Blennioidei: Clinidae)

BULLETIN OF MARINE SCIENCE, 41(1): 45-58,1987

COLOR PATTERN AND HABITAT DIFFERENCES BETWEEN MALE, FEMALE AND JUVENILE GIANT KELPFISH (BLENNIOIDEI: CLINIDAE)

Carol A. Stepien

ABSTRACT The giant kelpfish, Heterostjehus rostratus occurs in three color morphs; red, brown, and green, which vary in shade according to number ofmelanophores. Color morphs were usually collected from plant habitats matching their colors. Frequencies of the color morphs were linked to sexual dimorphism; adult males are brown (infrequently olive green) and adult females exhibit all three morphs. Juveniles are either brown or green and not sexually dimorphic. In addition to color differences between the sexes, adult males and females display different melanin patterns. These patterns are apparently used for intraspecific communication and cryptic coloration. Brown males are distinguishable from brown females by their sexually dimorphic melanin patterns. Melanin patterns, unlike coloration, change (often rapidly) during courtship and territorial displays. Adult males and females occupy plant habitats that differ in depth, predominant color, and species composition. The brown males closely ap- proximate color of the plants where the nests they guard are found. Females occupy other habitats, including red algae, green surfgrass, and other species of brown algae. Females venture away from matching habitats during the spawning season to reach male territories.

The giant kelpfish Heterostichus rostratus Girard is one of the largest members of the family Clinidae, reaching a total length of 41.2 cm (J. E. Fitch in Feder et aI., 1974). Ranging from British Columbia (Canada) to Cape San Lucas, Baja California (Mexico), it is most commonly encountered from Point Conception to central Baja California (Roedel, 1953). Heterostichus occurs in three basic color morphs, red, green, and brown. Kelpfish often blend closely with the plants in which they live, seldom moving and assuming a location in the midst of fronds, at a similar angle of inclination. Similar tri -color systems of red, green, and brown morphs appear to be common in several other blennioid fishes also inhabiting nearshore plants off the U.S. Pacific coast. Wilkie (1966) described the red, green, and brown color morphs of the penpoint gunnel Apodichthys flavidus (Pholididae) and Burgess (1976; 1978) described them in the rockweed gunnel Xererpesfucorum (Pholididae). The clinid Gibbonsia elegans also occurs in red, green, and brown morphs (Stepien, in press). All four genera (Heterostichus, Gibbonsia, Apodichthys, and Xererpes) are most frequently found in plant habitats of matching colors. Hubbs (1952) described color patterns of the giant kelpfish according to melanin patterns and color ranges exhibited by each color range within each pattern. C. L. Hubbs, in Hubbs, 1952 observed that Heterostichus readily changed from one color pattern to another in an aquarium, such as from barred to striped. This type of rapid change involves melanophore changes rather than a true color change. Color (color morph) in the present study was classified separately from the over- lying melanin pattern (Stepien, 1985 and Materials and Methods). Pigment analyses conducted by Wilkie and Stepien (Stepien, 1985) demon- strated that Heterostichus color morphs have different integumentary carotenoid pigments. Red morphs contain astaxanthin and green morphs have tunaxanthin, whereas brown morphs have canthaxanthin, as well as both of the above. Unlike

45 46 BULLETINOFMARINESCIENCE,VOL.41, NO. I, 1987

melanin patterns, changes in color morphs occur relatively slowly, involving acquisition or loss of types of pigments (Bagnara and Hadley, 1973; Fox, 1976). Such color changes encompass both changes in amount of pigments deposited in individual chromatophores and changes in numbers of chromatophores (Bagnara and Hadley, 1973; Britton, 1983). The present study analyzed sexual and developmental differences in color patterns and plant habitats of the giant kelpfish. These differences may be used to generate hypotheses about the evolution of intraspecific color variation. The following data were compared: (1) collection depths and habitats, (2) colors of fish and plant habitats, (3) melanin patterns, and (4) degree of association of kelpfish with habitats.

