Reproductive Behaviour of a Temperate Serranid ...

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REPRODUCTIVE BEHAVIOUR OF A TEMPERATE SERRANID FISH, Paralabrax clathratus (GIRARD), FROM SANTA CATALINA ISLAND, CALIFORNIA, U.S.A.

ERISMAN, B.E. AND L.G. ALLEN

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Journal of Fish Biology (2006) 68, 157–184 doi:10.1111/j.1095-8649.2005.00886.x, available online at http://www.blackwell-synergy.com

Reproductive behaviour of a temperate serranid fish, Paralabrax clathratus (Girard), from Santa Catalina Island, California, U.S.A. B. E. E R I S M A N*

AND

L. G. A L L E N †

Nearshore Marine Fish Research Program, Department of Biology, California State University, Northridge, CA 91330–8303, U.S.A. (Received 13 October 2004, Accepted 24 June 2005) The reproductive behaviour of the kelp bass Paralabrax clathratus was studied on Santa Catalina Island, California, U.S.A. from April 2000 to September 2002. Adults formed aggregations of three to > 200 individuals, and spawning occurred within subgroups of three to 23 individuals that contained a single female. The gonado-somatic index (IG) of collected ripe males (mean ¼ 5"8%, range ¼ 0"5–13"1%) indicated a large investment in sperm production that is common in group-spawning fishes characterized by intense sperm competition.

Spawning occurred 32 min before sunset to 120 min after sunset, and both males and females were capable of spawning multiple times during a single evening. Behavioural observations of adults and estimates of spawning periodicity from the collection of females with hydrated oocytes suggested that spawning occurred continuously throughout the summer months and showed no significant relationship with the lunar cycle. In general, the spawning behaviour of kelp bass was similar to other functionally gonochoric, group-spawning serranids. The dynamics of P. clathratus spawning aggregations, however, were inconsistent with that of tropical reef fish spawning aggregations, including the transient spawning aggregations of some tropical serranids. Aggregation spawning appeared to be an important component of # 2006 The Fisheries Society of the British Isles the annual reproduction of this species.

Key words: kelp forest fishes; mating systems; Paralabrax clathratus; Serranidae; spawning aggregations.

INTRODUCTION The Serranidae is a speciose family of fishes composed of three subfamilies and 449 species that are common inhabitants of nearshore tropical, subtropical and temperate waters worldwide (Nelson, 1994). Due to their considerable economic importance to fisheries and the overexploitation of stocks in many areas, the reproductive biology of many serranids is well documented (Moe, 1969; Fishelson, 1975; Shapiro, 1987; Sadovy et al., 1994a). Extensive research on this group of fishes has revealed that serranids exhibit a wide variety of sexual

†Author to whom correspondence should be addressed. Tel.: þ1 818 677 4037; fax: þ1 818 677 2034; email: larry.allen@csun.edu *Present address: Marine Biology Research Division, Scripps Institution of Oceanography, 9500 Gilman Drive, Mail Code 0208, La Jolla, CA, 92093-0208, U.S.A.

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patterns, social structures, spatial and temporal spawning patterns, and mating systems (Smith, 1965; Popper & Fishelson, 1973; Shapiro, 1981; Fischer & Petersen, 1987; Colin, 1992; Samoilys & Squire, 1994; Sadovy & Colin, 1995).

Most of the information on the mating systems and behavioural patterns of serranids is derived from studies of tropical species (Thresher, 1984; Colin et al., 1987; Shapiro, 1987; Donaldson, 1995), and the reproductive behaviours of temperate representatives are poorly understood, although some information does exist (Lavenda, 1949; Limbaugh, 1955; Quast, 1968a).

The genus Paralabrax, which is placed within the subfamily Serraninae, is composed of nine species of mesocarnivorous fishes common on the nearshore reefs of the eastern Pacific and western Atlantic Oceans. Protogyny and gonochorism have been reported among species of Paralabrax, and isolated populations of Paralabrax maculatofasciatus (Steindachner) may exhibit both sexual patterns (Smith & Young, 1966; Bo´rquez et al., 1988; Hastings, 1989; Hovey & Allen, 2000; Baca-Hovey et al., 2002). Sadovy & Domeier (2005) argued that P. maculatofasciatus is functionally gonochoric. Brief descriptions of general behaviour have been reported for a few species of Paralabrax (Limbaugh, 1955; Quast, 1968a, b; Turner et al., 1969; Feder et al., 1974), and voluntary spawning in captive P. maculatofasciatus was observed by Martı´ nez-Diaz et al. (2001). The mating systems and reproductive behaviours of any species of Paralabrax, however, have not been investigated thoroughly, and spawning has not been described from field observations.

The kelp bass Paralabrax clathratus (Girard), is a common nearshore reef fish of both the southern California mainland and the surrounding Channel Islands (Young, 1963; Quast, 1968a, b; Miller & Lea, 1972; Love et al., 1996a).

Historically, the species has been extremely important to local fisheries, however, intense fishing pressure following World War II led to major population declines and their eventual removal from commercial markets (Young, 1963). Kelp bass have remained an important component of recreational fisheries, where they have consistently ranked among the top three species landed annually by commercial passenger fishing vessels (CPFV) and private anglers of southern California over several recent decades (Collyer & Young, 1953; Oliphant, 1993; Love et al., 1996a). Annual sport and recreational landings of P. clathratus in southern California may reach 1 700 000 individuals (Allen & Hovey, 2001) in some years.

The continuing importance of kelp bass to local fisheries has stimulated a multitude of research projects on various aspects of their life history, including factors related to reproduction. Males and females mature at 22–27 cm total length (LT) and 2–5 years, grow to at least 72 cm LT, and live up to 33 years (Love et al., 1996b). Smith & Young (1966) classified P. clathratus as functionally gonochoric due to a lack of histological evidence of sex change and no differences in the size ranges of males and females. A recent study by Sadovy & Domeier (2005) reached a similar conclusion and found that individuals pass through a bisexual juvenile stage before becoming sexually mature.

Spawning in P. clathratus occurs from late spring to early autumn when adults form large aggregations along kelp beds, rock reefs and insular shelves (Limbaugh, 1955; Smith & Young, 1966; Quast, 1968a; Turner et al., 1969).

Histological sectioning by Oda et al. (1993) estimated that females spawn, on average, every 2"5 days, with larger females capable of daily spawning. #

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Backcalculated spawn dates from both newly settled larvae and young-of-year individuals indicated a semi-lunar pattern of spawning around new and full moons (Cordes & Allen, 1997; Findlay & Allen, 2002). Histological examinations and age classification of post-ovulatory follicles from ripe females suggest that spawning occurs during the late afternoon and evening hours (Oda et al., 1993), although the diel spawning period of P. clathratus has never been confirmed by direct observations. Adult kelp bass are sexually dichromatic during the spawning season, where most ripe males have bright orange snouts, and both males and females adopt conspicuous colour patterns during courtship and spawning (Erisman & Allen, 2005).

