes infested with this parasite: s. Chryromt~ar (I) 1/7: 1 Phsnrradon otriprr (I) 5/13: 1-4 HYPJYPO~Jrubicund4 2/20: 1 s. COnJtd~ntur(11 2/2: 1-5 Rhacorhilur wcca (1) 1/15: 1 Srbartrr Icrronoidrr 1/11: 4 S. miniatur (1) 1/5: 2 Chromir punrtipinnir (I) 1/10: 1 Hrtrrortirhur rortrntur 2/13: 1-2 s. myrtinvr (3) 5/9: 1-5 SIbaJtlJ atrovirmr (I) 1/16: 4 s. paucirpinir (I) 3/3: 1 S. ronrtrllatur (1) 1/2: 1 FISHES ON WHICH NO PARASITES WERE s. Jlrronoidcr (3) 8/11: 1-10 S. minintur (1 ) 5/5: 2-8 .FOLJND. - -. .-. S. rcrrircpr (2) 15/15: 1-25 ARGULIDAE (I species) Krnirtiur calilornirnrir O/ 1 Scorgnmirhthyr mafmordur (2) 8/10: 1-42 Fish infested with this parasite: Halirhornr rrmirinctur 0/10 Hdtfortirhur rortrntur (1) 2/13: 1-2 Athrrinoprir ralilornitnrir 1/1: 2 CorvPho9trrur.. . nirholri 0/5

indicate. They are the most mobile of the par- The above summary of the survey results gives asites, and probably many escaped when their a general picture of the ectoparasites infesting host fish was collected. The monogenetic trem- the fishes that co-occur with the cleaners and atode occurred on the outer body surface of 13 might be regarded as a list of the potential prey species of fishes, and the leech occurred simi- of the cleaning fishes. The following material larly on 3 species. However, neither was found considers the parasites that actually are known to be taken by the cleaners. The fish species to be prey. hosting the various isopods and also the trematode and leech are listed in Table 2. Listed also Ectoparasites in the diet of cleaners relative are the three fish-species on which no ectopara- to ectoparasites on fishes that are cleaned.- sites were found. Many of the ectoparasites listed above infest

505 FISIIERY BULLETIN: VOL. 69. NO. 3

A C

\"I

D E F

FIGURE7.-Representatives of the families of ectoparasitic copepods found to infest fishes in the La Jolla area. A. Bomolochidae (Bomolochus longicaudm, female, after Cressey, 1969b) ; B. Caligidae (Caligus hobsoni, male, after Cressey, 1969a) ; C. Dichelesthiidae (Hatschekia pacifica, female, after Cressey, 1970) ; D. Lernaeidae (Peniculus fissipes, female, after Wilson, 1917) ; E. Chondracanthidae (Chondracanthus gracilis, female, modified after Wilson, 1935) ; F. Lerneopodidae (Epibranchiella septicaudrc, female, after Shiino, 1956).

506 HOBSON: CLEANING SYMBIOSIS

topsmelt each carried from 1 to 23 specimens of the copepod Caligus serratus on their body surface. Two topsmelt also carried the copepod Parabomolochus constrictus on their gills, a single parasite on one, four on the other. Two topsmelt also carried the copepod Peniculus fissipes embedded in their fins. Six of the eight seiioritas that had been cleaning topsmelt when collected had ectoparasites among their gut con- 1 mm tents. Five contained only Caligus serratus- I I as many as 73 in each fish. One other contained only 10 ,mathiid larvae, a parasite that was not FIGURE8.-Gnathiid larva from the body surface of the black-and-yellow rockfish, Sebustes chrysomelus. seen on the topsmelt themselves; however, as noted above, I suspect that this parasite is more widespread than our survey data indicate. fishes that rarely or never interact with cleaners. Six species of ectoparasites were collected In considering the ectoparasites found in the gut from 20 garibaldis, 184 to 240 mm long. Nine- of particular seiioritas, it would be most mean- teen garibaldis each carried 1to 144 Caligus hob- ingful to do so in regard to the ectoparasites soni on their body surface. Thirteen each carried known to be hosted by the species of fishes that 1 to 4 individuals of an unidentified species of these particular seiioritas were cleaning when Lepeophtheirus on their body surface, and one collected. Of the 27 cleaning seiioritas taken carried a single Eomolochus ardeole in its for the gut-content analysis, 15 (56%) were branchial cavity. In addition, four carried 1 cleaning blacksmiths, 8 (30%) were cleaning to 8 gnathiid isopod larvae, two carried a single topsmelt, 2 (7%) were cleaning garibaldis, and leech, and one carried a single monogenetic 2 (7%) were cleaning halfmoons. Thus the trematode, all on their body surface. The two selection closely parallels the relative frequency seiioritas that were collected as they cleaned with which seiioritas were observed cleaning garibaldis had preyed mostly on gnathiid larvae, these same species (Table 1) and is a good sample with each containing over 400 of these parasites. of the fishes that are cleaned by seiioritas. In addition, one had consumed six Caligus hob- Three species of ectoparasites were collected soni, and the other had taken five Lepeophtheirus from 10 blacksmiths, 141 to 199 mm long. Each SP. of these blacksmiths carried from 2 to 39 indi- Four species of ectoparasites were collected viduals of the copepod Caligus hobsoni on their from 13 halfmoons, 166 to 295 mm long. Twelve body surface. One specimen also carried a single of the 13 halfmoons each carried 1 to 75 Caligus gnathiid isopod larva on its body surface, and hobsoni on their body surface. Each of two also another the copepod Clavellopsis flexicurvica on carried a single Lepeophtheirus sp. on its body a gill arch. All 15 seiioritas that were collected surface, and each of six carried 2 to 7 Peniculus as they cleaned blacksmiths contained either fissipes embedded in its fins. In addition, each Caligus hobsoni or gnathiid larvae, but no other of six carried from 2 to 16 monogenetic trema- ectoparasites: one contained gnathiids alone, todes on its body surface. Of the two seiioritas seven contained C. hobsoni alone, and seven con- collected as they cleaned halfmoons, each contained both gnathiids and C. hobsoni. Up to 256 tained only Caligus hobsoni in its gut contents, individuals of C. hobsoni and up to 263 gnathiid one a single specimen and the other eight. larvae were counted from among the stomach Significantly, with the exception of the gnath- contents of individual seiioritas that had been iid larvae in a cleaner of topsmelt, as discussed cleaning blacksmiths. above, no parasite was found in the cleaner’s Three species of ectoparasites were collected gut contents that did not occur on the species from 13 topsmelt, 122 to 212 mm long. These of fish that was being cleaned by the cleaner