MATERIALS AND METHODS

Collection and Description. -Approximately 660 kelpfish were collected in waters to 35 m deep by scuba diving off Santa Catalina Island, California during 1979 to 1983. An additional 42 kelpfish were collected from subtidal sites off the southern California mainland, including Ventura, Palos Verdes, Redondo Beach, Huntington Beach, and La Jolla. Collection methods were previously described (Stepien, 1985; 1986a). The following data were recorded for each individual at the time of collection: (I) color and species of plants in the collection site; (2) color morph and melanin pattern of the fish; (3) behavior of the fish and its degree of association with the collection site, including territorial defense against intruding con specifics and other fishes, close association with a particular plant, or swimming through several plant habitats; (4) collection depth (depths from 0 to 10 m were measured with a capillary depth gauge for increased accuracy at shallow depths, and those greater than 10 m were measured with an oil-filled gauge. All depths were corrected to mean lower low water). All kelpfish and samples of associated plants were brought into the laboratory for color description under standard conditions. Color and melanin patterns were described (Fig. I) at time of first sighting before collection and under daylight standard conditions within 2 h after collection. Total lengths of live kelpfish were recorded and the fish were sacrificed in order to determine sex and gonadal development (Stepien, 1985; I986b). Expected frequencies of males and females in various habitats were calculated from the overall proportions of each sex collected in the study. These were compared to the observed frequencies using G-tests (chi-square tests) (Sokal and Rohlf, 1981). Numbers of male and female kelpfish collected in close association with plants were similarly statistically compared. Color Classification. - The Munsell Color System (Munsell, 1946; 1969; 1976) was the standard method used for color designation. I have previously shown that this system is highly accurate and repeatable for describing kelpfish colors (Stepien, 1985). Fish and plant colors were measured under daylight illumination within 2 h after collection, against a neutral grey background, and using neutral grey masks to block out adjacent colors on the charts, as recommended (ASTM, 1974; 1980). A laminated chart for field and underwater use was constructed from Pantone Paint Company color chips which were visually matched to the Munsell chips. Color of the kelpfish was measured from an area directly posterior to the pectoral fin. Kelpfish having a strongly variable pattern ofIight and dark areas were given two separate notations, corresponding to average dark and average light colors. Munsell hues in the present study were grouped as major colors in data analysis as follows, according to the ISCC-NBS Color Name Charts (Kelly and Judd, 1976): GREEN:a) Olive Green 10 Y, 7.5 Y, 5Y; b) Yellow Green 7.5 GY, 5 GY, 2.5 GY; c) Green 10 GY, 2.5 G. BROWN:a) Gold Brown 2.5 Y; b) Brown 5 YR, 7.5 YR; c) Orange Brown 5 YR, 2.5 YR. RED: a) Brown Red 10 R, 7.5 R; b) Red 5 R, 2.5 R; c) Purple Red 10 RP.

RESULTS Frequencies of the Color Morphs. -Individual kelpfish examined in this study exhibited a single color morph, which persisted for long periods of time (weeks), even when the fish was kept in the laboratory without a matching background. Red, yellow, and brown pigments appeared to be contained in chromatophores STEPIEN: COLOR PATTERN AND HABITAT DIFFERENCES OF GIANT KElPFISH 47

Figure I. Drawings of kelpfish melanin patterns. (A) Plain pattern. (B) Barred pattern. Note clear areas (fin windows) in dorsal and anal fins. (C) Striped pattern. (D) Mottled pattern. 48 BULLETIN OF MARINE SCIENCE. VOL. 41. NO. I. 1987

NUMBER OF MALE AND FEMALE COLOR MORPHS ,eo 33.0"* '--I I '60 I NUMBER OF MALE AND FEMALE JUVENILE COLOR MORPHS I I I 50 I 140 I I I •• I Females ~ MALES J fill] I 40 '20 I ~ Males IEl FEMALES I ___ EJilPeCled frequency .- Expected freq . J 100 ~ ~ 30 Q. > Q; -,::> '0 "'0 eo 12' ~ .8 20 .P E E ::> ::> Z Z 60 r''; . I 10 40

o I 20 GREEN JUVENilES BROWN JUVENILES B

BROWN GREEN RED

A COLOR OF FISH

Figure 2. Number of brown, green, and red kelpfish color morphs collected. Chi-square values indicate differences between numbers of males versus females of each morpho * = Significant difference (P < .001). --- = Expected frequency per number of males and females in the population. (A) Number of adult male and female color morphs. N = 396 (229 females, 167 males). (B) Number of juvenile male and female green and brown color morphs. There are no significant differences (0.05 level). N = 104.