Knowledge of the behavioural patterns and characteristics of spawning aggregations is important to fully understand the function of group spawning in a species (Shapiro et al., 1993). This knowledge also is crucial to the implementation of proper management strategies for conserving economically important fishes like P. clathratus, whose spawning aggregations are heavily exploited by fishers (Sadovy, 1994; Coleman et al., 1996; Sadovy & Eklund, 1999; Koenig et al., 2000). Studies on many tropical serranids have demonstrated that heavy fishing pressure on spawning aggregations can have detrimental effects such as rapid and significant population declines, less intense courtship and spawning activity, reduced fertilization, loss of genetic diversity, dramatic shifts in size and sex composition and the complete disappearance of the aggregations (Olsen & LaPlace, 1979; Smith et al., 1991; Colin, 1992; Shapiro et al., 1993; Sadovy, 1994; Bohnsack, 1996; Beets & Friedlander, 1998; Johannes et al., 1999).

The recreational fishery for P. clathratus was previously considered to be sustainable, however, dramatic declines in recreational landings have occurred since the late 1980s when peak landings were recorded (Allen & Hovey, 2001).

Similarly, population declines in both adult abundances and larval production have been noted in some areas (Pondella et al., 2002; Stephens & Pondella, 2002). Although the decrease in P. clathratus populations may indicate longterm regional declines associated with a climatic regime shift (Brooks et al., 2002), these declines are probably affected by over-fishing of adult breeding aggregations, which are a primary target of anglers during the summer months.

By studying the mating system and spawning behaviour of P. clathratus, the potential effects of heavy fishing pressure on their populations may be assessed and better management strategies for conserving their stocks created.

The purpose of the present study was to describe several aspects of the reproductive behaviour of P. clathratus from Santa Catalina Island, California, U.S.A. Specific objectives of the project were to: 1) describe courtship and spawning behaviours of adults, 2) characterize the mating system (pair v. group spawning) of adults and 3) estimate temporal spawning patterns including spawning seasonality, diel spawning period, spawning frequency and spawning periodicity.

MATERIALS AND METHODS COLLECTION OF SPECIMENS Eight hundred and twenty-five individuals (365 males, 397 females and 63 juveniles) were collected by hook and line from May 2001 to April 2002 at several

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sites along the coast of Santa Catalina Island, California (33$ 260 N, 118$ 290 W) (Fig. 1). The handling, collection and sacrifice of all individuals used in this study followed the American Fisheries Society (AFS, 2004). Collections were made on a monthly basis during the non-spawning season and daily during the spawning season.

The time, lunar phase and date of collection were recorded for each individual.

Standard length (LS) of each individual was recorded to the nearest mm, and total body mass (MT) was recorded, to the nearest g. Gonads were removed from all collected individuals, and wet masses of gonads (MG) were recorded to the nearest 0"5 g. The gonado-somatic index (IG) of each individual was calculated according to the formula: IG ¼ 100MG(MT % MG)%1.

Macroscopic inspections of gonads were used to determine sex and maturity stages of individuals (Table I) (Hunter & Macewicz, 1985; DeMartini, 1987). Maturity stages (gonad development stages) were classified as: immature, inactive, ripe or hydrated (females only). When the determination of sex was uncertain (i.e. mature, inactive individuals), portions of gonad tissue were stained with aceto-carmine, squashed and observed under a dissecting microscope using magnifications of &25 to &200 to determine sex (Guerrero, 1974).

118°30′ W

LONG BEACH

SAN PEDRO

CA

NEWPORT BEACH

IA RN FO

LI

N

LION HEAD BIRD ROCK

33°30′ N

BLUE CAVERN

SA

10 km

N

TA

CATALINA HARBOR CA

WRIGLEY MARINE SCIENCE CENTER

TWO HARBORS

Intake Pipes Pumpernickel Cove

TA

Blue Cavern

LI

N

Habitat Reef

A

IS

.

Net Pen Reserve Boundary

FIG. 1. Map of Santa Catalina Island, California, U.S.A., showing study sites and proximity to the southern California mainland. Behavioural observations were conducted at several sites inside (Habitat Reef, Intake Pipes, Pumpernickel Cove) and outside (Bird Rock, Blue Caverns) the ‘no-take’ marine reserve adjacent to the University of Southern California Wrigley Marine Science Center. The captivity study was conducted at the net-pen site, located on the south-west region of Catalina Harbor.

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TABLE I. Maturity stages and macroscopic descriptions of gonads of Paralabrax clathratus Maturity stage

Macroscopic description

Immature Mature,

Mature, Mature, Mature,

Mature,

Small, thin, thread-like tissue; no visible oocytes or milt; transparent, pink or cream in colour; sex undetermined inactive male Testes relatively small, but larger and more rounded than immature gonads; greyish in colour; thickened gonad wall; small volume of milt present in some individuals; often indistinguishable from mature, inactive females and require microscopic validation ripe male Testes large and milt clearly visible; milt release with abdominal pressure inactive female Similar and often indistinguishable from mature, inactive males; require microscopic validation ripe female Ovaries large and yellow to white with transparent gonad wall; large vitellogenic oocytes are tightly packed and clearly visible hydrated female Ovaries large with thin, transparent gonad wall; oocytes large with water and visible yolk; egg release possible with abdominal pressure

BE H A V I O U R A L P A T T E R N S Observations were conducted at several locations on Santa Catalina Island, California at depths of 1–24 m. In situ observations were made at four sites within a no-take marine reserve (Habitat Reef, Intake Pipes, Pumpernickel Cove and Blue Caverns) located in the waters adjacent to the University of Southern California Wrigley Marine Science Center and at one site (Bird Rock) located outside the reserve boundary (Fig. 1). Observations were made on a monthly basis during the non-spawning season and daily during summer months when spawning occurred. Although observations were made throughout the day during the spawning season, the majority of observations were conducted from c. 1"5 h before sunset until light levels became too low to accurately describe behaviours.

Observation periods ranged from 30–80 min per dive. Approximately 450 h of behavioural observations were made while scuba diving or snorkelling from April 2000 to September 2002. Observations were recorded on plastic slates and digital video recordings were used and analysed for more detailed descriptions of behaviours.

Behaviours were identified initially based on their similarity to those described from other serranids (Popper & Fishelson, 1973; Fischer, 1980; Thresher, 1984; Hastings & Petersen, 1986; Colin et al., 1987; Petersen, 1990; Colin, 1992; Gilmore & Jones, 1992; Sadovy et al., 1994b; Samoilys & Squire, 1994; Donaldson, 1995; Domeier & Colin, 1997; Zabala et al., 1997; Deloach, 1999). Novel behaviours were defined precisely and catalogued to represent the repertoire of spawning behaviours (Martin & Bateson, 1993; Lehner, 1996). Specific colour patterns were used often to differentiate among males and females during the spawning season (Erisman & Allen, 2005).