507 FISHERY BULLETIN: VOL. 69, NO. 3

when it was collected. This fact further sup- the body surface of a singIe sheephead, and this ports the contention that cleaning tends to be fish has not yet been seen being cleaned. Fur- species-specific for n given seiiorita. thermore, up to 4 gnathiid larvae, which cleaners The data clearly show that the parasites most take from other fish, were found on 3 of the frequently taken by sefioritas are certain mobile sheephead. Similarly, the treefish, Sebastes ser- forms that occur on the body surface of their yiceps, which is heavily infested with caligids, host. It may be that other parasites on the ex- has not yet been seen being cleaned. The tree- ternal body surface are not taken. No leeches or fish is not known to carry C. hobsoni, but 13 of trematodes were found among gut contents, 15 specimens examined carried up to 12 Lepeoph- even though these forms are abundant on theirus longiges on their body surface, and 3 the garibaldi and halfmoon. Also, the gut con- carried up to 5 gnathiid larvae. The significance tents did not show evidence of the lernaeid of these exceptions to what seems a valid gener- Peniculus fissipes, an immobile form which par- alization has not been determined. Perhaps it tially embeds itself in the skin of its hosts- is significant that these two species of fish are mostly on the fins. This parasite occurs on top- not heavily infested by copepods of the genus smelt, garibaldis, and halfmoons among those Caligus, as are the more frequently cleaned known to be c!eaned by seiioritas. However, fishes. negative evidence based on the meager gut-con- The many parasites that infest the oral and tent data are weak, especially as the cleaning branchial cavities might seem to be potential labrid Labroides ph,thirophayus in Hawaii, prey for cleaners, but I found no evidence that which feeds mostly on caligoid copepods, fre- these parasites are taken by seiioritas. quently takes lernaeids (Randall, 1958; Young- The principal ectoparasites on the body sur- bluth, 1968). I would expect additional study face of the two most frequently cleaned fishes, to show that cleaning seiioritas at least occasion- the blacksmith and the topsmelt, are the copepods ally take P. fissiges. Nevertheless, several Caliyzls hobsoni and C. serratus, respectively, abundant fishes infested by P. fissipes, but not which are very similar to one another morpho- found to carry caligids, gnathiids, or other mo- logically. With just one exception among the bile external forms, were not seen being cleaned. fishes surveyed (discussed below), C. serratus For example, the white seaperch is one of the seems to be restricted to topsmelt. On the other most abundant species at the 3- to 10-m station hand, C. hobsoni occurs on a wide variety of off La Jolla and yet was never seen being cleaned. species and is also the principal form on gari- Twelve specimens of this fish were examined, baldis and halfmoons. Interestingly, a list of and the only ectoparasites found were one to the fishes hosting this parasite, ranked by in- four P. fissiges on three individuals. Similarly, cidence (Table 3), looks much like the ranking the only parasite found on 11 rainbow seaperch, of fishes that were observed being cleaned by the an abundant species in the study areas that was sefiorita (Tab!e 1). not seen being cleaned, was a single P. fissipes on one individual and two on another. The importance of cleaning in reducing the However, not all fishes whose external body incidence of ectoparasites on fishes.-Certainly surfaces are heavily infested by mobile forms cleaners remove many ectoparasites from the were observed being cleaned. The sheephead, bodies of certain fishes-the numbers in their Pimelometogon pzilchrum, is a case in point. diet attest to this fact. But does cleaning in Caligus hobsoni occurs on this fish, but only in- fact appreciably reduce the level of infestation frequently-a single specimen of this copepod on these fishes, or do other parasites quickly was taken from each of 2 of the 14 sheepheads replace those that are removed by the cleaners? that were examined. However, the sheephead Although this question is difficult to answer, some is heavily infested by two species of Lepeophthei- insight is provided by observatioxs on the gari- rus, a genus of copepods that is closely related baldi. When guarding eggs on their nests dur- to Caligus. Up to 70 L. parvus were taken from ing the reproductive season, male garibaldis be-

508 HOBSON: CLEANING SYMBIOSIS come especially intolerant of the presence of fested fishes. The samples included too few of other fish species. Clarke (1970) recorded the the other parasites to make a meaningful com- number of times garibaldis, in defence of their parison. It remains a question why Lepeoph- territory, attacked fish of various other species theiws sp. and the gnathiid larvae did not show at different times of the year. He found that a pattern of occurrence similar to that of C. when males were guarding eggs their attacks on hobsoni, as both of these parasites are known seiioritas increased elevenfold. Not surpris- to be prey of the cleaners. In any event, these ingly, I saw no cleaning of garibaldis that were data add to the evidence which indicates that guarding eggs. At other times of the year male C. hobsoni is the primary prey of cleaning seii- garibaldis do not guard their territory as vigor- oritas in the study areas. ously against members of other species and are frequently seen being cleaned. A series of these Ectoparasites on Seiioritas males were collected both in and out of the reproductive season, and the numbers of ectopar- Seiioritas that were closely observed as they asites they carried were assessed. Seven indi- cleaned other fishes often were noted to have viduals (mean length 228 mm) sampled as they caligid copepods on their bodies. One sefiorita, guarded their eggs carried a mean of 67 Caligus about 120 mm long, was host to an estimated hobsoni (range 20-144), 2.5 Lepeophtheirus sp., 100 of these parasites concentrated especially 1.4 gnathiid isopod larvae, and 0.2 monogenetic along the dorsal-fin base. These observations trematodes. These counts contrast strikingly were significant because during the survey for with those from six males (mean length 219 mm) ectoparasites, most seiioritas taken from the pop- sampled outside the reproductive season, which ulation at Iarge were free of external forms, carried a mean of only 4.8 C. hobsoni (range although many carried a chondracanthid cope- 0-13), 1 Lepeophtheims sp., 0.8 gnathiid larvae, pod on their gills. and no monogenetic trematodes. These findings Twenty seiioritas, 102 to 190 mm long, were suggest that males which are guarding eggs be- sampled from among those giving no indication come heavily infested with C. hobsoni when they of being cleaners. Eight of these carried 1 or do not allow cleaners to approach them, a con- more of the chondracanthids on their gills, but clusion strengthened by the fact that over this only 2, or lo%, had parasites on their external same period the relative numbers of this same body surfaces: one of these carried 10 speci- parasite were not noted to change on other in- mens of Culigus hobsoni and 1 specimen of

TABLE3.-Hosts of Caligus hobsoni.

Species

I I I mean (range) I Blacksmith, Chromir punrfipinnir IO IO 10.6(2391 100 Topsmelt, Athrrinopi a541 13 113 100 Garibaldi, Hyp~rpop~rubirundn 20 19 95 Halfmoon, Mrdinluw celi(ornirnrir 13 12 92 Opaleye, Girrlle nigrirnni IO a 80 Olive rockfish, Stbartrr Itrrnnoidrr 11 5 45 Blue rockfish, Stbortcr myrtinur 9 4 44 Sharpnose seaperch, Phonrrodon otriptr 13 5 38 Senorita, Oxyjulir rolilornico 36 9 24 Sheepheod, Pimdomrtopon pulrhrum 14 2 14 Rubberlip perch, Rhororhilur tomtti IO 1 IO Cabezon, Srorpernirhfhyr mnrmomtur IO 1 IO Gopher rockfish, Stbnrtrr rnrnotur 11 1 9 Pile perch, Rhororhilur vocca 15 1 7 Kelp rockfish, Srbnrtrr otrovirtnr 16 1 6

.Ithrrinopr afinir does not carry C. hobroni, but rather is the sole host (with one exception, see text) of the very sirnilor C. rtrratu. FISHERY BLLLETIN: VOL. 69, NO. 3

Lepeophtheirus sp.; the other seiiorita carried pected with fewer seiioritas present. Neverthe- a single Lepeophtheirus sp. Comparative data less, even considering the smaller numbers, the mere obtained by examining 16 senoritas, 114 to seiioritas present at lower temperatures seem 160 mm long, that had been cleaning. Of these, less active than those present at higher temper- 11, or nearly 70 p, carried copepod parasites on atures. The effect was striking on one occasion their external body surfaces: 6 carried from at 25 m when, with an influx of warm water, 1 to 59 Caligus hobsoni, 4 carried from 1 to 9 C. the temperature rose suddenly from 11" to serratus, and 1 carried 3 Lepeophtheirus sp. 14.5" C. No change was noted in the numbers Significantly, those seiioritas carrying Caligiis of seiioritas present over this short period of hobsoni all had been cleaning blacksmiths, those time, but where no cleaning had been seen dur- carrying C. serratus had been cleaning topsmelt, ing a 20-min survey immediately before, shortly and the one carrying Lepeophtheirzss sp. had after the temperature rise six different groups been cleaning a garibaldi. Thus the ectopara- of fishes being cleaned were in view simultane- sites found on cleaning seiioritas were in all in- ously. stances forms that also infest the species which that particular seiiorita had been cleaning. The Turbidity.-When the water is turbid because occurrence of C. serratus is especially interest- of plankton or suspended sediment, there is no- ing, because these sefioritas are the only fish ticeably less cleaning activity than when the other than topsmelt found so far to carry this water is clear. The fishes are generally more parasite. wary, and remain closer to cover when visibility Alerted to the phenomenon, I inspected the is reduced. bodies of many seiioritas that incidentally passed by during various phases of the work under- Surge.-When there is a strong surge, a fre- water. Ectoparasites were evident on some, but quen t occurrence, especially in water less than only on a small minority of the population. That 10 m deep, there is far less cleaning activity than the vast majority are not infested by such par- when the water is still. asites accounts for the observation, noted above, that seiioritas do not crowd around cleaners that Day-night.-The sefiorita, a strictly diurnal initiate activity in their midst, as do blacksmiths, species that takes shelter under cover at night, topsmelt, halfmoons, and others. does not clean after dark. On the basis of these data, and on the general cleaning picture that has developed, I believe that at least most of the seiioritas infested with caligid copepods are cleaners. Presumably they acquire these parasites while intimately associated with the former hosts during cleaning. That a given cleaner is found to carry parasites similar to those on the fish it has been attending, but no others, is further evidence that cleaning by individual seiioritas tends to be species-specific.

