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Sexual development and reproductive seasonality of hogfish (Labridae: Lachnolaimus maximus), an hermaphroditic reef fish

Journal of Fish Biology

October 2007
71(5):1270 - 1292

DOI:10.1111/j.1095-8649.2007.01580.x

Authors:

Richard S. McBride

National Oceanic and Atmospheric Administration

Michael Johnson

National Marine Fisheries Service

The seasonality, size, age, colour phases and sexual dimorphism of 13 reproductive classes of hogfish Lachnolaimus maximus are described. Analysis of histological sections of gonads (n = 1662) confirmed earlier conclusions that L. maximus is a monandric, protogynous hermaphrodite. Sex change was initiated at the end of the spawning season and over a broad range of sizes and ages. It occurred after a functional female phase (postmaturation) and proceeded more slowly (months) than previously believed. Eventually all individuals changed sex to a terminal male phase. Females were batch spawners, spawning as often as every day during winter and spring. There was no evidence of precocious sperm crypts in active females, sperm competition or other alternative male sexual strategies. Mating has been reported elsewhere to be haremic. The sexual development of L. maximus appears to be adaptive in terms of Ghiselin’s size-advantage model, which links monandric protogyny and polygyny. The slow rate of sex change, however, poses problems when fishing pressure is high because harvest of a single male has the potential to reduce the reproductive output of an entire harem.

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Sexual development and reproductive seasonality of

hogﬁsh (Labridae: Lachnolaimus maximus),

an hermaphroditic reef ﬁsh

R. S. MCBRIDE*AND M. R. JOHNSON†

Florida Fish and Wildlife Conservation Commission, 100 8th Avenue SE,

St Petersburg, FL 33701-5095, U.S.A.

(Received 11 August 2006, Accepted 15 May 2007)

The seasonality, size, age, colour phases and sexual dimorphism of 13 reproductive classes of

hogﬁsh Lachnolaimus maximus are described. Analysis of histological sections of gonads (n¼

1662) conﬁrmed earlier conclusions that L. maximus is a monandric, protogynous hermaphro-

dite. Sex change was initiated at the end of the spawning season and over a broad range of sizes

and ages. It occurred after a functional female phase (postmaturation) and proceeded more

slowly (months) than previously believed. Eventually all individuals changed sex to a terminal

male phase. Females were batch spawners, spawning as often as every day during winter and

spring. There was no evidence of precocious sperm crypts in active females, sperm competition

or other alternative male sexual strategies. Mating has been reported elsewhere to be haremic.

The sexual development of L. maximus appears to be adaptive in terms of Ghiselin’s size-

advantage model, which links monandric protogyny and polygyny. The slow rate of sex change,

however, poses problems when ﬁshing pressure is high because harvest of a single male has the

potential to reduce the reproductive output of an entire harem. #2007 The Authors

Journal compilation #2007 The Fisheries Society of the British Isles

Key words: dichromatism; dimorphism; monandry; postmaturation; protogynous; sexuality.

INTRODUCTION

Hermaphroditism is widespread and takes on many forms among teleosts, having

been reported for >350 species in 34 families in eight orders (Kuwamura &

Nakashima, 1998). The most common type is protogyny, when at least some in-

dividuals in a population change sex sequentially from female to male. Rarer

types are protandry (male to female), simultaneous hermaphroditism and

two-way sex change. Among protogynous hermaphrodites, there are two par-

allel patterns of sexual development: monandry, when all males present in a

*Author to whom correspondence should be addressed at present address: National Marine Fisheries

Service (NMFS), Northeast Fisheries Science Center, 166 Water Street, Woods Hole, MA 02543-1026,

U.S.A. Tel.: þ1 508 495 2244; fax: þ1 508 495 2258; email: richard.mcbride@noaa.gov

†Present address: NMFS, Northeast Regional Ofﬁce, 1 Blackburn Drive, Gloucester, MA 01930,

U.S.A.