The short time period of available light in which to observe spawning while scuba diving at the typical 10–20 m depth, when coupled with the highly mobile nature of spawning groups made it difficult to collect behavioural data in the field on a reliable basis. To collect more precise data on specific behaviours, 108 adults (50 males and 58 females) were captured from 20 June to 23 June 2002 and placed in a 700 m3 outdoor, floating net-pen located in Catalina Harbor (Fig. 1). Aggregation size and sex ratio were determined from previous studies (Limbaugh, 1955; Quast, 1968a; Feder et al., 1974),

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individuals collected in 2001, and from observations conducted by scuba diving during 2001 and 2002. Captive individuals were observed on a daily basis from 7 July to 14 August 2003 while scuba diving or snorkelling at depths of 0–8 m in order to identify specific spawning behaviours and estimate temporal patterns.

MATING SYSTEM The mating system of adults was determined from observations of spawning behaviour in wild and captive individuals on Santa Catalina Island, California. The IG of 193 ripe males collected from June to August 2001 and 50 ripe males from the captive study provided additional evidence of the mating system. The IG of these males were compared to known values of group-spawning and pair-spawning fishes, including other serranids, which were then used to predict the mating system in P. clathratus (Warner, 1984; Sadovy & Colin, 1995; Stockley et al., 1997; Petersen & Warner, 1998; Taborsky, 1998).

TEMPORAL SPAWNING PATTERNS Changes in the mean monthly IG of collected adults were used in conjunction with visual determinations of gonad maturity states of adults to estimate the annual spawning season (Quast, 1968a; Sadovy et al., 1994a; Rhodes & Sadovy, 2002). Direct observations of spawning, the presence of hydrated oocytes, and changes in the mean IG in 255 mature, ripe females collected from June to September 2001 at Santa Catalina Island were used to estimate spawning periodicity. Females with swollen ovaries containing eggs enlarged with water and having clear yolks were classified as hydrated (Table I). In P. clathratus, the final stages of oocyte maturation occur in the follicle and hydrated oocytes are stored in the ovaries for up to 15 h before spawning (Smith & Young, 1966; Oda et al., 1993), thus making the presence of hydrated oocytes in ovaries a reliable indicator of imminent spawning. Dates on which hydrated females were collected were used as daily markers of spawning, and these data were organized chronologically over the spawning season of 2001 in order to determine any clear patterns in spawning periodicity. The proportion of hydrated females collected among the four primary lunar phases (i.e. full, last quarter, new and first quarter) were used to assess the influence of the lunar cycle on spawning periodicity by applying the Pearson w2 goodness of fit test.

Changes in the IG of hydrated females during the spawning season of 2001 were also used to determine spawning periodicity. Data were grouped by lunar phase and differences in median IG among the four primary lunar phases and over several lunar cycles from June to September 2001 were analysed by applying the Kruskal-Wallis test.

Observations of spawning of wild and captive individuals were used to estimate the diel spawning period, with the time of onset of spawning rushes being recorded to the nearest minute. The time of first spawning was documented in captive individuals on 17 evenings between 13 July and 15 August 2003, and this time was compared to the time of sunset using Spearman’s coefficient of rank correlation (rS). Spawning continued well past dark, thus making it difficult to determine when spawning ceased from direct observations. During seven observation periods in the captive study, eggs were collected from the surface of the net-pen at 10 min intervals. The end of the diel spawning period was estimated from the time at which no more eggs were collected from the surface.

Data on the spawning frequency of captive individuals were collected on seven observation periods from 16 July to 14 August 2002. One observer would snorkel at the surface of the pen and monitor behaviour. When spawning occurred, the observer raised his hand, at which point a recorder noted the time of spawning to the nearest min.

Spawning frequency was determined only when the visibility of the water exceeded the boundaries of the pen, so that an accurate count of all spawns within the pen could be obtained.

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RESULTS COLLECTED SPECIMENS

Immature individuals ranged in size from 135–233 mm LS. The size range of males (165–397 mm LS) and females (172–437 mm LS) were similar (Fig. 2), however, the mean LS of males (265 mm) was slightly smaller than the mean LS of females (274 mm). Although the mean LS of both males and females differed significantly among months sampled (two-way ANOVA, F8,306, P < 0"001), there was no significant difference with respect to sex (two-way ANOVA, F1,306, P ¼ 0"095). The interaction between sex and month was also not significant (two-way ANOVA, F8,306, P ¼ 0"578).

ANNUAL SPAWNING SEASON

Mean monthly IG of males and females remained low from January to April (Fig. 3). The IG of both sexes increased from April to June, peaked in June, and steadily declined throughout the summer and autumn. The IG of males and females were lowest in February and December. Monthly variations in male IG (Kruskal-Wallis, P < 0"01) and female IG (Kruskal-Wallis, P < 0"01) were significant. Males and females containing visibly ripe gonadal tissue were collected from late May to early October and >93% of adults collected from June to August were visibly ripe. Females with hydrated oocytes were collected from June to early September, and the highest frequency of hydrated females occurred in July. Spawning events were observed from June to August in both wild and

50 45 40

Number

35 30 25 20 15 10 5 0

130

150

170

190

210

230

250

270 290 LS (mm)

310

330

350

370

390

410

430

FIG. 2. Sample distribution of 63 immature (6), 365 male (&) and 397 female (&) kelp bass collected from May 2001 to April 2002, showing the number of individuals from each sex represented among standard length classes.

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12 52 (82) 10 93 (101)

IG

8

48 (53)

6

29 (23) 21 (20)

4

45 (26)

35 (45) 2 0 (0) 0

18 (21)

24 (26)

Jan

0 (0) Feb

Mar

0 (0) Apr

May

Jun

Jul

Aug

Sep

Oct

Nov

Dec

Month

FIG. 3. Mean ( S.D. monthly gonado-somatic index of 365 male and 397 female kelp bass. Numbers above error bars are monthly sample sizes (n); female n are in parentheses. Data are organized to show variations over a single year.

captive individuals. Although spawning may occur from May to October, spawning activity probably peaks from June to August.

G E N E R A L B E H A V I O U R P A T T ER N S

Observed behaviours are summarized in Table II. In the open ocean, adults aggregated under dense kelp canopies, around kelp fronds located on shelf edges or reef slopes, above rocky substrata and in the open water. Aggregations, however formed also around man-made structures such as piers and harbour breakwalls. Aggregations varied considerably in abundance from three to >200 individuals. Aggregations were most common at depth ranges of 8–18 m and were positioned on the reef from the bottom to >20 m above the bottom of the reef. Large aggregations, however, were observed in open water at distances >10 m off the reef. This was most notable at the Bird Rock site, where c. 200 adults aggregated c. 5–15 m off the edge of the reef at depths of 10–20 m over a bottom depth of 30 m.

Aggregations of '50 individuals were observed at field sites throughout the year and were not limited to specific time periods. Aggregations were commonly associated with group-feeding events, where adults aggregated in close proximity to and preyed upon schooling fishes such as Trachurus symmetricus (Ayres), Sardinops sagax (Jenyns) and Engraulis mordax Girard. In April 2002, a dense aggregation of c. 100 adults was observed under the pier at the Wrigley Marine #

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Head turning

Head to head display

Hover

Rolling display

Lateral display

Female display

Sub-grouping

Schooling

Aggregating

Behaviour

Description

Individuals gather in loose to dense groups; vary in abundance from three to >200 individuals; common throughout the year.