9 Environmental Factors That Influence Cleaning 161' 156* 150' 144' 139' 133' 128' 122. 117' 11 I' 106'PC) TEMPERATURE Temperature.-As noted above, the numbers FIGURE9.-Number of sefiorita cleaning bouts seen dur- of seiioritas present at the 20- to 25-m station ing each of 33 observation periods, 15-25 min long, at fluctuated in an apparent response to water different water temperatures in an area 25 m deep at temperature, with the critical level at about 12" La Jolla. Periods during which temperature A uctuated to 13" C. Less cleaning occurred at lower tem- were not considered. n = number of observation periods at that temperature; where n > 1, value given is the peratures (Figure 9), which would be ex- mean.

510 IIOBSOW: CLEANING SYMBIOSIS

CLEANING ACTIVITY OF THE (Table 4). Despite the fact that sefioritas were SHARPNOSE SEAPERCH observed to be far more numerous than perch throughout the depth range of this study Unlike seiioritas, which clean as adults as well (3-50 m), seaperch performed almost all as juveniles, all of the sharpnose seaperch that I the cleaning observed at the 30- to 35-m lo- observed cleaning were juveniles less than about cation, where cleaning by the much more 125 mm long. Occasionally noncleaning sea- abundant seiiorita was limited to a few isolated perch swim in groups of 15 or more, but those instances. seen cleaning were always solitary, or in groups A measure of the incidence of cleaning indi- of two or three. In agreement with seiioritas, viduals within the population of juvenile sharp- cleaning seaperch do not establish well-defined nose seaperch was obtained during 39 observa- cleaning stations, but instead may clean other tion periods at the 20- to 25-m and 30- to 35-m fish at any point as they move from place to locations at La Jolla. These observations, to- place. I found no evidence that fishes which taling more than 26 hr, were made from Sep- are residents of other areas come to where sea- tember 1968 to February 1969. During this perch are located for cleaning; rather, cleaning period, 201 juvenile seaperch were seen, of which seaperch occur where resident fishes are nu- 105, over 52%, were cleaning other fishes. Thus merous. As is true of seiioritas, seaperch use it appears that at least most sharpnose seaperch the same picking technique to clean material are cleaners when they are juveniles, whereas from the bodies of other fish that they use to only a small minority of the seiiorita population take small organisms from a benthic substrate. seem to be cleaners. Clearly bottom-picking can be preadaptive to cleaning. Cleaning by seaperch, as by seiioritas. Fishes Cleaned by the Sharpnose Seaperch usually occurs within 3 m of the substrate. How- ever, there is little overlap in the cleaning areas Because sharpnose seaperch were observed of the two species: generally seaperch clean at only at depths below 20 m, substantially less data greater depths and/or in colder water than are available on their cleaning activity than on seiiori t as, where limited observations indi- that of seiiokitas. Of the 105 seaperch obqerved cate they may predominate as cleaners even cleaning during the 39 observation periods re- when sefioritas are more abundant. Data ported above, all but one were cleaning black- illustrating this distribution of cleaning activ- smiths; the lone exception was cleaning a soli- ity at a point in time were obtained at the tary blue rockfish, Sebastes mystinus. On two 20- to 2E-m and 30- to 35-m locations off other occasions, I saw sharpnose seaperch clean- La Jolla, where the two species co-occur ing rubberlip perch, but otherwise the only fish seen being cleaned have been blacksmiths (Fig- ure 10). Undoubtedly additional observations, TABLEI.-Number of bouts in which sharpnose seaperch and sefioritas, respectively, were seen cleaning other especially in other areas, would expand this list. fishes during 15-min observation periods at the 20- to I observed seiioritas cleaning in many different 25-m and 30- to 35-m locations off La Jolla. Two obser- areas, but my observations of cleaning seaperch vation periods, one at each location, and never more than are limited to La Jolla. Clarke et al. (1967) 45 min apart, were made on each of the dates indicated. saw a sharpnose seaperch cleaning a rockfish at -7 Number of cleoning bouts observed 150 m off La Jolla, and Gotshall (1967) reported Dote I 20- to 25-m location I 30- to 35-m location what he believed to be this species cleaning Motu I Seoperch I SeSorito I Seoperch I Seiiorito mola off Monterey. Yet no matter how many 22 Nov. 2 13 17 0 27 Nov. 0 7 1 0 different species the seaperch may in fact clean, 9 Jon. 2 5 9 0 there seems no doubt that blacksmiths are prime IS Jon. 2 4 8 0 3 Feb. 2 12 9 2 recipients in southern California, at least in Total 8 41 44 2 depths shallower than 35 m.

511

...... I ." . . FISHERY BULLETIN: VOL. 69, NO. 3

to have been cleaning blacksmiths, were each kept under surveillance for 15 min, while their activity was monitored on tape. Both swam on irregular courses among the rocks but remained within an area encompassing about 15 to 20 111'. During this time one entered into 4, the other 5, separate cleaning bouts, averaging 2.6 (range 0.5-7.5) and 1.8 (range 0.75-3.5) min long, respectively, all with blacksmiths. The cleaner initiated the activity in each instance, but immediately thereafter a number of other blacksmiths converged on the spot. Most of the cleaning bouts continued after the original blacksmith had left the group, and a succession of others arrived and departed before the bout ended. Although usually they hovered head-down before the cleaners, the blacksmiths nevertheless assumed a wide variety of attitudes. During much of the time they swam with the blacksmiths, the two seaperch under surveillance closely inspected the blacksmith's bodies and actually picked at them 18 and 14 times, respectively. Most of the cleaning was directed at the fin bases, particularly the caudal. While in company with the blacksmiths, one of the seaperch broke away from the group and swam to look closely at the dorsal fin of a blue rockfish. However, no cleaning oc- FIGURE10.-Sharpnose seaperch inspecting a blacksmith, curred: the blue rockfish swam away as though which hovers to solicit cleaning. uninterested in cleaning and the seaperch returned to the blacksmiths. When not in company Specific Cleaning Interactions -Seaperch- with the blacksmiths, the two seaperch swam Blacksmith alone 1 or 2 m over the substrate. One descended to the bottom twice and picked at gorgonians: The limited observations on cleaning by sharp- five times on the first descent, once on the nose seaperch provide details only on interac- second. tions with blacksmiths. As nearly as could be Once a blacksmith was seen obviously attempt- seen, when sharpnose seaperch clean blacksmiths ing to present its caudal fin to a seaperch, with- the activity proceeds much as it does when black- out success in enticing the seaperch to clean. smiths are cleaned by sefioritas, as described Close inspection did not reveal parasites, but above. However, the observations were too few part of the fin was torn away and shredded to determine whether or not cleaning activity flesh was exposed. Apparently this blacksmith is consistently initiated by the cleaner. Several was presenting a point of irritation to the clean- times blacksmiths hovered in their typical head- er, which in this instance was an injury, not a down posture before seemingly unresponsive sea- parasite. Some cleaners, for example, Abudef- perch, but perhaps the seaperch had earlier made duf troschelii,which picks molting skin from the some initial gesture. Whenever it could be de- GalSpagos marine iguana (Hobson, 1969b), termined, the seaperch initiated the cleaning. will clean dead or injured itssue, but at least Some details were obtained at the 20- to 25-m on this occasion the seaperch showed no inter- location at La Jolla, where two seaperch, known est.