although yellow-green pigments often permeated the skin and underlying muscle tissue in green fish and did not appear to be solely confined to chromatophores. The three basic color morphs of kelpfish contained several different shades per morph, according to the Munsell designations of hue, value (lightness), and chroma (saturation). Green color morphs included olive green and yellow green shades; brown morphs included gold brown and orange brown shades, while red morphs fish ranged from brown red to purple red. Frequencies of adult color morphs (maturity of both sexes being reached at approximately 18 cm TL and an age of 1 to 1.5 years) (Stepien, 1985; 1986b), were found to differ significantly between males and females. Almost all males collected were brown (164 of 167), the other 3 were green (Fig. 2A). These males were exclusively olive green in shade. Females of all three color morphs were collected, although brown morphs were approximately twice as common (I13 brown, 55 green, and 61 red morphs). There were no significant size differences between the 3 colors of adult females. Significantly more brown fish were males than females, and significantly more green fish were females. No red males were collected during the present study. The smallest red female collected in the present study was 17.4 cm TL and aged as 11 to 12 months. Juveniles occurred in two different color morphs, green and brown. The frequencies of the two colors did not correspond to sex (Fig. 2B). There were approximately equal numbers of brown and green males and females, although green juveniles were more abundant than brown. STEPIEN: COLOR PATTERN AND HABITAT DIFFERENCES OF GIANT KELPFISH 49

Tab]e 1. Colors, melanin patterns, sizes, and gonadal maturity of kelpfish collected from sites along the southern California mainland (M = mature, I = immature, N = 42)

Total length Location (em) Color Melanin pattern Sex Maturity Ventura 13.0 Brown Plain F I 13.5 Brown Plain F I 13.6 Brown Plain F I 16.0 Brown Plain M I 23.2 Brown Mottled M M Palos Verdes 8.1 Brown Plain F I 9.5 Green Mottled M I 13.6 Green Striped F I 14.8 Brown Mottled M I 19.2 Brown Striped M I 20.4 Green Plain F M 20.9 Red Barred F M 23.6 Brown Plain F M 24.] Brown Mottled M M 30.6 Green Plain F M Redondo Beach 10.0 Brown Plain F I 10.7 Brown Plain F I 11.3 Brown Plain F I 11.5 Brown Plain M I 11.5 Brown Plain M I 12.0 Brown Plain F I 14.2 Brown Mottled M I 14.7 Brown Barred F I 17.4 Red Barred F M 18.9 Brown Plain M I 19.0 Red Barred F M 21.2 Red Barred F M 22.4 Brown Barred F M 23.6 Brown Mottled M M 24.6 Brown Plain F M 24.8 Brown Mottled M M 28.6 Brown Mottled M M Huntington Beach 14.6 Brown Plain F I 19.0 Red Barred F I La Jolla 11.2 Green Striped M I 14.3 Brown Striped M I 15.2 Brown Barred F I 15.2 Brown Mottled M I 16.8 Green Barred F I 20.7 Red Barred F M 22.8 Brown Plain F M 28.5 Green Plain F M