Spawning season Adults form dense, polarized groups of up to 150 individuals; characterized by rapid, uniform movement along the reef; observed only during afternoon and evenings during the spawning season.

Courtship Groups of three to >23 individuals that separate from larger aggregations or schools during courtship periods; often move away from larger aggregations towards open water; spawning occurs within these groups.

Courtship A gravid female hovers motionless in the water column or adjacent to the substrata, using a fanning motion of the pectoral and caudal fins to maintain position; body is relatively straight with the head angled upwards at 20–60$ ; ventral region of female is white and distended.

Courtship aggression During courtship, a male positions his body perpendicular in front of a female and he hovers in position for several seconds; the male’s head is pointed slightly upwards and his dorsal fin is completely extended; observed also during aggressive encounters.

Courtship aggression A male pauses in front of and perpendicular to a female and rolls slowly back and forth from side to side with his dorsal fin extended; the male may execute this while oriented horizontally or with his head pointed upward at an angle; also observed during aggressive encounters.

Courtship A courting male hovers in close proximity to a female; common in subgroups during courtship.

Courtship A male approaches a female head-on with his dorsal fin completely extended and pauses near the female; often followed by head turning.

Courtship During head to head displays, the female turns her head away from the male in a single motion; the male turns his head with the female and re-establishes the head to head position; during courtship, the male and female may engage in several head turning bouts.

Year-round

Occurrence

TABLE II. Occurrences and descriptions of observed behaviours in adult Paralabrax clathratus REPRODUCTIVE BEHAVIOUR OF PARALABRAX CLATHRATUS

165

#

Male colour change

Female colour change

Female pause

Darting

Mobbing

Courtship chase

Following

Bumping

Nipping

Rubbing

Behaviour

Description

A male approaches a gravid female from the side or from underneath; the snout, operculum and dorsal portion of the male’s body makes physical contact with the lower abdomen of the female as he swims past.

Courtship aggression One individual will nip or bite the posterior flank or caudal region of another individual; often occurs during courtship chase and aggressive chase events; during courtship, male nipping behaviour is often followed by female darting behaviour.

Courtship aggression The snout or operculum of a male makes physical contact with the lower abdomen of the female for several seconds; sometimes results in displacing the location and orientation of the female; occurs also among individuals involved in aggressive encounters.

Courtship One to several males swims behind a gravid female, without making physical contact with the female; common during early courtship periods.

Courtship One to several males swims rapidly after a gravid female that is also swimming rapidly; often occurs before and after mobbing events.

Courtship spawning Several males swim along side a gravid female while maintaining a close distance to the female and usually making physical contact with the female; common during late courtship periods and directly precedes a spawning rush; usually associated with bumping, nipping, darting and chasing behaviours.

Courtship A female swims in an erratic manner, constantly changing directions while swimming away rapidly from chasing males; in some cases, the female turns 180$ and burst swims away from pursuing males.

Spawning A gravid female that is being mobbed and chased by courting males, stops for several seconds before initiating a spawning event; can vary in duration from c. 5 –15 s; directly precedes tilting behaviour.

Courtship The dorsal portion of the female turns dark grey to black with the spots becoming less distinct; the side and underside of the female become white; observed in most females during the spawning period.

Courtship Males turn a charcoal body colour with four to five black bars overlaying white spots; seasonal orange-snout colouration present; observed in males during the spawning period.

Courtship

Occurrence

TABLE II. Continued

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Spawning

Spawning

Aggression Aggression

Aggression Aggression Aggression Aggression

Aggression

Aggression

Rolling rise

Spawning rush

Dorsal flare Gaping

Parallel hover Parallel flare Aggressive chase Fleeing

Spiralling

Face-off

Aggressive colour change Aggression

Spawning

Tilting

Follows female display; the female lowers her head to be horizontal or turned slightly downwards and begins to scull rapidly with her pectoral fins; directly precedes rolling rise behaviour during spawning events.

The female rolls slightly (5"10$ ) on her side while rising slowly upwards using pectoral and caudal fin motion; a horizontal orientation is maintained during the rise of 20"40 cm; directly follows tilting behaviour; followed by mobbing and spawning rush.

A gravid female and several males swim rapidly in a straight line for c. 1 to 5 m while tightly clustered together and oriented in the same manner; rushes vary in direction from vertical (most common) to horizontal (rare); the female is located in the centre of the group, with males surrounding her on all sides as well as behind her; males orient themselves so that their vents are closest to that of the female; this creates a cylindrical shape, with males positioned all around the female, with some males swimming in an inverted orientation; rushes end with males and females releasing gametes synchronously into the water column and the group separating rapidly; immediately follows rolling rise and mobbing behaviour.

An individual raises its dorsal fin completely when approached by another individual.

An individual opens its mouth completely agape and holds it open for several seconds; often associated with flaring and face-off behaviour.

Two individuals hover or rest in a parallel orientation; often occurs between face-offs.

Two individuals hover or rest in a parallel orientation, with their dorsal fins erect.

One individual rapidly swimming directly behind another individual that is fleeing.

One individual swimming rapidly in front of and away from another individual that is chasing.

Two individuals involved in an agonistic bout, move in a spiralling motion around one another. Usually associated with ramming and nipping behaviour.

Two individuals that are facing each other, rise up in the water column while performing gaping and flaring behaviour; individuals will often bite or lock their jaws together for brief periods.

The body colour of an individual will turn dark green or black, with large, amorphous blotches covering the head and body; this colour fades immediately after an agonistic encounter.

REPRODUCTIVE BEHAVIOUR OF PARALABRAX CLATHRATUS

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Science Center on Santa Catalina Island, and it persisted for c. 1 week. Most of the individuals of the aggregation had visibly swollen abdomens, and the collection and examination of several individuals revealed large quantities of the atherinid fish, Leuresthes tenuis (Ayres), within their guts.

Similar to observations made by Hobson & Chess (2001), large adult kelp bass (>300 mm LS) were rare on Santa Catalina Island at all sites outside the reserve, and this is probably due to intensive fishing exerted over many years by the recreational fishing industry. Although large adults were more common within the reserve sites, there was no obvious difference in the number of individuals among aggregations inside and outside the reserve, as both small (<10 individuals) and large aggregations (>100 individuals) were observed at all sites.

There were no obvious differences in size, location or timing among spawning and non-spawning aggregations, and the identification of courtship or spawning behaviours (i.e. mobbing and spawning rushes) (Table II) within an aggregation was the only reliable characteristic distinguishing spawning aggregations from non-spawning aggregations. Both spawning and non-spawning aggregations appeared to be spatially and temporally unpredictable. During observations, it was not uncommon for large aggregations of adults to be present for one to several days, only to disappear from the area completely during later observations. During one observation period, a large aggregation was observed swimming actively along the reef for several hundred metres before moving off the site completely.

MATING SYSTEM AND SPAWNING BEHAVIOUR

Approximately 250 spawning events were recorded from 2000 to 2002.