Journal of Fish Biology (2007) 71, 1270–1292

doi:10.1111/j.1095-8649.2007.01580.x, available online at http://www.blackwell-synergy.com

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population have changed sex (i.e. secondary males) and diandry, when gon-

ochoristic males (i.e. primary males) are present with secondary males. Sex

change can proceed along two serial pathways relative to maturation: prematu-

ration, when an individual initiates female development but changes sex prior

to maturing as a female (i.e. functional analog to primary males) and postmatu-

ration, when an individual matures ﬁrst as a female and changes sex later.

Finally, adults of many hermaphroditic species are dichromatic, dimorphic or

both (Robertson & Warner, 1978; Warner & Robertson, 1978).

Much of the comparative research of hermaphroditic species has concerned

wrasses (Labridae) worldwide (Yamamoto, 1969; Reinboth, 1970, 1975; Dipper

& Pullin, 1979; Charnov, 1982; Hoffman, 1983; Warner, 1984; Warner &

Lejeune, 1985; Moyer, 1991). This should not be surprising because Labridae

is a large family, with nearly 600 species distributed in tropical and temperate

waters (Gomon, 1997; Parenti & Randall, 2000). In a single study, Warner &

Robertson (1978) compared the sexual patterns of nine western North Atlantic

wrasses, and further comparative work has been published since (Robertson,

1981). Conspicuously absent from this body of work are comparative data

for hogﬁsh Lachnolaimus maximus (Walbaum), the largest and most economi-

cally valuable wrasse in the western North Atlantic Ocean (McBride &

Murphy, 2003). In Florida, L. maximus are most commonly associated with

reef edges, but uncommon among reef-ﬁsh fauna in general (Starck, 1968;

Smith, 1976). Several hundred specimens were collected over several years

and with a variety of sampling gears; an otolith method was used to age

these ﬁsh, and a histological method was used to determine their sex and

spawning condition. In the present study, the monandric, protogynous nature

of L. maximus (Davis, 1976; Claro et al., 1989) is investigated, as is the juvenile

period, postmaturative sex change, rate of sex change, lack of sperm competi-

tion, the eventual change of all individuals into secondary males, and the

appearance of dichromatic characters and dimorphism.

These data are also ‘confronted’ with Moe’s life-history model for a monan-

dric, protogynous hermaphrodite. Moe (1969) ﬁrst developed this model for

Epinephelus morio (Valenciennes) (Serranidae), when he deﬁned 10 classes to

integrate both sexual development (a linear process of ﬁrst maturation, transfor-

mation and a second maturation) and reproductive seasonality (a cyclic process:

ﬁrst as a female, then as a male). Moe’s (1969) paper is commonly cited, but few

papers rigorously test Moe’s life-history model with data from new species.

MATERIALS AND METHODS

Specimens of L. maximus were collected from November 1995 to April 2001 in two

geographic regions along Florida’s coast: the eastern Gulf of Mexico (within the

boundaries of 255°to 300°N; 815°to 845°W) and south Florida (within 240°to

255°N; 805°to 835°W). Specimens were collected from both regions during

all months of the year. The majority of ﬁsh were collected by spear, from ﬁshery-

dependent sources in both regions, and ﬁshery-independent collections in south Florida.

Other notable sources included a commercial trap ﬁshery in 20–30 m depths, offshore

of the Suwannee River, two ﬁshery-independent, otter-trawl surveys in the eastern Gulf

of Mexico and a ﬁshery-independent otter-trawl survey in south Florida; a few miscel-

laneous samples (hook & line or unknown gear) were recorded as well.

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These diverse sampling methods collected the complete, known size and age spectra.

Fish <305 mm fork length (L

)(c. age 3 years) are smaller than the minimum size

regulation, but were collected by ﬁshery-independent methods. Fish as large as previous

reports of maximum size (11 kg; Randall & Warmke, 1967), and ﬁsh older than reports

of maximum age (age 11 years; Claro et al., 1989), were made available from the ﬁsh-

ery. In this study, L

was measured to the nearest mm, and whole body mass (M

) and

gonad mass (M

) were measured to the nearest 10 and 01 g, respectively. The gonado-

somatic index (I

) was calculated as I

¼100M

M

)

1

. Fish ages were deter-

mined by a validated otolith method (McBride & Richardson, 2007).