Colors and sexes of kelp fish from locations along the southern California mainland were very similar to those from Santa Catalina Island (Table 1). Color of freshly-laid or well-developed ripe eggs from 33 female kelpfish were observed during the course of the study. Brown females most often had brown eggs (20 of 32), but a considerable number had red eggs (12 of 32). Red females sampled had either brown (6) or red (5) eggs. Melanin Pattern Frequencies. -Although color morphs did not rapidly change in either the laboratory or in situ, the dark patterns produced by melanophores could change rapidly. Male and female adults could usually be distinguished by presence 50 BULLETIN OF MARINE SCIENCE, VOL. 41, NO. I, 1987 of one of four different melanin patterns, the frequencies of which differed significantly between the sexes (Fig. 3A). Female kelpfish most often exhibited barred or plain melanin patterns (Fig. lA, B), while males most often had striped or mottled patterns (Fig. 1C, D). Each fish appeared to display a particular melanin pattern, although the patterns sometimes changed rapidly (within seconds) in both the field and laboratory. Melanin pattern changes occurred when the fish were subjected to stress, such as when handled, and during courtship and territorial displays. During incidences of stress, most kelpfish assumed a barred pattern. During courtship and territorial displays, females became barred while males assumed an intensified striped pattern. Skin samples of the three kelpfish color morphs, which were examined under a dissecting microscope and melanophores per area counted, indicated that barred fish had the greatest number of melanophores. Plain fish contained few melanophores, which at maximal pigmentary expansion produced only a slight barring. Male kelpfish usually had an intermediate number of melanophores. The majority of red fish collected had barred melanin patterns, while most green females were either plain or barred (Fig. 3B). Brown females were more frequently plain than barred. Although most mottled kelpfish were males (Fig. 3A), mottled females were relatively common (Fig. 3B). It was sometimes difficult to distinguish barred from mottled patterns. In the majority of cases, brown females could be distinguished from brown males by their melanin patterns. Kelpfish from southern California mainland collections displayed similar sexual dimorphism in melanin patterns (Table 1). Melanin patterns of adult kelpfish were also correlated with plant habitat. Kelp- fish collected in algae having thin and finely branched thalli typically were barred or mottled. These included kelpfish in red algae, and brown Sargassum spp. and Cystoseira neg/ecta. Kelpfish in algae having wide blades, including Macrocystis pyrifera and Eisenia arborea, most often had plain or slightly striped patterns. Although melanin patterns are sexually dimorphic, the number of melanophores and degree of expansion also appear to be related to the type of habitat. Melanin patterns, as well as color, were consistent in given habitats. Brown and green juveniles exhibited plain, barred, mottled, or striped melanin patterns. These melanin patterns appeared more variable than those of adults, often changing in the laboratory and in the field and individuals displayed one particular pattern less consistently. Melanin patterns did not appear to be correlated with sex or habitats of juveniles. Other Disruptive C%ration. - The majority of kelpfish have other disruptive coloration marks. For example, plain and barred females (72%) had a white dorsal nose bar that extended the length of the head (split-head pattern, see Barlow, 1967). Males less frequently had the nose bar (34%), and the bar was less pro- nounced when present. Almost all females (87%) had numerous fin windows, which are transparent areas in the dorsal, anal, and caudal fins extending across one or more rays. These were located within the less-pigmented areas between the vertical bars of barred fishes, and also occurred in most plain females (shown in Fig. 1). Males either lacked the fin windows or had very few, limited to the anterior and posterior ends of the dorsal and caudal fins. Approximately 50% of large females (24 cm TL or larger) had a small (approximately 4 to 5 mm in diameter) circular red spot (in varying locations) along one side, above or below the lateral line. Some kelpfish had white lateral patches of various sizes and intensities arranged linearly under the lateral line. These were particularly prom- inent in plain females captured in Macrocystis and Eisenia. Some kelpfish had STEPIEN: COLOR PATTERN AND HABITAT DIFFERENCES OF GIANT KELPFISH 51

rn J: Q. a: rn o ::; \"::; "0 a: ":?:::::: o a:" ..J aJ o c: U ~ Q. W ~ ..J 'iO « Q. ::; c: w u. rn i: u. Q;'" o c: ::;; rn "0 w " c: aJ (5" u .c:'" z C- w ::l o o E w 0 a: "0 u. rn u z a: w c: t- ~ t- o « aJ .Ii Q. z Q. Z « ..J woo o o o o o o o ::; lXI t-- <0 ... (') "' '" m

x w rn en > z a: w t- t- « Q. z z « ..J w ::;;

o o o o o lXI <0 .•. 8 '" 52 BULLETIN OF MARINE SCIENCE, VOL. 41, NO. I, 1987

NUMBER OF COLOR MORPHS IN PLANT HABITATS NUMBER OF JUVENILE COLOR MORPHS IN PLANT HABITATS

'30 280 158· COLOR OF FISH .20 240 o Brown G,•• n 110 Brown juveniles 220 fZI 0 i:ZI Red .00 D Green juveniles 200 90 180 ~ "~ E! 80 Q. .80 Q; .~ 70 140 '""0 ~ 80 l;; 120 "0 .c l;; E 50 , 100 .c z E 40 80 Z 19.93* 80 30 7.0S* 20 40

10 20

MacrocystisSargassum Cystoseira Eisenia Phyllospadix Blown spp. Green spp. Redspp. ~------,'Brown spp '--'Green spp A PLANT HABITATS B PLANT HABITATS

Figure 4. Numbers of kelpfish color morphs on colors of plant habitats. Chi-square values indicate significant differences in numbers of kelpfish matching versus not matching plant habitat color. * = Significant difference (P < 0.01). (A) Adult kelpfish. N = 396 (229 females, 167 males). (B) Juvenile kelpfish in brown and green plant habitats. Plants include Macrocystis pyrifera, Sargassum muticum, Cystoseira neg/ecta, Eisenia arborea, and Phyllospadix torreyi. * = Significant difference (P < 0.000 I). N = 263.