Spawning occurred in single female, multi-male groups in both the field and captive studies. Mobbing and other behaviours common in group-spawning fishes were observed at all field sites from June to August of 2001 and 2002.

Thirteen spawning events were recorded at field sites during five observation periods in 2001 (Intake Pipes: 15 June, 16 June and 23 July; Blue Caverns: 12 July; Bird Rock: 31 July) and two observation periods in 2002 (Intake Pipes: 26 June; Bird Rock: 27 June). Spawning in wild individuals occurred in groups of five to 16 individuals within larger aggregations, and pair spawning was never observed. Spawning in captive individuals ranged from three to 23 individuals, however, spawning events typically involved seven to 15 individuals. A spawning group of three individuals (one female and two males) was observed once in captivity. Thirty-two wild spawning events occurring outside the net-pens in Catalina Harbor were recorded over 18 observation periods during the captivity study, and spawning groups ranged from six to 20 individuals. Pair spawning was not observed in captive individuals or in spawning events occurring outside the net-pens. The IG of ripe males collected from June to August 2001 ranged from 0"5â&#x20AC;&#x201C;13"1, and mean male IG was 5"8 (Fig. 4). The IG of males from the captive study was 2"39 to 10"06, and mean IG was 6"21 (Fig. 4). Although IG varied within size classes, large IG values were present throughout the size ranges of both collected and captive males.

Courtship and spawning behaviour were not observed during the morning and afternoon periods and appeared to be restricted to the evening hours. #

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14 12 10

IG

8 6 4 2 0 150

200

250

300 LS (mm)

350

400

FIG. 4. Gonado-somatic index of 193 ripe male kelp bass collected from June to August 2001 (^) and 50 ripe males from the captivity study of 2002 (&).

Aggregations were common throughout the day and schooling behaviour of breeding adults began as early as 2"5 h before sunset. Approximately 30â&#x20AC;&#x201C;50 min before sunset, adult males became increasingly active and began visiting and courting females. In the field, groups of males in the checkered colour phase (male courtship phase; Erisman & Allen, 2005) were consistently observed swimming in the water column and visiting gravid females that were positioned on or near the substratum (i.e. kelp or rock). In captivity, males often swam rapidly around the pen, and they visited and courted several females for periods of 20 s to several minutes. During early courtship, male behaviour consisted of one or a combination of the following patterns: following, lateral display, rolling display, hover, head to head display, head turning and rubbing. The most common sequence of male courtship consisted of a male in checkered colour phase approaching a female, performing various display behaviours for several seconds, then swimming to the side of the female and hovering nearby for several minutes before approaching again. In some cases, males would approach females from the side or from behind and perform bumping and nudging behaviours before displaying to the female. If the female swam away, males followed or approached another female.

Gravid females were identified by their white, highly distended bellies and by their distinct behaviours. During the early courtship period, gravid females were less active than males, and they usually hovered in close proximity to the kelp or perched on rocks. Females were intermittently active for brief periods when displaying to nearby males. Female display behaviours began with a female rising slowly away from the kelp or bottom by rapidly fanning their pectoral fins and maintaining a slight head-up posture. The white, distended bellies of gravid females were especially conspicuous at this time. One or more males

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responded to female display behaviours by visiting and executing various courtship patterns (i.e. following, bumping, and mobbing). After brief displays, females retreated into the substratum and were often pursued and mobbed by courting males. Female courtship colouration (dark phase; Erisman & Allen, 2005) was not observed during the early courtship period.

As the courtship period progressed, subgroups consisting of three to '20 individuals within aggregations formed around gravid females. During this time, males exhibited the checkered colour phase and some gravid females exhibited the dark phase. Repeated bouts of courtship and display behaviour occurred within subgroups prior to spawning events and consisted of a combination of the following behaviours: rubbing, bumping, chasing, mobbing, nipping and darting. Rubbing and bumping behaviour became more frequent and intense as the spawning period approached. Courting males often physically displaced females at this time. In the field, spawning females were located sometimes by a dense group of males swimming in a frenzied manner around a kelp head, mobbing and bumping a solitary individual that was perched deep inside the kelp. During one observation period of captive fish, two males moved a female away from the side of the net by applying steady pressure against her abdomen with their snouts. The female was then turned on her side and elevated from a horizontal position to a completely vertical position. The female remained in this position for c. 10 s before swimming away, with courting males chasing her.

Courtship bouts leading to spawning rushes varied in duration from 15 s to several minutes. Early spawns were usually preceded by extended courtship consisting of repeated mobbing, darting and chasing events, whereas during peak spawning periods spawning often occurred after a single, brief mobbing event.

During the peak spawning period, males courted unresponsive females only briefly before swimming away to court other females or to join other subgroups.

Several different types of spawning rushes (Table II) were observed. The most common pattern began with the gravid female in dark colour phase showing female display behaviour (Fig. 5) surrounded by several courting males. Female display behaviour was followed by tilting and rolling rise behaviour. Briefly, the female lowered her head (tilting) and began to scull rapidly with her pectoral fins. Then, the female rolled slightly onto her side while rising slightly upwards (rolling rise), using pectoral sculling and maintaining a horizontal position. A brief mobbing bout and a subsequent vertical spawning rush of 1–4 m immediately followed, and spawning ended with gamete release by the female and the participating males (Fig. 5). Following gamete release, the female quickly swam downward towards the kelp or substratum. Males swam away in random directions and often participated in newly formed spawning groups. The second most common pattern occurred in closer relation to male mobbing behaviour and was common during the peak spawning period. In this case, subgroups formed quickly into mobbing groups and male courtship behaviour did not occur. A brief female pause behaviour (2–5 s) followed single mobbing and chasing events by males, and in turn led to an immediate spawning rush. This pause appeared to allow pursuing males just enough time to regain physical contact with the female before the spawning rush ensued. Sometimes during the peak spawning period, the typical pause and lateral rise behaviours of the female, usually seen

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FIG. 5. Spawning sequence of kelp bass showing several males surrounding a gravid female, which is positioned with her head pointing slightly upward. The female lowers her head and rises slowly in the water column while maintaining a horizontal orientation. Males quickly rush toward the female from all directions, forming a dense mob around her as she continues to rise. The female raises her head and leads the group into a quick vertical rush. During the spawning rush, males maintain body contact with the female and orient themselves to align their vents with that of the female. The spawning rush ends with the female and males releasing gametes followed by the quick separation of the group.

individually or together, did not occur at all, and mobbing and chasing events led directly into spawning rushes.

The angle of ascent in spawning rushes also showed a great deal of variation from long, vertical rushes of several metres to quick, horizontal bursts of )1 m.

Some rushes resulted in ‘false starts’ (Fischer, 1984; Deloach, 1999), where the female initiated a spawning rush and then quickly darted downward, away from the group just prior to gamete release. A few males often released their gametes during ‘false starts’, but gamete clouds were notably smaller. The courtship and spawning behaviour of adult males did not differ among males of different size classes. Rather, both large and small males participated in group-spawning events and spawning groups often included males of mixed size classes. #

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No obvious differences in the spawning behaviours of adult P. clathratus were observed among spawning aggregations at sites located inside and outside the marine reserve. Similarly, the types of spawning behaviours observed in the field were very similar to those observed in captive individuals, although some differences were noted. At field sites, subgroups often swam considerable distances in >10 m away from the larger aggregation during courtship and spawning periods.