The sexual development of 1662 ﬁsh (1191 of which were aged) was determined from

histological preparations of gonad tissue. Fish were kept on ice in the ﬁeld, and they

were processed in the laboratory within hours of collection. A small piece of tissue

was excised and ﬁxed in 10% buffered formalin. Rinsed and dehydrated in ethanol,

tissue samples were embedded in glycol methacrylate, sectioned along the transverse

plane and stained in periodic acid Schiff’s haematoxylin and counterstained with meta-

nil yellow (Quintero-Hunter et al., 1991). Anterior, middle and posterior tissue sections

from 14 L. maximus (including female, transitional and male classes) were examined for

germ cell development, appearance of the tunica albuginea and the formation of atretic

bodies. No effect of sub-sample location was evident, so a single sample from the

middle of the gonad was used for characterizing an individual’s sex and development.

At least one whole section of tissue was scanned per ﬁsh by two independent readers

at 100–200 magniﬁcation.

The most advanced oocyte stage was noted, ordered in sequence, as perinucleolar,

cortical alveoli formation, vitellogenesis, germinal vesicle (¼nucleus) migration and

germinal vesicle breakdown. Perinucleolar oocytes represent an early stage of meiotic

development, namely the ascension to the diplotene part of prophase I. As an oocyte

develops, cortical alveoli emerge in the cytoplasm, which is recognized as a separate

stage (historically called the yolk vesicle stage; West, 1990). Vitellogenic oocytes, those

cells with yolk globules that accumulate vitellogenin, indicate a speciﬁc hormonal

response to spawning readiness (Wallace & Selman, 1978). The end of vitellogenesis

is marked by the diakinesis part of prophase I, which is followed by three steps of ﬁnal

oocyte maturation: nucleus migration, oocyte hydration and nucleus breakdown.

Postovulatory follicles (POFs) and atretic germ cells were also noted. POFs appear

following release of the egg into the lumen. They were identiﬁed as POFs if they were

no more than partially collapsed, so the theca and granulosa layers were still evident,

which is postulated to indicate that these POFs were <24 h old; this assumption seemed

reasonable because the frequency of occurrence of such POFs was very similar to the

occurrence rate of hydrated oocytes (McBride et al., 2002; McBride & Thurman,

2003; unpubl. data). The presence of atretic oocytes was also noted to aid in the iden-

tiﬁcation of postspawning females and transitional ﬁsh.

Stages of spermatogenesis were noted in the following order: spermatogonia, sperma-

tocytes, spermatids and spermatozoa. Later stages were typically observed, in varying

amounts in all of the different male classes. Therefore, males were classiﬁed by (1)

the dominant stage of spermatogenesis evident in spermatocysts and (2) by the amount

of spermatozoa in discontinuous lobules and in the tunica sinuses. The extent of inﬁl-

tration of the seminiferous tissue, into the ovigerous lamellae and away from the tunica,

was also noted, which aided in identifying transitional, immature and other ﬁrst-year

males.

Initially, L. maximus gonads were sorted into the 10 developmental classes (Table I)

deﬁned by Moe (1969). These data were tested against Moe’s (1969) model for a monan-

dric, postmaturative, protogynous hermaphrodite (Fig. 1); ‘testing’ is used here to refer

to a process of ‘confronting’ the data with speciﬁc model predictions. This model pre-

dicts that: female maturation, sex change and male maturation occur in an orderly

sequence with respect to age; no primary males exist; spawning activity is synchronized

between mature females and mature males; sex change occurs after at least one spawn-

ing season as a female. Modiﬁcations to Moe’s (1969) model are tabulated in Table I

and described in the text for each class.