512 HOBSON: CLEANING SYMBIOSIS

Material Removed from Other Fish by the perch, 80 or 81 mm long, speared in this habitat, Sharpnose Seaperch were filled with (showing percent of total volume) caprellid amphipods (80 % ) , gammarid To determine the food of cleaning seaperch, amphipods (5%), isopods (2%1, fragments of I examined the gut contents of 16 specimens, algae with encrusting bryozoans (10%) ,and un- 74 to 122 mm long, that were speared as they identified crustacean parts (3%). Quast (1968) cleaned blacksmiths. Food items in their guts, found that specimens from a kelp bed had fed ranked as percentage of each item in the entire mostly on small bottom-dwelling crustaceans, sample, were as follows: caligid copepods, 68% ; polychaetes and bivalves, as well as kelp frag- caprellid amphipods, 16% ; gnathiid isopod lar- ments, some of which were heavily encrusted vae, 9%; algae, 1% ; and unidentified items, with bryozoans. Thus the bottom-picking feed- 6%. Thus ectoparasitic caligids and gnathiids ing habits of the white seaperch are very similar made up 7'796 of the material. All 16 specimens to the noncleaning habits of the sharpnose sea- contained ectoparasites; in fact, ectoparasites perch. constituted the vast bulk of the material in all On one occasion, I saw a white seaperch swim but one individual, which had fed more heavily 1 or 2 m above the surfgrass in company with on caprellids. As with seiioritas, when an appre- a lone blacksmith, which hovered head-down in ciable amount of free-living material was pres- the manner typical of one that desired to be ent, it was usually sharply divided from the ecto- cleaned. The white perch picked at the black- parasites and more digested to the rear in the smith's body several times, but the bout was digestive tract. All the identifiable caligid cope- brief, and the perch soon joined a group of 8 pods among this material were Caligus hobsoni, to 10 others of its own kind near the surfgrass which is consistent with what is known of ecto- below. This seaperch, which proved to be 79 mm parasites on blacksmiths, the species cleaned by long, was speared, and its gut contents included these seaperch, and indicates feeding habits si- 58 caprellid amphipods, a single gammarid am- milar to those of the cleaning seiiorita, presented phipod, one small isopod, plant fragments with above. encrusted bryozoans, and some unidentified non- parasitic crustacean remains. No ectoparasites Incidental Cleaning by a Close Relative were found; its food was similar to that of the Although sharpnose seaperch were not seen other white seaperch reported above. On an- in water less than 20 m deep, the white seaperch, other occasion I saw a white seaperch cleaning a very similar species, is frequently abundant several blacksmiths over a sandy bottom in 12 m there. The white seaperch was probably the of water, but this individual was not collected. most numerous of the embiotocids during most Probably the observed cleaning was no more of the observations made at the 3- to 10-m lo- than a brief incidental activity for these fish. cation off La Jolla. Underwater the white sea- At no other time did I see any indication of clean- perch and the sharpnose seaperch are nearly ing by this species, but perhaps the activity is identical, but can be distinguished by the dusky more frequent under appropriate conditions. bordered caudal fin of the former and the black- tipped pelvics and more pointed snout of the CLEANING ACTIVITY OF latter. THE KELP PERCH White seaperch are especially abundant in groups of 10 or more close to surfgrass in 3 or Because the kelp perch is not abundant in the 4 m of water off La Jolla. Typically they hover La Jolla study area, where larger kelps are head-down; in this attitude they are not solic- sparse, most observations of cleaning by this iting cleaning but rather are intently regarding fish were made incidentally during other projects the surface of the vegetation, at which they pick in areas heavily forested with kelp. However, occasionally. Tiny organisms that live on the these other projects generally were centered on surfgrass are prey of these fish: five white sea- the sea floor, whereas kelp perch concentrate

513 FISHERY BULLETIN: VOL. 69. NO. 3 above in the midwater and canopy regions. volume) : gnathiid isopod larvae (50 o/o ) , non- Nevertheless, observations of cleaning were suf- parasitic isopods (5 5% ) , gammarid amphipods ficiently frequent to recognize this species as a (55), caprellid amphipods (20c/c),and uniden- habitual cleaner, though probably less so than tified material (20% ) . Neither of the two that either the sefioritas or the juvenile sharpnose were not known to have cleaned contained evi- seaperch. In taking material from the bodies dence of ectoparasites: one was full of caprellid of other fishes, the kelp perch uses the same amphipods (90 ) and unidentified material picking technique that it employs to pick items (lop) , whereas the other had nothing in its from an algal substrate, or that are adrift in digestive tract except a few unidentified frag- midwater. Its pointed snout and dentition, which ments posteriorly. is similar to that of the seiiorita, as described Limbaugh (1955) reported kelp perch clean- above, are well suited to cleaning. ing kelp bass, opaleyes, garibaldis, blacksmiths, Insofar as an aggregation of kelp perch tends and walleye surfperch (Ilyperprosopon argen- to remain in one location, these fish can perhaps teum). be regarded as maintaining a station at which other fishes are cleaned. But I saw no indication DISCUSSION that more than one or a few members of a given aggregation clean, or that other fishes come to Various cleaning fishes remove a wide variety these locations from any distance for cleaning. of deleterious material from the bodies of the In fact, I saw only blacksmiths and other kelp animals they service. In addition to ectopar- perch being cleaned by this fish. In the one asites, this material includes diseased, injured, observation of intraspecific cleaning, a single or necrotic tissue, fungi, and unwanted food kelp perch swam among others of its aggrega- particles (Feder, 1966; Hobson, 1968, 1969b; tion, intently inspecting their bodies. Usually and others). However, the discussion below con- the subject of this attention moved away, where- siders cleaning only as the removal of ectopar- upon the cleaner moved to another fish. A few asites, because my data indicate that these are responded to the cleaner by erecting their fins the only items taken in significant amounts from and hovering immobile in a head-down posture, California fishes by the cleaners considered in and these were cleaned. Occasionally a fish be- this report. ing cleaned suddenly darted away as if the cleaner had been too vigorous in its attentions. All INCIDENTAL VS. HABITUAL CLEANING blacksmiths being cleaned were solitary individuals that hovered in head-down soliciting Cleaning is widespread among small-mouthed fashion close to an aggregation of kelp perch. marine fishes that characteristically pick minute Whether or not one of the perch had earlier organisms from the substrate (Hobson, 1968). made an initiating overture was never deter- Included are species of the families Chaetodon- mined. Never more than one or two of the perch tidae, Pomacentridee, Labridae, Embiotocidae, in the aggregations were seen cleaning these Blenniidae, and others. Morphological and be- blacksmiths. Occasionally a cleaner would close- havioral characteristics suited to their way of ly follow a halfmoon or kelp bass that inciden- life have preadapted many species of these fami- tally passed close by, but I saw no evidence that lies for the cleaning habit. Probably some such these fish were interested in the perch, and no fishes pick ectoparasites only incidentally during cleaning occurred. routine foraging when under certain conditions Three kelp perch, 94 to 99 mm long, one of the body of an adjacent fish, infested with ecto- which had been cleaning a blacksmith, were col- parasites, becomes accessible as just another lected from an aggregation hovering near a feeding substrate. The relative tendency of a stand of feather-boa kelp. The gut contents of given species to clean likely is influenced by both the individual known to have cleaned the black- short-term and long-term environmental smiths contained (showing the percent of total changes. Such changes may be expected to alter