Subgroups often swam several metres over open water before returning to the reef several minutes later, presumably after spawning was completed. Other spawns were observed in closer proximity to the kelp canopy. Subgroups would form within aggregations located under the kelp canopy, and they would swim to the top of or above the canopy for brief periods to perform spawning rushes.

Although subgroup formation also occurred in captive individuals, spawning groups were more clustered, probably due to the confined space of the pen. A second difference, also probably due to the location of the nets, was the depth range at which spawning occurred. During mobbing and spawning events in the field, subgroups often covered large vertical and horizontal distances, with spawning rushes commencing at 10–15 m and gamete release occurring at 5 m in depth. Movement in captive individuals was limited in both horizontal and vertical dimensions. Spawning groups would form anywhere from 2–5 m below the surface, and gamete release often occurred just below the surface. In many cases, spawning groups would actually splash at the surface.

Adults showed little evidence of territoriality, as intraspecific bouts of aggression were rare during both spawning and non-spawning periods (Table II), and individuals did not occupy specific areas of the reef nor guard certain areas from conspecifics. Interactions were usually brief and occurred over a period of 3–5 s.

During the non-spawning season, aggressive interactions among adults were observed at an estimated frequency of <0"2 bouts h%1 of observation. Males did not defend females from other males, and bouts of conspicuous aggressive behaviour among courting males were observed only twice in the field and four times in the captive aggregation. Inter-female aggression and male – female aggressive behaviour was not observed during courtship periods.

Aggressive bouts occurred usually as follows: one individual approached a stationary individual and bumped or nipped the posterior region of the stationary individual, thus causing the stationary individual to flee several metres away.

Other interactions consisted of various display behaviours exhibited by one or both participants; these included lateral display, rolling display, fin flaring, parallel rest, reverse rest and ended with one or both individuals swimming slowly away. Individuals sometimes changed body colour from the ‘calico’ to the ‘marbled’ phase (Erisman & Allen, 2005) during aggressive encounters. On rare occasions, individuals would engage in intense bouts that lasted from 10 s to several minutes. These bouts generally began with a slow, simultaneous approach by both individuals, usually of similar size, followed by face-off behaviour. Face-offs often lasted several seconds and ended when the two individuals locked jaws and separated quickly afterwards. Spiralling behaviour was also observed in prolonged aggressive encounters. Between face-offs and spiralling events, the two combatants sometimes settled down to the reef in a parallel rest or reverse rest for several seconds to minutes and exhibited various

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display behaviours. The longest observed agonistic bout lasted c. 4 min and consisted of repeated aggressive displays, face-offs, and spiralling events.

SP A WN IN G P E R I O D IC I T Y

Hydrated females were collected continuously from June to September 2001 and were collected during all sampled lunar phases where more than five individuals were represented (Fig. 6). When data were pooled for lunar phase, there was no significant difference in the frequency of hydrated females (Pearson w2, d.f. ¼ 3, P ¼ 0"310) or the median IG of hydrated females (one-way ANOVA, F3,31, P ¼ 0"60) among the four primary lunar phases. In addition, the median IG of hydrated females was not significantly different among lunar phases from several lunar cycles during the spawning season of 2001 (Kruskal-Wallis test, P ¼ 0"22) (Fig. 6).

Spawning behaviour was observed in the field during all lunar phases throughout the spawning seasons of 2001 and 2002. This suggested that spawning was not following a lunar rhythm. Spawning in captive individuals was observed on 38 consecutive days from 7 July to 14 August 2002. During this period, wild spawning events were observed on 18 nights within aggregations of adults that formed around the outside of the net-pen facility. Spawning may have occurred outside the pens on other nights, however, the visibility was sometimes too poor to observe behaviour beyond the boundaries of the pens. When captive females were dissected at the end of the study, 77"6% of the females were visibly hydrated, thus indicating that spawning was still imminent. Spawning activity was high on the night previous to

Proportion of females with hydrated oocytes

0·4 17

0·3 13

18 36

11

0·2

30

27

20

30

44

0·1

0 0

Full

Last

New

June

First

Full

Last

New

First

Full

July

Last

9

1

New

First

August

Full

September

Lunar phase and month

FIG. 6. Proportion of females with hydrated oocytes among 255 female kelp bass collected from Santa Catalina Island, California, U.S.A., by lunar phase and month from June to September 2002.

Numbers over bars represent samples sizes for each lunar phase.

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sacrifice, with 45 spawning events observed over a 77 min period. Thus, it is probable that many of the females spawned on consecutive evenings.

D I E L S P A WN I N G P E R I O D

Ripe ovaries with hydrated oocytes were collected from mature females throughout all time periods (0700–2100 hours) during the spawning season.

This suggests that females have a prolonged period of hydration prior to spawning. Similar results were found in P. clathratus by Oda et al. (1993). Courtship and spawning, however, were observed only during the evening hours. Many dives were made during sunrise, morning and afternoon time periods, but courtship and spawning behaviours were never observed during those periods.

Activity during the morning hours was limited largely to feeding behaviour.

Spawning events were observed at field sites between 1934 and 2025 hours, or 21 min before sunset to 24 min past sunset. The time of first spawning in captive individuals was significantly correlated with time of sunset (rS, d.f. ¼ 16, P ¼ 0"021) (Fig. 7). Observations of spawning events by captive individuals ranged from 1910 to 2110 hours, or 33 min before sunset to 20 min after sunset.

Spawning in captive individuals continued well past dark and was observed >1 h after sunset. Eggs were collected on the surface as late as 2155 hours, c. 2 h after sunset. From this, a maximum diel spawning period of c. 2"5 h was estimated, beginning c. 30 min before sunset and continuing for up to 2 h after sunset.

SP A W N I N G F R E Q U E N C Y

Both males and females participated in multiple spawnings during a single evening, and individual males were observed participating in up to three

Time (hours)

2100

2000

1900 13 Jul

18 Jul

23 Jul

28 Jul

2 Aug

7 Aug

12 Aug

17 Aug

Date FIG. 7. Time of first observed spawn of captive adult kelp bass from Catalina Harbor, Santa Catalina Island, California, U.S.A., by date of observation from 12 July to 16 August, 2002. The onset of first spawning (!) was compared to the time of sunset (– –) for each observation period.

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spawning events within a 10 min period. Often males that had just spawned would swim rapidly towards a newly formed subgroup and immediately spawn within that group. The continually high activity levels of males throughout observation periods suggested that males might have spawned continuously throughout the course of the evening. Two females were observed to spawn twice in a single evening. On both occasions, the time between the first and second spawns was c. 5 min. It is not known whether females spawned throughout the evening. Within a single observation period, the number of spawnings observed varied from 17–45, and the spawning rate varied from 0–5 spawnings min%1 [Table III]. The mean spawning rate ranged from 0"58–1"56 spawnings min %1 among observation periods, and the mean spawning rate over the entire study was 0"94 spawnings min%1.