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TABLE I. Tabulation of reproductive classes used in this study, including histological descriptions of each class’s gonad tissue as summarized

for Epinephelus morio by Moe (1969), and as modiﬁed for Lachnolaimus maximus. Changes in class names, differing from those used

speciﬁcally by Moe (1969), are in italics. All mature classes are identiﬁed here as active or inactive to identify them as ready to spawn at time of

capture (or within days) or not

Class Moe (1969) This study

1 Immature female ‘gonad shows no signs of prior

[vitellogenin] activity’

Moe (1969) included in class 1 those individuals with

cortical alveoli present in some oocytes, referring to

this as ‘limited’ vitellogenesis. Here, such individuals

were advanced into class 2, which conservatively

limits class 1 to virgin ﬁsh with no immediate prospect

of spawning

2 Mature recrudescing

(inactive) female

‘vitellogenesis absent but atretic bodies and

sometimes expanded tunica indicate prior

oocyte maturation and spawning’

Moe (1969) labelled this class a ‘mature resting female’;

here, the term ‘recrudescing’ was used to indicate that

while active spawning was not occurring, the gonad

was ‘busy’ preparing for a new spawning season.

This class included those ﬁsh with proliferating nests

of oogonia and previtellogenic oocytes (see above)

3 Mature (active) female ‘vitellogenesis present with [gonad]

developing towards spawning condition’

This class was not modiﬁed in relation to Moe (1969).

It included actively spawning ﬁsh as well:

females undergoing ﬁnal oocyte maturation or with

postovulatory follicles <24h old

4 Mature postspawning

(inactive) female

‘degenerate [vitellogenic] oocytes present,

tunica expanded and loose and atretic

bodies forming’

Moe (1969) labelled this class as ‘spent female’, which

may be misleading because, although advanced oocytes

are degenerating, nests of proliferating oogonia can be

frequently observed. It was often difﬁcult to distinguish

class 4 from class 2 because of post mortem atresia,

common in ﬁshery-dependent collections; ‘suspicious’ ﬁsh

were classiﬁed as class 2

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TABLE I. Continued

Class Moe (1969) This study

5 Transitional female–male Similar to a class 4 ﬁsh ‘but crypts of

spermatogonia and spermatocytes

also present in the epithelium

at the periphery of the lamella’

This class was narrowly deﬁned here as only exhibiting

a small number of seminiferous crypts along the tunica,

or spermatogenesis within only a small number of tunica

sinuses. Thus, class 5 is the earliest and most discrete

point of sex change

6 Immature male ‘similar to the transitional [class], but

spermatogenesis spread throughout

the lamellae, and oocyte nuclei are

pycnotic’

A ﬁsh was a class 6 once seminiferous crypts formed

a continuous strip along the tunica and for as long as

clusters of ovigerous tissue (more than just isolated

oocytes) were present in the lamellae

7*, 8*, 9* Maturing,

ﬁrst-year male

Not recognized as separate classes by

Moe (1969) (Fig. 1)

These ﬁrst-year males were observed as a regular, seasonal

progression between class 6 and 9 (Fig. 3) and thereby

warranted speciﬁc status as classes (Fig. 10). The

seminiferous tissue of classes 7*, 8* and 9* had the same

appearance as classes 7, 8 and 9, respectively, but isolated

oocytes were still present in the former classes

7 Mature, recrudescing

(inactive) male

Gonad ‘dominated by early stages

of spermatogenesis’

The present observations indicated that class 7*, and not

class 7, followed class 6 (see above and Fig. 10). The term

recrudescing was added to the label to indicate active

meiosis in this class

8 Mature, ripening (active) male Gonad ‘dominated by the later stages

of spermatogenesis’

This class was not modiﬁed in relation to Moe (1969)

9 Mature, ripe (active) male Gonad ‘fully developed and distended with

tailed sperm’

This class was not modiﬁed in relation to Moe (1969)

10 Mature, postspawning

(inactive) male

Gonad ‘dominated by stromal tissue

and rapidly developing crypts of

spermatogonia, tunica

somewhat extended and loose’

This class was not modiﬁed in relation to Moe (1969)

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Sexual development was also examined based on external characteristics. Colin

(1982) stated that males, but not females, have dark reddish-brown markings about

the head (i.e. appearing as a mask) and along the base of the medial ﬁns, and a pigment

patch posterior to the pectoral ﬁn. Morphologically, males have a longer snout, and

some ﬁn elements are more elongated than those of females. The following attributes

were recorded for a sub-set of 329 individuals: pigmentation along the forehead and

nape area, along the medial ﬁns and on the body (i.e. as a dash behind the pectoral

ﬁn). Upper jaw length, as deﬁned in Hubbs & Lagler (1947), was also recorded. Meas-

urements of (elongated) dorsal ﬁn spines and caudal ﬁn rays were attempted but aban-

doned because these elements were frequently broken.