varying numbers of these lateral white spots scattered along their sides, resembling the encrusting bryozoan Membranipora spp. common on Macrocystis and Eisenia blades. Habitats of M ales, Females, and Juveniles. - Most kelpfish of all three color morphs significantly matched the color of their plant habitats at the time of collection (Fig. 4A, B). Nonmatching fish in red or green plant habitats were most often brown in color. Brown and green juvenile morphs also were most frequently collected on matching colors of plant habitats (Fig. 4B). There were more nonmatching (brown) juveniles than adults on green Phyllospadix torreyi. Groups of juveniles swimming in loose schools in Phyllospadix beds often included both color morphs. Kelpfish collected in matching plants were very hard to see. Once located, they were usually easy to collect, since most remained relatively stationary in plants. When chased, they often entered a nearby matching plant, again assuming a stationary position, later returning to the original plant. The majority of those collected were feeding, when they briefly left their cover to dart out at small passing fishes and crustaceans. Those most difficult to collect were actively swimming and not associated with a given plant. Kelpfish off matching plant habitats appeared to be more wary of divers, readily swimming away and avoiding net capture. Kelpfish were most frequently observed while feeding in early morning and late afternoon hours, and least often collected in midday. Most plants were actively defended against intruding kelpfish. Kelpfish released after laboratory tagging (within 24 h), were repeatedly chased from their choices of plant cover by resident kelpfish (15/22 cases; see Stepien, 1986a). When kelpfish were released near the same plant they had been captured on, some approached already occupied plants (3/7 cases) and were chased. Kelpfish kept in the same STEPIEN: COLOR PATTERN AND HABITAT DIFFERENCES OF GIANT KELPFISH 53

(/) I >- "-W Cl Z w > (5 >- « Cl w >- () W ...J ...J o () (/) W «...J ::0 ...w en > (/) W «...J ...::0 o a: w III::0 ::> Z I o o o 0 0 0 o o o

o 0- (/) >- "C]() ~. « c >- >- '" iii .r= ~ « I "- '" z>- :5 ci. 0- "-Z o ii: "C" (/) I ~ ~ «>- ... ~ "-...J [IJ W « >:: I c W o >- ...J Z « N « ::0 ...J w ... ijj" "- o z .N « o w :: ·t};:~f::t:::::~%:~::::::. ~" «...J ::0 . '"N ... N o N a: w III::0 ::> Z 0 o o 0 0 0 o o

NUMBERS Of MALES VS. FEMALES MATCHING AND NOT MATCHING PLANT HABITATS 250

1,79 200 ~ Males i---- I I fEj Females I

Expected frequency ...... ~ 150 ;;:: ----- a. I I 'ii I ~ I -o Ci) 100 .D E ::l Z 8,37* 50 ......

r-----, ...... ' . I I I I ...... I •...... ,I ...- - . o I Not Matching Matching Habitat Color Habitat Color Figure 6, Numbers of adult males versus females in matching and not matching colors of plant habitats, Chi-square values indicate differences between numbers of males versus females, - - - = Expected frequency if numbers of males and females equal, per sex ratio of the population. * = Significant difference (0.05 level). N = 396, aquarium established and defended territories and sometimes injured other individuals by nipping at their caudal fins. Distributions of male and female kelpfish among species of plant habitats differed significantly (Fig, 5A). More females than males were collected in the brown alga M. pyrifera, in the red algae Gelidium nudifrons, Plocamium cartilagineum, and Pterocladia capillacea, as well as in the green surfgrass Phy!lospadix torreyi. Significantly more males than females were collected in the brown algae Sargassum spp., Cystoseira neglecta, and Zonaria (Laminaria) farlowii. Approximately equal numbers of males and females, according to their projected incidence in the population, were collected in the brown alga Eisenia arborea. Juvenile kelpfish were most frequently collected in the Macrocystis canopy (Fig. 4B). The second most common habitat was Phy!lospadix beds, followed by the brown algae Sargassum and Cystoseira. Juvenile males and females did not differ in distribution. In addition to differences in plant habitats, males and females varied in depth distribution (Fig. 5B). Females were more common than males in shallow waters STEPIEN: COLOR PATTERN AND HABITAT DIFFERENCES OF GIANT KELPFISH 55