DISCUSSION MATING SYSTEM AND BEHAVIOUR PATTERNS

Group spawning appears to be the predominant mating pattern of P. clathratus at Santa Catalina Island, as supported by both behavioural observations and the IG of ripe males. Spawning occurred in groups of three to 23 individuals that formed within larger breeding aggregations, and pair spawning was never observed. There was no evidence of alternative male strategies such as female defence or female mimicry (Taborsky, 1994; Gross, 1996). Males of all size classes participated in group-spawning events, and male-male aggressive behaviour was observed rarely. Several males often engaged in simultaneous courtship with gravid females, and males did not attempt to exclude other males from spawning with females.

The size of testes in ripe males often has been used as an index of sperm competition and a method for predicting the mating system of fishes. Studies on interspecific patterns of IG and sperm competition of fishes have found that relative testes size and IG increases with increasing levels of sperm competition (Stockley et al., 1997; Petersen & Warner, 1998). When sperm competition is TABLE III. Spawning frequencies of 50 male and 58 female kelp bass by date of observation from a captivity study conducted from June to August 2002 at Catalina Harbor, Santa Catalina Island, California, U.S.A. Individuals were placed in a 700 m3 floating net-pen in order to document patterns in spawning behaviour Date 16/7/02 18/7/02 24/7/02 5/8/02 6/8/02 7/8/02 14/8/02

#

Number of spawning events

Duration (min)

Rate (number of spawning per min)

Maximum rate (number of spawnings per min)

27 18 28 17 21 36 45

25 20 18 13 40 60 77

1"08 0"9 1"56 1"31 0"53 0"6 0"58

3 2 3 3 4 5 3

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high, such as in fishes that spawn in large groups, males often possess large testes and produce more sperm in order to increase their potential number of fertilizations (Warner, 1997; Petersen & Warner, 1998). In general, high IG (i.e. '4) in males is common in group-spawning fishes under intense sperm competition, while low male IG (0"5–3) is typical of pair-spawning fishes where sperm competition is less important (Warner, 1984; Stockley et al., 1997; Petersen & Warner, 1998; Taborsky, 1998).

Mean IG of collected and captive male kelp bass (5"8 and 6"1 respectively) were similar to published values of IG from fishes characterized by external fertilization, intense sperm competition and communal spawning (Petersen & Warner, 1998). The IG of male kelp bass attained values of up to 13"1, which ranks among the highest reported values for any species of fish. An IG of >7% was found in ripe males of all size classes, and this supports the observations that both small and large males participate in group-spawnings. Male IG values of group spawning fishes, however, are not consistent among fish families, and comparisons within the Serranidae are particularly important (Petersen & Warner, 1998). Although IG data are only available for a few species of serranids, similar results were found for the group-spawning grouper, Epinephelus striatus (Bloch), where sperm competition is high and testes masses reach 10% of body mass (Sadovy & Colin, 1995). Conversely, the IG of pair-spawning serranids is usually <2% (Petersen & Warner, 1998; Chan & Sadovy, 2002; pers. obs.).

There is considerable evidence that the sexual patterns of fishes are influenced by their mating systems (Warner, 1984). The size advantage model (Ghiselin, 1969; Warner, 1975; Mun˜oz & Warner, 2003) makes several predictions regarding the relationships between mating systems and sexuality, and these predictions are well supported by a variety of observational and experimental studies on several groups of marine fishes, including many species of wrasses and parrotfishes (Robertson & Warner, 1978; Warner & Hoffman, 1980; Hoffman, 1985; Mun˜oz & Warner, 2004). In particular, sex change should be less common in species where large males have less opportunity to monopolize mating. Thus, a gonochoric sexual pattern is predicted for fishes with a group spawning mating system, where mate monopolization by large males does not occur, all males have access to females and sperm competition is intense. Moreover, territorial defence of females or spawning sites should be rare or absent in gonochoric fishes with group spawning mating systems characterized by intense sperm competition. In general, the mating system of P. clathratus at Santa Catalina Island was consistent with predictions of the size advantage model and the gonochoric sexual pattern found by previous histological studies.

The spawning behaviour of adult P. clathratus was very similar to that observed in other functionally gonochoric, group-spawning serranids. In Paralabrax nebulifer (Girard), a congener of P. clathratus with an overlapping geographic range, adults form large breeding aggregations of hundreds to thousands of individuals over soft bottom habitats in water depths of 20–40 m during the summer months (Turner et al., 1969; Feder et al., 1974; Love et al., 1996a).

Although the mating system of the species has not been investigated thoroughly, spawning probably occurs in smaller groups within these aggregations (BacaHovey et al., 2002; pers. obs.). Observations of adult P. nebulifer during the #

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course of this study suggest they have many behavioural similarities to P. clathratus, including year-round aggregating behaviour and non-territorial social patterns. Recent investigations on the reproductive biology of southern California populations have characterized P. nebulifer as functionally gonochoric (Baca-Hovey et al., 2002; Sadovy & Domeier, 2005). Epinephelus striatus form large breeding aggregations along reef edges and spawning occurs around sunset within smaller groups of three to 25 fish that consist of a lead female and multiple males (Colin, 1992; Aguilar-Perera & Aguilar-Davila, 1996). Although once thought to be protogynous, more recent work characterized this species as functionally gonochoric (Sadovy & Colin, 1995).

Many tropical reef fishes, including several species of serranids, aggregate to spawn at precise locations and times of the year (Colin, 1992; Gilmore & Jones, 1992; Shapiro et al., 1993; Samoilys & Squire, 1994; Rhodes & Sadovy, 2002). A review of the current knowledge of tropical reef fish spawning aggregations by Domeier & Colin (1997) defined a spawning aggregation as â&#x20AC;&#x2DC;a gathering of conspecific fish, for the purposes of spawning, that consisted of fish densities significantly higher than are found during the non-reproductive period, or for fishes that normally occur in dense schools, must occur in significantly greater number and take up significantly more space.â&#x20AC;&#x2122; Furthermore, they identified two aggregation types, resident and transient, based on the frequency and duration of the aggregation, site specificity of the aggregation and distance travelled by individuals to aggregation sites. Epinepheline serranids known to form spawning aggregations were classified as transient spawning aggregations.

Kelp bass do not appear to fit the criteria of a typical spawning aggregation for several reasons. First, kelp bass formed aggregations throughout the year, and spawning aggregations were not necessarily larger or more dense than nonspawning aggregations. Second, P. clathratus spawning aggregations were unpredictable both temporally and spatially throughout the year, and the formation of aggregations did not follow any specific pattern, such as a lunar or semi-lunar rhythm. Feder et al. (1974) described a similar pattern in kelp bass and noted the periodic disappearance of adults from study sites during the summer months.

Sport fishers have also reported the sudden formation and disappearance of mass aggregations of adults during the spawning season (Love, 1996).