RESULTS

Histological sections of L. maximus gonads were initially classiﬁed into 10

reproductive classes consistent with Moe’s (1969) scheme (Table I and Fig. 1).

A female phase consisted of an immature class (1) and three mature classes

(2–4). A male phase was categorized into transitional and immature classes

(5–6) and four mature classes (7–10). All males had a vestigial lumen, along

with sperm sinuses in the tunica, which conﬁrmed their secondary nature.

Many ﬁsh had ovo-testes. Those that still exhibited extensive ﬁelds of ovi-

gerous tissue adjacent to seminiferous tissue were assigned to class 5 or 6. Those

that exhibited only isolated oocytes embedded within seminiferous tissue were

initially assigned as class 7, 8 or 9, depending on the extent of spermatogenesis

(and no class 10 ﬁsh had isolated oocytes). It was apparent, however, that the

seasonal occurrence of males with isolated oocytes was different than the sea-

sonal occurrence of males without isolated oocytes. Thus, individuals with iso-

lated oocytes were put into three new classes (7*, 8* and 9*), a departure from

Moe’s (1969) original scheme. Size and age within these new classes were not

10 7

First maturation

Sex change

Final

oocyte

maturation

Recrudesence

Regression

Spawning

period

Spawning period

Non-spawning period

Non-spawning

period

Second maturation

FIG. 1. The sexual and reproductive development of a protogynous grouper (Serranidae: Epinephelus

morio) as proposed by Moe (1969). Reproductive classes 1–4 are female and classes 7–10 are male.

Classes 5 and 6 represent transitional and immature males. The classiﬁcation of Lachnolaimus

maximus gonads was compared to this scheme (see Table I for class names, histological criteria for

each class and deviations used in this study).

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signiﬁcantly different than class 6; in addition, class 7*, 8* and 9* followed

class 6 in an orderly seasonal progression. Thus, the hypothesis that males with

isolated oocytes occurred randomly, by month, size or age, is rejected. Instead,

it is postulated that classes 7*, 8* and 9* were still ﬁrst-year males, identiﬁable

because oocyte degeneration occurs slowly.

The histology, seasonal appearance, ﬁsh size and age, and I

of each class

(1–10) and including the three new classes (7*, 8* and 9*) are described in

sequence and summarized in Tables I and II.

FEMALE CLASSES

Class 1 immature female

Histological sections of immature females displayed only perinucleolar oocytes,

a thin tunica and few, if any, atretic oocytes [Table I and Fig. 2(b)]. Class 1

females were most frequently collected during autumn (Fig. 3). They were the

smallest and youngest ﬁsh observed (Table II and Figs 4 and 5). Class 1 gonads

were small relative to other female classes: I

<04 throughout the year (Fig. 6).

TABLE II. Descriptive statistics for (a) fork length (L

) and (b) age for each reproductive

class of Lachnolaimus maximus. Classes 6, 7*, 8* and 9* are pooled (6þ) because neither

size nor age differed signiﬁcantly among these classes. Letters signify size or age

groupings as identiﬁed by a Duncan’s multiple range test; different upper case letters

are in signiﬁcantly different groups (P<005). Sample size (n) are different between

(a) and (b) because not all ﬁsh were aged

Class Group Mean 95% CL Median Range n

(a) L

(mm)

1 A 192 8 185 80–368 197

2 B 299 8 275 121–640 491

3 C 269 7 254 147–571 408

4 BC 287 24 288 136–541 53

5 D 381 33 345 280–694 41

6þD 369 19 341 213–692 92

7 E 417 23 392 150–737 88

8 E 416 17 380 245–820 174

9 D 380 20 358 230–765 79

10 D 389 37 352 265–720 39

(b) Age (years)

1A 0

902 1 0–9* 135

2B 3

402 3 0–12 359

3B 3

002 3 0–9 283

4B 3

007 2 0–11 41

5C 4

810 5 1–11 24

6þC4

606 4 1–13 72

7D 6

407 6 0–13 57

8D 6

306 6 2–21 118

9D 5

906 5 1–15 66

10 D 6411 6 2–15 36

*There was one age 9 years ﬁsh among class 1 ﬁsh; the next oldest class 1 ﬁsh was age 4 years.