Table 2. Seasonal variation in numbers offemale kelpfish matching versus not matching plant habitats (N = 229). Contingency table G-test (Seasonal variation in numbers matching versus nonmatching), x2 = 16.27, P = 0.001. Pearson's coefficient of contingency (Siegel, 1956) = 0.26

Spring Summer Fall Winter Total

Not matching 20 16 10 3 49 Matching 29 58 69 24 180 Totals 49 74 79 27 229

(0 to 8 m) as well as in deeper (13 to 25 m) waters. Male kelpfish were more common than females only in depths of 9 to 12 m. Significantly more females than males were collected on nonmatching plants (Fig. 6). Larger numbers of nonmatching females were collected in the spring and summer seasons (Table 2). Most males were closely associated with a given plant habitat which was actively defended against intruding con specifics and other fishes. Females were less frequently collected in plants than were males (Table 3), particularly during the spring spawning season (Table 4).

DISCUSSION Color Morphs and Sexual Dimorphism. -In the present study, giant kelpfish were found to be sexually dimorphic in color. Unlike adults, juveniles were not dimorphic. All red morphs collected were adult females, indicating that males and juveniles may not be capable of depositing large amounts of the red pigment astaxanthin. In situ caging experiments showed that although green and brown females slowly changed to red within 2 to 3 weeks after placement on red algae, neither adult males nor juveniles of either sex became red (Stepien, 1985; 1986a). Juveniles in laboratory and in situ experiments readily changed between green and brown colors, matching the color of background plants within 1 to 2 weeks. Almost all adult females were capable of changes between all three colors, in contrast to adult males, only a few of which assumed an olive brown-green color on green backgrounds (see Stepien, 1985; 1986a). These results suggest that few adult male kelpfish retain the ability to deposit large amounts of tunaxanthin. It appears probable that kelpfish coloration is influenced by sex hormones. It is not known whether other c1inid species exhibit sexually dimorphic color patterns, although Hubbs (1952) indicated that color variation was extensive in many species ofthe family and sexual dimorphism common. The spotted kelpfish, Gibbonsia elegans (Clinidae), also occurs in red, green, and brown morphs, which are not sexually dimorphic (Stepien, in press). Wilkie (1966) found no sexual differences between frequencies of red, green, and brown color morphs of the penpoint gunnel, Apodichthys jlavidus. Burgess did not investigate the possibility

Table 3. Differences between numbers of males versus females collected in given plants versus swimming through several plant areas (N = 396). Contingency table G-test (Sex differences in numbers in plants versus not in plants), x2 = 8.01,0.01 < P < 0.05. Pearson's coefficient of contingency (Siegel, 1956)=0.14

Sex In plants Not in plants Tolal Males 128 39 167 Females 145 84 229 Totals 273 123 396 56 BULLETIN OF MARINE SCIENCE, VOL. 4[, NO. I, [987

Table 4. Seasonal variations in kelpfish collected in given plants versus swimming through several plant areas (N = 396). Results of contingency table G-tests (for seasonal differences) are shown. Pearson's coefficient of contingency (Siegel, 1956) = 0.20 females, 0.01 males

Spring Summer Fall Winter Total Chi-Square Females Not in plants 26 28 21 9 84 In plants 23 46 58 18 145 Total 49 74 79 27 229 9.30 (0.01 < P < 0.05) Males Not in plants 7 12 II 9 39 In plants 22 47 44 15 128 Total 29 59 55 24 167 3.34 (N.S., P > 0.10)