It is unclear whether adult P. clathratus form local spawning aggregations or migrate to form spawning aggregations elsewhere, although there is evidence that both patterns occur. A tagging study by Young (1963) showed very limited adult movement in kelp bass from southern California, and Lowe et al. (2003) reported small home ranges and high site fidelity in adults tracked using acoustic telemetry within the marine reserve on Santa Catalina Island.

The sporadic formation and disappearance of aggregations observed by the authors and by fishers suggest that adult P. clathratus may migrate under certain conditions. Additional evidence of adult migration was described by Love (1996), who observed large schools of adult kelp bass several kilometres off the coast of southern California and reported significant movements of tagged individuals away from offshore oil platforms and reefs during the autumn months. In the future, large-scale tracking studies on adult aggregations could be very useful in understanding the movement patterns of kelp bass spawning aggregations. #

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TEMPORAL SPAWNING PATTERNS

Several factors indicated a daily pattern of spawning by P. clathratus.

Spawning in captive adults was observed on a daily basis for 5 weeks in 2002 and did not appear to fluctuate within the lunar cycle. Females containing hydrated oocytes, a clear indication of imminent spawning, were collected continuously throughout the spawning season and showed no evidence of a lunar or semi-lunar rhythm. The IG of hydrated females did not appear to fluctuate with the lunar cycle, which suggested that the relative fecundity of spawning females did not change over the lunar cycle. In addition, all but four of the captive females (n ¼ 60) in this study, when sacrificed, contained hydrated oocytes. This suggested that these females would spawn that evening. Spawning was very active on the previous night, and this indicates that many captive females were capable of spawning on consecutive evenings. Daily spawning in captive individuals was consistent with the results found in histological work by Oda et al.

(1993), who concluded that females spawned every 1–2 days, with larger females capable of spawning daily. Paralabrax clathratus males and females were also capable of spawning multiple times during a single evening; this behaviour has been reported in several epinepheline groupers (Sadovy et al., 1994b; Samoilys & Squire, 1994; Zabala et al., 1997).

Spawning during specific lunar periods is well documented in several epinepheline serranids (Smith, 1972; Thresher, 1984; Shapiro, 1987; Sadovy et al., 1994a, b; Rhodes & Sadovy, 2002;), however, serranines and anthiines do not appear to follow this pattern (Thresher, 1984). Past studies on the settlement patterns of kelp bass in southern California, including Santa Catalina Island, found a significant relationship between the lunar cycle and settlement patterns of post-larval individuals, where settlement occurred mainly around new and full moons (Cordes & Allen, 1997; Findlay & Allen, 2002). Obviously, backcalculated spawning dates indicated that spawning followed a similar pattern. Data from the present study, however, do not support the existence of a semi-lunar rhythm. Spawning in P. clathratus occurred throughout the lunar cycle, thus indicating that spawning and settlement are independent events. Settlement appears to be most successful after spawning events that occurred during new and full moon phases characterized by spring tides. Therefore, successful settlement may reflect successful larval transport both offshore and onshore by strong tidal fluctuations (Thresher, 1984; Cordes & Allen, 1997; Findlay & Allen, 2002).

This pattern would seem to select for individuals that spawn during spring tides, so that the high cost associated with gamete production could be limited to successful periods. Surprisingly, P. clathratus at Santa Catalina Island do not seem to adhere to this pattern. Adults appear to be increasing their reproductive output by spawning frequently, thereby maximizing the number of larvae present in the plankton over time.

IMPLICATIONS FOR MANAGEMENT

Fishes that aggregate in large numbers are extremely vulnerable to over-fishing, because many adults can be removed from the population in a short period of time. A reduction in the abundance of breeding adults could have many #

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dramatic effects, including a reduction in stock abundance and reproductive output, shifts in size structure and age at first maturity, altered sex ratios and changes in the genetic makeup of populations (Olsen & LaPlace, 1979; Smith et al., 1991; Colin, 1992; Shapiro et al., 1993; Sadovy et al. 1994a; Bohnsack, 1996; Beets & Friedlander, 1998; Johannes et al., 1999; Sadovy & Eklund, 1999; Levin & Grimes, 2002; Rhodes & Sadovy, 2002). In some cases, lowered aggregations densities may lead to a decrease in the per capita spawning rate of adults.

For example, Colin (1992) observed a significant reduction in courtship activity and spawning colouration in spawning aggregations of E. striatus that had been significantly reduced by fishing pressure. If aggregations require a minimal density for spawning to occur or adults depend on each other for spawning cues, over-fishing may cause spawning to cease altogether (Coleman et al., 1996; Vincent & Sadovy, 1998; Levin & Grimes, 2002).

Similar to many tropical serranids, aggregation spawning appears to be an important component of the annual reproduction of this species, and spawning activity is probably disrupted by intense fishing activity on these aggregations.

Although the spawning activity of adults in breeding aggregations is potentially very high, the removal of many adults from these aggregations could have many negative effects on kelp bass populations, including significant decreases in reproductive output. The large declines in kelp bass landings caused by commercial fisheries after World War II clearly demonstrate the vulnerability of the species to over-fishing. More recently, significant declines in larval recruitment, adult abundances and recreational fishery landings have been reported in some areas of southern California (Allen & Hovey, 2001; Pondella et al., 2002; Stephens & Pondella, 2002). Although many factors may have contributed to these declines, the over-fishing of spawning aggregations by recreational fisheries undoubtedly has had the greatest impact on adult population abundance and fishery landings. Recreational fisheries target P. clathratus breeding aggregations throughout the summer months, often removing several hundred to over a thousand individuals from an area in a single day. Clearly, more research is necessary to determine the effects of fishing pressure on the reproductive patterns of kelp bass. Nevertheless, future management considerations that limit the exploitation of P. clathratus spawning aggregations, including reductions in catch limits and area closures, may help to offset current declines and enhance the fishery.

The authors thank M. Adreani, E. Bing-Sawyer, K. Doctor, S. Albers, D. Pondella, K.A. Miller, J. Froeschke and E. Miller for their contribution to this project. We also would like to thank the CSUN Fish Lab., the Vantuna Research Group of Occidental College and the crew of the RV Vantuna and RV Yellowfin for their assistance in the collection of samples. We are grateful to S. Albers and the Catalina White Seabass fund for use of the grow-out facility during the captive study. Special thanks to P. Hastings, T. Donaldson, C. Petersen, R. Carpenter, C. Lowe and P. Edmunds for their advice and for reviewing the manuscript. This research was supported by the University of Southern California’s Wrigley Institute for Environmental Studies, the PADI Foundation and several funding sources at California State University, Northridge, including the Nearshore Marine Fish Research Program (NMFRP), the Office of Graduate Research and International Programs and the Student Projects Committee. This is contribution number 235 from the University of Southern California’s Wrigley Marine Science Center, Santa Catalina Island.

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Aguilar-Perera, A. & Aguilar-Davila, W. (1996). A spawning aggregation of Nassau grouper Epinephelus striatus (Pisces: Serranidae) in the Mexican Caribbean.

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