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Class 2 mature recrudescing (inactive) female

Perinucleolar oocytes dominated the lamellae, but cortical alveolar stages

arose and became common during recrudescence of the ovary [Table I and

Fig. 2(d)]. These females were either ﬁrst-time spawners undergoing their ﬁrst

maturation [indicated by no atresia; Fig. 2(d)] or they were already mature,

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repeat spawners [indicated by the presence of atretic cells; Fig. 2(j)]. Although

considered mature, they exhibited only previtellogenic oocytes and were not

considered capable of spawning at time of capture. Class 2 females, like class

1 females, were more frequent in autumn (Fig. 3). Class 2 females were sig-

niﬁcantly larger and older than class 1 females (Table II and Figs 4 and 5).

Class 2 gonads were larger than class 1 gonads; I

c.0

4–06 throughout the

year (Fig. 6).

Class 3 mature active female

These ready to spawn, often actively spawning, females were identiﬁed by the

presence of vitellogenic oocytes [Table I and Fig. 2(e)–(h)]. The cyclic fre-

quency of class 3 females indicated that spawning was concentrated during

winter and spring (December to May), peaking in April. There were some,

but relatively few, spawning individuals during summer and autumn (June to

November; Fig. 3). Class 3 females were signiﬁcantly larger but not older than

class 2 ﬁsh (Table II and Figs 4 and 5). Class 3 gonads were much larger than

gonads of all other classes: mean 95% CL I

3102(n¼350) during

December to May (Fig. 6).

Class 4 mature postspawning (inactive) female

Perinucleolar oocytes were dominant in this class. Key features to diagnose

this class were the additional presence of more advanced but degenerating

oocytes, and a high degree of vascularization by blood cells throughout the

ovigerous lamellae [Table I and Fig. 2(i)]. Class 4 females began to arise in

March, but most were observed in June (Fig. 3), which reconnects the seasonal

spawning cycle of females (i.e. class 2, 3, 4, then 2, 3, 4 and so on until the ﬁsh

change sex). Class 4 females were not larger or older than class 3 females, but

they were signiﬁcantly smaller and younger than any male class (Table II

and Figs 4 and 5). Class 4 gonads were similar in size to class 2 gonads: I

c. 04–05 (Fig. 6).

FIG. 2. Whole female Lachnolaimus maximus and histological images of ovarian tissue for classes 1–4 (see

Table I). (a) Class 1 female (65 mm fork length, L

, age 0 years) collected in February, (b) class 1

female (207 mm L

, age 1 years, June), (c) class 2 female (263 mm L

, age 5 years, April), (d) class 2

female with signs of recrudescence (240 mm L

, no age, September), (e) class 3 female with oocytes in

an early phase of vitellogenesis (248 mm L

, age 2 years, January), (f) class 3 female with vitellogenic

oocytes (267 mm L

, age 2 years, April), (g) class 3 female with a hydrated oocyte (445 mm L

, age 7

years, April), (h) class 3 female with a postovulatory follicle adjacent to an oocyte with a migrating

nucleus (285 mm L

, age 3 years, March), (i) class 4 female with signs of regression (193 mm L

, age

1 years, April) and (j) class 2 female with evidence of prior spawning (239 mm L

, age 2 years, April).

The major stages of oocyte development are indicated by upper case letters: P, perinucleolar; C,

cortical alveolar (yolk vesicle); V, vitellogenic (yolk) and H, hydrated (H). Other features include A,

an atretic oocyte; ch, the chorion; cy, cytoplasm; bv, blood vessels; fo, follicle; lu, lumen; nu, nucleus;

pasþ, periodic acid-Schiff reaction-positive bodies; pof, postovulatory follicle; tu, tunica (¼gonad

wall); yo, yolk formation; yv, yolk vesicles. (b) The scale bar ¼100 mm; all histology images are

scaled to this bar.