of sexual dimorphism in his study of red, green, and brown color morphs of the kelp gunnel, Xererpesfucorum. Lindquist (1980) found the red phase of the browncheek blenny Acanthemblemaria crockeri was exhibited only by females in the central Gulf of California; males are black, although red individuals of both sexes were collected in submarine canyons located further south. Melanin Patterns and Sexual Dimorphism. - Kelpfish melanin patterns appear to function in intraspecific communication. Adult males and females display different melanin patterns, which flash or rapidly change during courtship and territorial displays. Melanin patterns also disrupt the color of the fish, aiding in their ability to blend in with plant backrounds. Results showing correlation of melanin pattern with habitat agree with those reported by Hubbs (1952). Melanin patterns of members of the genus Hypsoblennius similarly function in blending with background as well as in male courtship displays (Losey, 1976). Habitat Differences between Males and Females. - The majority of adult and juvenile color morphs were collected in plant habitats that closely matched the color of the fish. In laboratory and in situ plant color choice experiments, kelpfish consistently chose matching colors of plant habitats (Stepien, 1985; 1986a). Color matching appears to be, at least in part, an aid to hunting efficiency. Heterostichus is a camouflaged lying-in-wait predator of small fishes and crustaceans (Limbaugh, 1955; Coyer, 1979; Stepien, 1985). Behavioral experiments with color morphs of the spotted kelpfish, Gibbonsia elegans showed that matching the color of plant habitats also may aid kelpfish in avoiding detection by predators (Stepien, in press). Male and female giant kelpfish are found in different habitats. Females are more numerous among green and red plants, where most green and red morphs were collected in the present study. Males were more often collected than females only in the brown algae Sargassum, Cystoseira, and Zonaria, which are located in the mid-depth range. This mid-depth range was the most frequent location of kelp fish nests, which the males guard (Coyer, 1982; Stepien, 1985; 1986b). Although nests were sometimes laid in red algae, most of them were in mixed color habitats, where red algae were covered by taller brown ones (Stepien, 1985; 1986b). Males, blending in with the brown algae, guard the nests of eggs from predators until hatching (Coyer, 1979; Stepien, 1985; 1986b). Male ke1pfish may occur exclusively in the brown morph as an adaptation for nest guarding in the brown-dominated STEPIEN: COLOR PATTERN AND HABITAT DIFFERENCES OF GIANT KELPFISH 57 mid-depth zone. Females were more frequently found in shalIower and deeper habitats. A similar difference in depth distribution between the sexes has been described for a related c1inid, the spotted kelpfish G. elegans (WilIiams, 1954; Stepien, in press). The wide variety of colors exhibited by females apparently alIows them to occupy a wider range of plant habitats than males. Males may occur almost exclusively in the brown morph due to their nest guarding in brown-dominated areas. Green and red females are apparently adapted to blend in with green and red algae in shalIower habitats. Brown females were often collected in deeper waters, but are less common at the intermediate depths where the males nest. Color pattern differences between males and females may be a result of exclusion of females from male territories. Adult kelpfish are highly territorial and actively defend their home algae against conspecifics and other intruders. Kelpfish appeared to be evenly spaced and numerous in favorable habitats. It may thus be advantageous for some females to assume green or red colors, enabling them to occupy nonmale habitats, while retaining the advantages of camouflage. However, green surfgrass and red algae occupy much less seafloor and are smalIer in size than brown algae in southern California nearshore habitats. Thus, many kelpfish females are brown but live in other species of brown algae and at depths other than those used for nesting. In conclusion, sexual dimorphism is well developed in adult giant kelpfish, females differing from males in color and melanin pattern frequencies. These differences appear closely related to differences in plant habitats occupied by males and females. Some of these color variations, notably melanin pattern (which has been observed to playa role in courtship), may also function in sex recognition.

ACKNOWLEDGMENTS

Grants and funds supporting this research were generously provided by Sigma Xi, the Lerner Fund for Marine Science, the Theodore Roosevelt Memorial Scholarship Fund of the American Museum of Natural History, and the University of Southern California Biology Department. I greatly appreciate the research laboratory facilities which were provided gratis by the Catalina Marine Science Center and U.S.c.'s Institute for Marine and Coastal Studies Fish Harbor Research Laboratory. I especially thank those who helped me in collecting kelpfish: S. Naffziger, R. Moore, N. Jones, C. Winkler, D. Wilkie, B. Kulik, M. Carr, L. Craft, J. Sudick, R. Wright, and L. Allen. S. Azen and D. Perry gave statistical advice. R. Provin helped to draw and paste-up the figures. This manuscript benefitted substantially from critical reviews by B. Nafpaktitis, D. W. Wilkie, R. H. Rosenblatt, R. C. Brusca, B. C. Abbott, and G. J. Bakus.