514 HOBSON: CLEANING SYMBIOSIS interspecific relations, by affecting not only the seems to be characteristic not so much of a spe- relative availability of various prey organisms cies as of just certain individuals. At least at and the incidence of various ectoparasites, but a given time, most seiioritas do not clean, where- also the species composition of the interacting as some seem to be facultative cleaners, and a fishes themselves. few might even be obligate cleaners. Juvenile In California the white seaperch likely is one sharpnose seaperch follow a similar pattern, but of those species that cleans only occasionally as with a relatively higher incidence of individuals an incidental adjunct to regular foraging. Sever- that clean. Limited data can only suggest that al other California species reported by Limbaugh the status of the kelp perch may be similar. (1955) and Gotshall (1967) clean, including black perch, pile perch, and rainbow seaperch, CLEANING INITIATED BY THE SE~ORITA but they have not been seen doing so by me. The report of cleaning by the blacksmith (Tur- Usually there seem to be fishes present that ner et al. 1969) remains an anamoly, as this fish need cleaning, as shown when a seiiorita identi- does not fit the pattern of a bottom-picking pred- fies itself as a cleaner by initiating action with, ator described above. However, it may be sig- say, a blacksmith or a topsmelt, and immediately nificant that many of those substrate-picking is converged upon by many other fish that crowd predators which clean most frequently are spe- in its way seeking attention. That such fishes cies that also feed on material adrift in mid- generally wait for a seiiorita to begin the clean- water, as do the seiiorita, sharpnose seaperch, ing, rather than attempting to initiate activity and kelp perch. Thus this mode of feeding too, themselves with one of the many seiioritas including the taking of plankton, may, in some present, likely reflects a low probability of suc- species, favor adaptations that are suited to cess if they make the first move. If, as it seems, cleanirig. Fishes that are adapted to both sub- the vast majority of seiioritas are not cleaners, strate-picking and plankton-picking may possess or at least not currently predisposed to clean, adaptations especially well suited to cleaning. then random efforts to solicit service would not Probably many species of fishes clean inci- seem adaptive. dentally on isolated occasions, but relatively few This situation contrasts with that of the Ha- are habitual cleaners. And even the habitual waiian wrasse Labroides phthirophagus, of cleaners vary greatly in the degree to which they which all individuals seem to be obligate cleaners are specialized for this habit. Species of the (Youngbluth, 1968), and which is not nearly Indo-Pacific labrid genus Labroides are highly as abundant on Hawaiian reefs as the seiiorita specialized cleaners that feed almost exclusively is in California. In centering their activity on ectoparasitic crustaceans (Randall, 1958; around well-defined stations, the distinctive L. Youngbluth, 1968). These fishes possess many phthirophagus can be recognized readily by specific morphological and behavioral specializa- others that need cleaning. Thus, not surpris- tions that are adapted to this way of life (Feder, ingly, cleaning encounters that involve L. phthi- 1966; Losey, 1971). However, only a small mi- rophagus are regularly initiated by fishes seek- nority of cleaners are so highly specialized; most ing cleaning (Losey, 1971). are but part-time practitioners of the cleaning We have seen that under certain circumstances habit, with much of their food being derived various fishes initiate cleaning encounters from other sources. with seiioritas. Some fishes successfully do so That some cleaners depend on ectoparasites by hovering amid unusually dense concentra- for prey, whereas others can subsist equally well tions of seiioritas, but the overtures of such fish on food from other sources, has led to classifying are not directed at individuals ; rather, they are various species as either obligate or facultative broadcast to the assemblage at large. The suc- cleaners (e.g., Youngbluth, 1968). The seiiorita, cess of this tactic presumably follows the proba- sharpnose seaperch, and kelp perch may well bility that an individual predisposed to clean oc- resist being so classified because their cleaning curs among such a large number of seiioritas.

515

.. _. I- FISHERY BULLETIN: VOL. 69, NO. 3

Kelpfish regularly solicit cleaning from indi- all of the different species are essentially the vidual seiioritas, but the situation is exceptional. same. , Because kelpfish rise into midwater for cleaning, Cleaning by the seiiorita may not be specim- it appears that they do not receive satisfactory specific on those few occasions when the cleaning service in their regular habitat amid benthic veg- activity is initiated by the fish in need of such etation. In their usual surroundings, where they service, for example by the kelpfish, as described are extremely diRcult to discern, the cryptic above. Although they show some difficulty lo- kelpfish may be relatively inaccessible to cleaning cating a receptive seiiorita, kelpfish nevertheless seiioritas. One can see why a fizh thus handi- seem far more successful at doing so than one capped might be required to initiate needed would expect if indeed they are required to find cleaning itself. The number of unsuccessful at- one that will clean only kelpfish. Thus, although tempts experienced by kelpfish before a seiiorita individual seiioritas seem to be species-specific was finally induced to clean them underscores when they themselves initiate cleaning, they may the existing problem of locating a cleaning indi- be considerably less so, and perhaps even non- vidual. specific, when the other fish makes the initial overture. There are no data on this point, how- SPECIES-SPECIFIC CLEANING ever. The extent to which these considerations ap- Because the cleaning sefiorita initiates most ply to juvenile sharpnose seaperch and kelp of its activity, it has the opportunity to select perch cannot be ascertained because data are its clients, and the data indicate that a species- lacking. specific choice is exercised. That individual cleaners tend to limit their selection to members SIGNIFICANCE OF POSTURES ASSUMED of only one species may be related to the fact BY FISHES THAT SOLICIT CLEANING that they initiate cleaning on the home ground of the fishes they serve, when these fishes are When members of an assemblage of fishes like engaged in some of their regular activity, As blacksmiths or topsmelt converge on a cleaning each of these clients has distinctive habits, a seii- site that has developed in their midst, probably orita approaching to clean a fish of one species their attention was initially alerted by the un- faces a somewhat different situation than a seii- natural-appearing posture assumed by the indi- orita approaching to clean a fish of another spe- vidual first approached by the cleaner. Usually cies: The distinctions often are subtle, but may this posture does not seem to be assumed pur- be significant enough to account for a given posefully, but rather results when the fish, hav- seiiorita’s tendency to seek out members of only ing ceased swimming and immobilizing its fins, one species. passively drifts out of its regular attitude (Hob- Again we can draw a contrast with the clean- son, 196513). The posture thus assumed varies, ing behavior of Labroides phthirophagus, indi- especially between species, where perhaps dif- viduals of which receive members of many dif- fering centers of gravity are determining fac- ferent species at well-defined cleaning stations tors. Thus the blacksmith usually hovers head- (Randall, 1958; Youngbluth, 1968). Probably down, whereas the topsmelt is more often such nonspecific cleaning is characteristic of tail-down. Sometimes an unnatural-appearing cleaners whose activity is confined to these estab- posture is actively assumed when the fish at- lished locations. Fishes that visit such cleaning tempts to present to the cleaner a certain part stations enter the cleaner’s own territory, and of its body, presumably that part carrying an frequently join a mixed-species group that hov- irritation. By virtue of their unusual appear- ers in wait for service. In tending these fishes ance, these postures in cleaning interactions on its home ground, the cleaner is receiving serve to draw attention to the fish that is cleaned. them on its own terms, so to speak, so that the It does not seem necessary that any particular situations surrounding cleaning bouts with posture be assumed, only that it look out of the