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Frequency

J FMAM J J A S ON D

Month

Class 1 (n = 197)

Class 2 (n = 491)

Class 3 (n = 408)

Class 4 (n = 53)

Class 5 (n = 41)

Class 6 (n = 51)

Class 7 (n = 88)

Class 7* (n = 11)

Class 8 (n = 174)

Class 8* (n = 23)

Class 9 (n = 79)

Class 9* (n = 7)

Class 10 (n = 39)

FIG. 3. Monthly frequency of occurrence of Lachnolaimus maximus reproductive classes. All classes,

including ﬁrst-year males (5, 6, 7*, 8* and 9*) are depicted separately. n, number of ﬁsh per class.

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SEX CHANGE AND MALE CLASSES

Class 5 transitional female–male

Ovigerous lamellae were still dominated by perinucleolar oocyte stages in

this class. If cortical alveolar or vitellogenic oocyte stages were present, then

they were atretic. This class was deﬁned narrowly as having isolated male germ

cells within tunica sinuses or within crypts along the edge of the tunica [Table I

and Fig. 7(b)]. Although the seminiferous tissue in a class 5 gonad was limited

in area, it typically contained all stages of male germ cells, from spermatogonia

to spermatozoa. The frequency of this class peaked in July and was observed

for only a short period (Fig. 3). Class 5 ﬁsh ranged in age from 1 to 11 years,

but most individuals in this class were larger and older than those in class 4

(Table II and Figs 4 and 5). The average I

for this class (c. 04) was only

slightly less than that of postspawning females, indicating that little change

in the gonad structure had occurred (Fig. 6).

Class 6 immature male

As sex change proceeded, seminiferous tissue inﬁltrated ovigerous tissue

medially from the periphery [Table I and Fig. 7(c)]. A ﬁsh was no longer con-

sidered class 5, and was instead categorized as class 6, once seminiferous tissue

extended more than halfway around the gonad wall. This class also occurred

for only a relatively short period, peaking in abundance in September (Fig. 3).

Sizes and ages of class 6 males were not signiﬁcantly different than those

assigned as class 7*, 8* or 9* (ANOVA, L

: d.f. ¼3, 88, P>005; age:

d.f. ¼3, 68, P>005), so data for these classes were pooled together in

Table II and Figs 4 and 5. The average I

for class 6 males was 02 during

June to November, demonstrating a continued shrinking of the gonad after

class 5, as the gonad reorganizes from a functioning ovary to a testis (Fig. 6).

Classes 7* and 7 maturing (7*) or mature (7), recrudescing (inactive) male

The seminiferous tissue of both class 7* and 7 is dominated by the early

stages of spermatogenesis (spermatogonia and spermatocytes) (Table I).

Spermatozoa were conspicuously absent or rare. Class 7* males had isolated

perinucleolar oocytes throughout the gonad [Fig. 7(d)], whereas class 7 males

did not [Fig. 7(g)]. Class 7* males were most abundant during September to

October, whereas class 7 males were most common during the summer (Fig. 3).

The tunica sinuses were small, empty or collapsed. Class 7 males were distinc-

tively larger and older than ﬁsh in classes 6 or 7* (Table II and Figs 4 and 5).

The I

of class 7 males during June to November was among the lowest

measured for any class (005–006; Fig. 6); the average I

was 015 during

December to May, for those few class 7 males collected during this period.

Classes 8* and 8 maturing (8*) or mature (8), ripening (active) male

Crypts of spermatocytes, spermatids and spermatozoa were assembled in

a mosaic (Table I). Isolated perinucleolar oocytes were found in class 8*

[Fig. 7(e)] but not in class 8 males [Fig. 7(h)]. Class 8* males were present

brieﬂy, mostly during October to December, whereas class 8 males were found

1280 R. S. MCBRIDE AND M. R. JOHNSON

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10 Class 1

15 Class 2

15 Class 3

15 Class 4

15 Class 5

15 Class 6+

15 Class 7

15 Class 8

15 Class 9

60 160 260 360 460 560 660 760 860

LF (mm)

Class 10

Frequency

FIG. 4. Fork length (L

) frequency of Lachnolaimus maximus reproductive classes. Classes 6, 7*, 8* and 9*

are pooled (6þ) because L

did not differ between these classes (see Table II for sample sizes).