LITERATURE CITED

ASTM. 1974. Standard method for visual evaluation of color differences of opaque materials. No. D 1729-69. ASTM, Philadelphia. 6 pp. --. 1980. Standard method of specifying color by the Munsell system. No. D 1535-80. ASTM, Philadelphia. 23 pp. Bagnara, J. T. and M. E. Hadley. 1973. Chromatophores and color change: a comparative physiology of animal pigmentation. Prenctice-Hall, Inc., New Jersey. 202 pp. Barlow, G. W. 1967. The functional significance of the split-head color pattern as exemplified in a leaf fish, Polycentrus schomburgkii. Ichthyologica 39: 57-70. Britton, G. 1983. The biochemistry ofnatura1 pigments. Cambridge University Press, London. 336 pp. Burgess, T. J. 1976. Seasonal intertidal distribution, high tide movements, substrate preferences, and color change capabilities of red and green colormorphs of Xererpesfucorum (Family: Pholidae), an intertidal fish from central California. Unpublished Master's thesis, Calif. State Univ., Ful- lerton. 114 pp. --. 1978. The comparative ecology of two sympatric polychromatic populations of Xererpes fucorum Jordan and Gilbert (Pisces: Pholidae) from the rocky intertidal zone of central California. J. Exp. Mar. BioI. Ecol. 35: 43-58. 58 BULLETINOFMARINESCIENCE.VOL.41. NO. I. 1987

Coyer, J. A. 1979. The invertebrate assemblage associated with Macrocystis pyrifera and its utilization as a food resource by kelp forest fishes. Ph.D. Dissertation, University of Southern California. Los Angeles. 314 pp. --. 1982. Observations on the reproductive behavior of the giant kelpfish, Heterostichus rostratus (Pisces: Clinidae). Copeia 1982: 344-350. Feder, H. M., C. H. Turner and C. Limbaugh. 1974. Observations on the fishes associated with kelp beds in southern California. Calif. Fish Bull. 160: 1-144. Fox, D. L. 1976. Animal biochromes and structural colors, 2nd ed. Univ. of Calif. Press, Los Angeles. 433 pp. Hubbs, C. 1952. A contribution to the classification of the Blennioid fishes of the family Clinidae, with a partial revision of the eastern Pacific forms. Stanford Ichth. Bull. 4: 41-165. Kelly, K. L. and D. B. Judd. 1976. Color: universal dictionary of names. U.S. Dept. Commerce, Washington, District of Columbia. 83 pp. Limbaugh, C. 1955. Fish life in the kelpbeds and the effects of kelp harvesting. Univ. Calif. lnst. Mar. Res. Ref. 55: 1-158. Lindquist, D. G. 1980. Aspects of the polychromatism in populations of the Gulf of California browncheek blenny, Acanthemblemaria crockeri (Blennioidea: Chaenopsidae). Copeia 1980: 137- 141. Losey, G. S., Jr. 1976. The significance of coloration in fishes of the genus Hypsoblennius Gill. Bull. Southern Calif. Acad. Sci. 75: 183-198. Munsell, A. H. 1946. A color notation. Munsell Co., Baltimore. 74 pp. Munsell Color Co. 1969. Munsell book of color, neighboring hues edition, matte finish collection. Munsell Color Co., Baltimore. ---. 1976. Munsell book of color, pocket edition. Munsell Color Co., Baltimore. Roedel, P. M. 1953. Common ocean fishes of the California coast. Cal. Fish. Bull. No. 91. 184 pp. Siegel, S. 1956. Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York. 312 pp. Sokal, R. R. and F. J. Rohlf. 1981. Biometry: the principle and practice of statistics in biological research, 2nd ed. W. H. Freeman and Co., San Francisco. 859 pp. Stepien, C. A. 1985. Life history, ecology, and regulation of color morphic patterns of the giant kelpfish, Heterostichus rostratus Girard. Ph.D. Dissertation, University of Southern California, Los Angeles. 318 pp. ---. 1986a. Regulation of the color morphic patterns of the giant kelpfish, Heterostichus rostratus: genetic versus environmental factors. J. Exp. Mar. BioI. Ecol. 100: 181-208. ---. 1986b. Life history and larval development of the giant kelpfish, Heterostichus rostratus. Fish. Bull. 84(4): 809-826. ---. In press. Regulation and significance of color morphic patterns of the spotted kelpfish Gibbonsia elegans Cooper (Blennioidei: Clinidae). Copeia 1988(1). Wilkie, D. W. 1966. Colour pigments in the penpoint gunnel Apodichthysjlavidus and their ecological significance. Unpublished Master's thesis, Univ. of British Columbia, Vancouver. 143 pp. Williams, G. C. 1954. Differential vertical distribution of the sexes in Gibbonsia elegans with remarks on two nominal subspecies of this fish. Copeia 1954: 267-273.

DATEACCEPTED: October 30, 1986.

ADDRESS: Marine Biology Research Division A-002. Scripps Institution of Oceanography. University of California at San Diego. La Jolla, California 92093.