516 IIOBSON: CLEANING SY.MBIOSIS ordinary. Reports are widespread (see Feder, has identified itself by initiating activity with 1966) of cleaning recipients assuming these un- some fish in the area. Once this has occurred, natural-appearing postures. one can see the value of the posture, when as- Attention-getting postures assumed by fishes sumed by the first fish to be approached, as a being cleaned probably occurred incidentally cue in alerting other fish that need cleaning to during the early development of cleaning sym- the presence of a cleaner. In effect, then, the biosis, when fishes hovering to be cleaned quite fish assuming the soliciting posture advertises naturally stopped moving and passively drifted the temporary existence of the transient cleaning out of their regular attitudes. As the various “station” €0 other potential recipients of clean- cleaning relations evolved, apparently this ob- ing. Well-defined cleaning stations like those vious cue subsequently assumed a different role of Labroides phthirophagus do not need this sort as a signal in different situations. Generally of advertisement, as their locations are well these postures are suggested to be signals be- known to the fishes that visit them. Nor is it tween the recipient of cleaning and the cleaner, necessary that cleaning individuals of L. phthi- indicating a readiness to be cleaned. Quite likely rophagus be pointed out, as all members of that this is the primary signal-function in activity distinctive species are cleaners. Despite this, involving such cleaners as Labroides phthiro- it is probable that fishes hovering to be cleaned ghagus, where all members of the species are at a Labroides station themselves create a visual cleaners and where activity is centered around cue that tends to attract other fishes. cleaning stations that are well known to other There may also be a maladaptive aspect to fishes in the area. In this situation a fish in the postures assumed by fishes that solicit clean- need of cleaning should be reasonably successful ing; In hovering at an unnatural angle, fins im- in advertising its condition by assuming the mobile and erect, a fish may enhance its chances characteristic soliciting posture before a fish of being cleaned, but it would also seem likely recognizable as a cleaner. Losey (1971) showed to draw the attention of predators and to handi- that various fishes regularly employ this tactic cap itself in evading attack. Perhaps such an to induce L. phthirophagus to clean them. Ob- increased vulnerability accounts at least in part servations in the Gulf of California demonstrated for the sharp decline in cleaning that occurs that the cleaning station itself has played a role with reduced visibility, when predators can ap- in establishing the soliciting posture as a cue. proach closer undetected. Increased vulnera- There I have seen the goatfish Mulloidichthys bility may also account for the observation dentntus hovering head-down at cleaning sta- reported earlier (Hobson, 1965~1,where poma- tions of the butterflyfish Heniochus nigrirostris, dasyids in the Gulf of California abruptly broke when the resident cleaner was itself temporarily away from cleaners when a predator approached. absent. Losey (1971) observed similar behavior among Hawaiian fishes. In such a situation the THE POSSIBILITY THAT FISHES BEING hovering posture probably alerts the cleaner to CLEANED EXPERIENCE STRESS fishes that have arrived for cleaning. However, in cleaning activity involving the Being prodded and picked over by an animal seiiorita, the soliciting posture usually is assumed of another species would seem to require a dif- only after cleaning has been initiated by the ficult adjustment for a fish. It may well be that cleaner. The problem of recognizing an indi- fishes experience stress under this circumstance, vidual that will clean among the vast majority even when the behavior is well established. Cer- of seiioritas that do not clean, coupled with the tainly observations have shown that this exper- absence of well-defined cleaning stations, would ience can be uncomfortable, judging from how reduce the adaptiveness of the client’s soliciting often fishes being cleaned suddenly bolt forward, posture as a cue to initiate cleaning. Probably and swim away, apparently having been nipped the most effective way for a fish to obtain needed too vigorously by the attending cleaner. Some- cleaning in this situation is to wait until a cleaner times too, a fish approached by a cleaner clearly

517 FISHERY BULLETIN: VOL. 69, NO. 3 experiences conflicting responses, one moment I doubt that cleaners enjoy immunity in tolerating or even soliciting the cleaner’s atten- the sense that predators, recognizing them as tions, and the next moment chasing it away on benefactors, actively avoid preying on them. each approach. Such ambivalent behavior was Cleaners may recognize those predators which especially evident in rubberlip perch. Losey are not at that time intent on feeding and may re- (1971) noted that Labroides phthirophagus in strict their cleaning to such individuals. A preda- Hawaii is sometimes attacked by fishes that it tor that assumes a soliciting posture may effec- attempts to clean, and suggested that this may tively advertise this situation, and no doubt other occur when the cleaning is painful to the host cues exist. Such mechanisms would reduce the fish. chance of cleaners placing themselves in vulner- The color changes shown by many fishes being a.ble situations while cleaning. In addition, clean- cleaned (Randall, 1958; and others) may in fact ers probably are not as vulnerable while cleaning be manifestations of stress. It is well known large predators as might be expected simply be- that many fishes experience color changes in re- cause cues characteristic of feeding situations sponse to stress. Earlier (Hobson, 1965a) I dis- are not present. In associating themselves so cussed the striking color change of the goatfish intimately with predators, cleaning fishes show Mulloidichthys de.iztatzcs when it solicits cleaning behavior that is so unlike that of prey that preda- in the Gulf of California, and pointed out that tors probably do not regard them as food. How- this fish shows the same color change in other ever, even if such factors do reduce the danger situations that are obviously stressful. Such that might seem inherent in the cleaning act, color changes have been regarded as signals be- I doubt that their cleaning role affords these tween the fishes being cleaned and the cleaners, fishes any security from being eaten in non- (e.g., Feder, 1966), functioning in the cleaning cleaning situations. interaction much like the soliciting attitudes discussed above. As with the attitudes, any role PARASITES AS PREY OF THE such color changes may now have assumed as a CALIFORNIA CLEANERS signal probably evolved from an incidental by- product of early cleaning. I have no data on this It is hardly surprising that the fishes which point relating to the California species, as such are cleaned most frequently in California are color changes are not especially evident in fishes those which are the most abundant and at the that were observed being cleaned there. same time carry the most ectoparasites. Thus the blacksmith, topsmelt, halfmoon, and gari- ARE CLEANERS IMMUNE FROM baldi are the fishes cleaned most frequently, PREDATION? and the survey of ectoparasites showed them to be among the most heavily parasitized. The Reportedly some cleaners are immune from vast majority of ectoparasites on these particular predation because of the service they provide fishes are mobile forms, mostly caligid copepods the predators (Feder, 1966; and others). Lim- and gnathiid isopod larvae, that occur on the baugh’s (1961) belief that the seiiorita enjoys body surface of their hosts. That these same such immunity is based on observations of this parasites were found to make up the diet of the labrid entering the open mouth of kelp bass to cleaners attending these fishes is consistent with clean and on not finding it among the stomach the observation that only the exteriors of fishes contents of predators during a food-habit study. were seen being cleaned during this study. However, Quast (1968) found seiioritas in the Although the forms infesting the external stomachs of kelp bass, and H. Geoffrey Moser, body surface are the most numerous ectopara- U.S. National Marine Fisheries Service (unpub- sites on the fishes available to the California lished data), found seiioritas in stomachs of the cleaners, many other types were found to infest bocaccio, Sebastes pamispinis, and the starry the oral and branchial cavities. One might ques- rockfish, S. constellatus. tion why these other parasites do not seem to be

618 HOBSON : CLEANING SYMBIOSIS taken, especially as Limbaugh (1955, 1961) re- type predominates; rather, they occur in a wide ported seiioritas entering the mouth of the kelp variety of forms, none widespread among the dif- bass and cleaning beneath the gill covers of the ferent species of fishes, and none especially garibaldi. Furthermore, such behavior has been abundant (except on an occasional individual widely reported for some other cleaners, such as fish). Thus a cleaner probably could not subsist species of Labroides (Eibl-Eibesfeldt, 1955; on one type alone but would have to master a Randall, 1958; and others), and some echeneids repertoire of specialized techniques in order to are known to habitually feed on copepods from exploit enough of these varied forms to make the branchial cavities of sharks (Cressey and it worthwhile. And before access is gained to Lachner, 1970). Nevertheless, any such activity the site of infestation, a much more refined clean- by seiioritas must be relatively rare. In discuss- er-host interaction must have evolved than is ing this situation I limit my remarks to the necessary when parasites are simply cleaned seiiorita, because data are presently insufficient from the external body surface. No such re- to determine whether the same may apply to lation would evolve unless the cleaner acquired the sharpnose seaperch and kelp perch. the precise manipulations necessary to pick at- Seiioritas would not be expected to take par- tached parasites off the gills without damaging asites from the oral or branchial cavities as often the delicate gill membranes. Obviously the as species of Labroides or echeneids if for no cleaning relation would not be adaptive if such other reason than they simply are too large rel- damage occurred. In short, to feed habitually ative to most of the fishes they clean. Whereas on parasites from the oral and branchial cavities species of Labroides or the echeneids are small would seem to require a higher degree of spe- enough to enter the oral and branchial cavities cialization than has been demonstrated -by the of most of the fishes they service, the seiiorita seiiorita. It seems unlikely that such special- is nearly as large, and sometimes even larger, ization would develop as long as the more abun- than most of its clients. Significantly, Limbaugh dant and readily available forms on the body observed seiioritas cleaning within the oral and surfaces continue to satisfy the cleaning needs branchial cavities of kelp bass and garibaldis, of the species. Certainly judging from the way both of which are relatively large species. Most blacksmiths, topsmelt, and other fishes vigor- of the seiiorita’s cleaning is directed toward ously compete to have their external parasites smaller species, like the blacksmith and the removed, it would seem that there is little imme- topsmelt. diate chance of these parasites falling into short The specialized techniques that would be re- supply. quired to prey on the parasites of the oral and branchial cavities would probably pose another CLEANING SYMBIOSIS AND THE problem to the seiiorita. In its regular habit DISTRIBUTION OF SHORE FISHES of taking parasites from the external surfaces of fishes, the cleaning seiiorita concentrates on In his often-cited report on cleaning symbiosis, just a few forms that not only are numerous Limbaugh (1961: 48) stated: on many of the most abundant fishes, but also In my opinion it is the presence of the sefiorita and are not too dissimilar from free-living prey of kelp perch that brings the deep-water coastal and the species, Sometimes these external forms pelagic fishes inshore to the edge of the kelp beds also occur in the branchial cavity, and some on the California coast. Most concentrations of reef similar forms, e.g., bomolochids (Figure 7), ha- fishes may similarly be understood to be cleaning stations. Cleaning stations would therefore account bitually occur there and in the oral cavity. But for the existence of such well-known California sport- the majority of parasites characteristic of the fishing grounds as the rocky points of Santa Catalina branchial and oral cavities are aberrant forms, Island, the area around the sunken ship Valiant off e.g., dichelesthiids, chondracanthids, and lerne- the shore of Catalina, the La Jolla kelp beds and sub- opodids (Figure 7), and these are unlike any- marine canyon and the Coronado Islands. thing else encountered by the seiiorita. No one Presumably this conclusion was intuitive, as no

519 FISHERY BULLETIN: VOL. 69, NO. 3 data were presented. In his review of cleaning spatial reference point. Obviously such fishes symbiosis, Feder (1966: 368), basing his con- will center themselves here, because the sur- clusion on Limbaugh’s work, similarly stated: rounding featureless substrate does not meet “In all probability, many good fishing grounds their requirements. I am describing a well- are such primarily because they are cleaning known phenomenon, one that is the rationale be- stations.” I believe that this contention is un- hind constructing artificial fishing reefs. Thus founded. Seiioritas are the major cleaners in food and a suitable substrate often appear to be California inshore waters, so that if cleaning key features in a habitat that supports large symbiosis does account for most concentrations numbers of fishes. Of course to cite just one or of reef fishes in this region, as Limbaugh sug- the other would be an oversimplification, as re- gested, then seiioritas would be the cleaner large- quirements in both must be satisfied, along with ly responsible. Cleaning occurs wherever seii- many other perhaps more subtle needs. The var- oritas are concentrated but clearly is not a major ious species assembled at such locations inter- activity of the population, even though it may act in a variety of ways; cleaning symbiosis is be so for a relatively few individuals. In any one such interaction, and undoubtedly an impor- event, it seems safe to conclude that cleaning tant one, but hardly the prime reason for them is not among the major factors determining the being there. distribu!ion of seiioritas. And if cleaning does not determine the distribution of seiioritas them- CHANGES IN HABITS WITH TIME selves, it seems unlikely that it would determine the distribution of other species. Uncertainty remains regarding changes in Undoubtedly many factors contribute to cre- habits with time. The picture of activity devel- ating si,tuations that draw concentrations of oped in this report was derived directly by ob- fishes to certain locations. Where a number of serving activity and also indirectly by examining different species have similar requirements, as- both digestive-tract contents and the specific semblages will develop where cpnditions satis- ectoparasites that infest the various fishes. But fying these requirements are optimum. The these methods only define situations that exist presence of these fishes increases the complexity over a relatively brief span of time. Data on of the environment, thus creating situations that individual activity over longer periods are need- support still other species, and so on. Often ed. Certainly habits of individuals change with it is apparent that certain features are especially time, but how much change and over how much significant as a basis for these concentrations. time? The fact that material in the digestive Consider, for example, the rocky points that Lim- tracts frequently occurs in sharply delimited baugh included in his list of “well-known Cali- homologous blocks indicates that these fishes fornia sport-fishing grounds.’’ The flora and often feed heavily or even exclusively on one fauna of these locations are generally rich, a particular type of prey, and then abruptly shift fact probably related to such local features as to something else. Are habits such as a relative converging currents that frequently produce up- tendency to clean and to clean members of just welling and nutrient-rich waters. Plankton is one species immutable characteristics gf indi- commonly abundant here, along with plankton- viduals, or have the observations described in feeding fishes like the blacksmith. Seiioritas this report simply defined temporary situations and other species frequently are numerous here that the various individuals just happened to be too, but the main attraction seems to be a gen- experiencing at the time they were singled out erally rich food supply rather than available for study? It is possible that all seiioritas clean cleaning. Similarly it is unrealistic to attribute at one time or another, though not all at once, concentrations of fishes around sunken ships to and only a few at a time. It is also possible that cleaning activity. Where a wreck has settled a seiiorita, which tends to clean members of just on an open expanse it becomes a haven for fishes one species during a given period of cleaning, that require a nearby structure for cover or a may select members of another species during

520 HOBSON: CLEANING SYMBIOSIS

a subsequent period of cleaning. Despite these and the same seems to be true of the kelp perch. questions, the conclusions drawn in this report The incidence of cleaners is much higher among are dependent only on an accurate assessment juvenile sharpnose seaperch, but the adults of of the immediate situation, so that their validity this species do not seem to clean regularly. The is not affected by whether or not the habits of major food of all three species is free-living or- individuals under study remain basically un- ganisms which they pick from a substrate and changed over time. midwater. 4. There is little overlap between the cleaning A NOTE ON INDIVIDUAL VS. areas of the three species. The seiiorita is the SPECIES HABITS major cleaner in southern California inshore waters by virtue of its great abundance in a Information on variations in feeding behavior variety of rocky habitats. However, the kelp among individual fish under natural conditions perch may be the predominant cleaner in the is difficult to acquire. Typically a given behavior canopy region of the kelp beds, where the spe- is described as a species characteristic, and the cies concentrates, and the sharpnose seaperch extent to which this behavior varies among the is the predominant cleaner where it occurs at different members of the species is unknown. depths below about 20 to 30 m and/or water Observations of cleaning by the seiiorita dem- under 12" or 13" C, even though the seiiorita onstrate that different individuals in a popula- may be more abundant. tion may react differently to a given situation. 5. The seiiorita and sharpnose seaperch do not Unquestionably this phenomenon extends beyond establish well-defined stations at which they re- cleaning behavior to other facets of the animal's ceive other fishes seeking to be cleaned-a situ- activity. If, as is probable, some of the charac- ation frequently described for other cleaner teristics of individual fish result from early im- fishes. Rather, as they move from place to place, printing, then different members of the same individuals of these species approach and clean population could be expected to react differently other fishes in various different locations. in certain situations throughout life. In any 6. Cleaning activity by these species is essen- event, it seems unquestionable that the behavior tially limited to removing ectoparasites from the of an individual is considerably more limited than external body surfaces of fishes. They do not that descriptive of its species, or even its own ordinarily take parasites of the oral and branch- population. ial cavities. The dentition of the seiiorita and kelp perch, which is similar and which includes a number of long, curved canines that project CONCLUSIONS forward at the front of each jaw, seems especially suited to pick ectoparasites. 1. Three inshore species of fishes in southern 7. The major prey taken by these fishes California are habitual cleaners: the seiiorita, through cleaning are caligid copepods and gnath- the sharpnose seaperch, and the kelp perch. A iid isopod larvae. The species of parasite taken number of other species clean occasionally as most often by the seiiorita and sharpnose sea- an incidental adjunct to their regular feeding. perch is Caligus hobsoni. 2. The seiiorita may clean throughout its post- 8. Some species of fishes are cleaned far more larval life, whereas cleaning by the sharpnose often than others, and many species that co- seaperch is an activity largely of juveniles. The occur with these cleaners are not cleaned at all. life-history period during which kelp perch clean The fishes most frequently cleaned are those has not been defined. which at the same time are most abundant and 3. Cleaning is of secondary significance to most heavily infested with ectoparasites. The these species, although it may be of major sig- most numerous ectoparasites on these fishes are nificance to certain individuals. Only a few of caligid copepods, the most abundant of which is the many sefioritas present at a given time clean, C. hobsoni.

52 1 FISHERY BULLETIN: VOL. 69. NO. 3

9. Cleaning effectively reduces the number of from being eaten during noncleaning situations. ectoparasites that infest the external body sur- 18. Cleaners are widespread among small- faces of fishes that interact with the cleaners. mouthed marine fishes that characteristically 10. At any given time, many individuals of pick tiny organisms from a substrate. This mode the more frequently cleaned species are in need of feeding, especially when combined with the of cleaning. Nevertheless, in activity involving capacity to pick tiny prey that are adrift in mid- the seiiorita, infested fishes do not ordinarily water, preadapts fishes Io the cleaning habit. attempt to initiate cleaning but instead wait for 19. There is no basis for the contention that cleaning to be initiated by the cleaner. Because many of the good fishing grounds in southern the vast majority of sefioritas are not cleaners, California are such because fishes have congre- or at least are not currently predisposed to clean, gated to be cleaned by resident cleaners. random efforts to solicit cleaning from seiioritas 20. Feeding behavior varies significantly in the population at large would not be adaptive. among individuals of at least some species. Thus 11. When initiating its cleaning activity, a the habits of an individual can be more limited given individual seiiorita tends to approach and than those descriptive of its species or even its clean members of only a single species of fish. own population. 12. Because the vast majority of seiioritas are not currently predisposed to clean and because there are no well-defined cleaning stations, the unnatural-appearing posture assumed by a fish ACKNOWLEDGMENTS approached by a cleaner is an important cue in advertising the location of available cleaning to Lloyd D. Richards assisted me in collecting other fish in need of this service. the data for this study, I thank Roger F. Cressey 13. Fishes being cleaned probably experience and Thomas Bowman, U.S. National Museum, some degree of stress. The color changes ex- who identified the parasitic copepods and iso- hibited by some fishes when being cleaned are pods, respectively, around which much of this essentially manifestations of this stress; sec- study is centered. I thank, too, Carl L. Hubbs ondarily, they may have assumed a signal-func- and Richard H. Rosenblatt, Scripps Institution tion in certain cleaning interactions. of Oceanography, and John R. Hunter, U.S. Na- 14. While intimately associated with the fishes tional Marine Fisheries Service, for helpful com- they clean, seiioritas frequently become infested ments on a draft of the manuscript. themselves by the same parasites they are attempting to remove from these other fishes. 15. Cleaning activity is sharply curtailed when visibility is reduced by turbid water or when there is strong water movement, such as a heavy REFERENCES surge. CLARKE,T. A. 16. Cleaning activity among these fishes is a 1970. Territorial behavior and population dynam- diurnal phenomenon. There is no evidence that ics of a pomacentrid fish, the garibaldi, Hypsypops it continues after dark. rubicunda. Ecol. Monogr. 40: 189-212. 17. Any so-called “immunity” from predation CLARKE,T. A., A. 0. FLECHSIG,AND R. W. GRIGG. that a cleaner may enjoy probably relates (1) to 1967. Ecological studies during Project Sealab 11. Science (Wash., D.C.) 157: 1381-1389. an ability to recognize predators that are not in- CRESSEY,R. F. tent on feeding and to limit cleaning to such indi- 1969a. Caligus hobsoni, a new species of parasitic viduals, and (2) to the fact that behavior exhib- copepod from California. J. Parasitol. 65: 431- ited by a cleaner servicing a predator is so unlike 434. 1969b. Five new parasitic copepods from California that of prey that the predator does not regard the inshore fish. Proc. Biol. SOC.Wash. 82: 409-427. cleaner as food. However, their role as cleaners 1970. Hatschekia pacifica new species (Copepoda: probably does not afford these fish any security caligoida) a parasite of the sand bass, Paralebrax

522 IIOBSON: CLEANING SYMBIOSIS

nebulifer (Giard). Proc. Biol. SOC. Wash. 82: LONGLEY,,W. H., AND S. F. HILDEBRAND. 843-846. 1941. Systematic catalogue of the fishes of Tor- CRESSEY,R. F., AND E. A. LACHNER. tugas, Florida. Pap. Tortugas Lab. 34. Carnegie 1970. The parasitic copepod diet and life history Inst. Wash. Publ. 535, 331 p. of diskfishes (Echeneidae). Copeia 1965 : 310-318. LOSEY,G. S., JR EIBL-EIBESFELDT,I. 1971. Communication between fishes in cleaning 1955. uber Symbiosen Parasitismus und andere symbiosis. In T. C. Cheng (editor), Aspects of besondere zwischenartliche Beziehungen tropis- the biology of symbiosis, p. 45-76. Univ. Park cher Meersfische. Z. Tierpsychol. 12 : 203-219. Press, Baltimore. FEDER,H. M. MILLER,D. J., D. GOTSHALL,AND R. NITSOS. A field guide some common ocean sport 1966. Cleaning symbiosis in the marine environ- 1965. to fishes of California. revision. California De- ment. In s. M. Henry (editor), Symbiosis, Vol. 1, 2d p. 327-380. Academic Press, New York. partment of Fish and Game, 87 p. GOTSHALL,D. W. QUAST,J. C. Cleaning symbiosis in Monterey Bay, Cali- 1968. Observations on the food of the kelp-bed 1967. fishes. W. J. North and C. L. Hubbs (editors), fornia, Calif. Fish Game 53: 125-126. In Utilization of kelp-bed resources in southern Cal- HOBSON,E. S. ifornia, p. 109-142. Calif, Dep. Fish Game, Fish Forests beneath the sea. Animals 1965a. 7: 506- Bull. 139. 611. RANDALL,J. E. A visit with el barbero. Underwater Nat. 1965b. 1958. A review of the labrid fish genus Labroides, 3(3) : 5-10. with descriptions of two new species and notes on 1965c. Diurnal-nocturnal activity of some inshore ecology. Pac. Sci. 12: 327-347. Copeia fishes in the Gulf of California. 1965: 1962. Fish service stations. Sea Frontiers 8: 291-302. 40-47. 1968. Predatory behavior of some shore fishes in ROEDEL,P. M. the Gulf of California. U.S. Fish Wild. Serv., 1953. Common ocean fishes of the California coast, Res. Rep. 73, 92 p. Calif. Dep. Fish Game, Fish Bull. 91, 184 p. 1969a. Comments on certain recent generalizations SHIINO,S. M. regarding cleaning symbiosis in fishes. Pac. Sci. 1956. Copepods parasitic on Japanese fishes. 12. 23: 35-39. Family Lernaeopodidae. Rep. Fac. Fish. Prefect, 1969b. Remarks on aquatic habits of the Galapagos Univ. Mie 2: 269-311, marine iguana, including submergence times, TURNER,C. H., E. E. EBERT, AND R. R. GIVEN. cleaning symbiosis, and the shark threat, Copeia 1969. Man-made reef ecology. Calif. Dep. Fish 1969 : 401-402. Game, Fish Bull. 146. 221 p. HIJBBS, C. L., AND L. C. HUBBS. WILSON, C. B. 1954. Data on the life history, variation, ecology, 1917. North American parasitic copepods belonging and relationships of the kelp perch, Brachyistiuu to the family Lernaeidae with a revision of the frenatus, and embiotocid fish of the Californias. entire family. Proc. U.S. Natl. Mus. 53: 1-150. Calif. Fish Game 40: 183-198. 1936. Parasitic copepods from the Pacific coast. LIMBAUGH,C. Am. Midl. Nat. 16 : 776-797. 1966. Fish life in the kelp beds and the effects of YOUNGBLUTH,M. J. kelp harvesting. Univ. Calif, Inst. Mar. Resour. 1968. Aspects of the ecology and ethology of the IMR Ref. 55-9, 168 p. cleaning fish, Labroides phthirophague Randall. 1961. Cleaning symbiosis. Sci. Am. 205: 42-49. Z. Tierpsychol. 25: 915-932.