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40 Class 1

Class 2

Class 3

Class 4

60 Class 5

Class 6+

60 Class 7

Class 8

60 Class 9

0246810121416182022

e (

ears)

Class 10

Frequency

FIG. 5. Age frequency of Lachnolaimus maximus reproductive classes. Classes 6, 7*, 8* and 9* are pooled

(6þ) because age did not differ between these classes (see Table II for sample sizes).

1282 R. S. MCBRIDE AND M. R. JOHNSON

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nearly year-round but were most abundant during winter and spring (Fig. 3).

Variable amounts of spermatozoa were present in tunica sinuses. Class 8 males

were not different in size and age than class 7 males (Table II and Figs 4 and 5).

The average I

increased 50–90% between June to November and December to

May (class 8*: from 008 to 012; class 8: from 012 to 022; Fig. 6).

Classes 9* and 9 maturing (9*) or mature (9), ripe (active) male

Spermiation was the deﬁning feature of this class, with spermatozoa packed

into discontinuous lobules and greatly expanded tunica sinuses (Table I). Iso-

lated perinucleolar oocytes were still observable in class 9* [Fig. 7(f)] but not

in class 9 males [Fig. 7(i)]. Class 9* males were observed from November until

April; class 9 males were observed from November to June. Class 9 males were

signiﬁcantly smaller than class 8 males, but they were not signiﬁcantly different

in age (Table II and Figs 4 and 5). The average I

for class 9 males was the

highest for any male class and was very consistent (c. 023) between June to

November and December to May; the average I

during the December to May

was also relatively high for class 9* males (019; Fig. 6).

Class 10 mature, postspawning (inactive) male

This class exhibited either spermatozoa within collapsed lobules or a bimodal

mix of spermatogonia and spermatozoa [Table I and Fig. 7(j)]. The seasonal

frequency of class 10 overlaps, but falls between, that of class 9 and 7 (Fig. 3),

reconnecting the seasonal spawning cycle of males (i.e. classes 7, 8, 9, 10, and

then 7, 8, 9, 10 and so on). The amount of germ cells in the tunica sinuses was

variable. Class 10 males were not different in L

and age than class 9 males

(Table II and Figs 4 and 5). The average I

was relatively high for those

few class 10 males collected during December to May (020) but very low during

June to November (005; Fig. 6).

GONAD MORPHOLOGY

A vestigial lumen was evident in all transitional and male L. maximus (Fig. 7;

i.e. no primary male-type gonad tissue was observed). Relative gonad size (I

)

0·0

0·5

1·0

1·5

2·0

2·5

3·0

3·5

4·0

123456 789107*8*9*

roductive class

nd nd

FIG. 6. Mean 95% CL gonado-somatic indicies (I

) for each class of Lachnolaimus maximus during two

alternating periods: a central component of the spawning season ( , December to May) and the rest

of the year when spawning is infrequent ( , June to November). nd, no data (<5 females).

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FIG. 7. A whole male Lachnolaimus maximus and histological images of gonad tissue for classes 5–10 (see

Table I). (a) Class 10 male (326 mm fork length, L

, age 6 years) collected in April, (b) class 5 male with

isolated pockets of seminiferous tissue forming along the gonad wall (box; 302 mm L

, age 5 years,

July), (c) class 6 male with ovarian tissue (top) and seminiferous tissue (bottom), both extensive and

adjacent to each other (326 mm L

, no age, January), (d) class 7* male (345 mm L

, no age, October),

(e) class 8* male (290 mm L

, no age, October), (f) class 9* male (340 mm L

, age 7, November),

(g) class 7 male (517 mm L

, no age, July), (h) class 8 male (359 mm L

, no age, April), (i) class 9 male

(457 mm L

, age 6 years, May) and (j) class 10 male (300 mm L

, no age, June). Stages of spermatogenesis

are indicated: sg, spermatogonia; sc, spermatocytes; sz, spermatozoa. Other labels are the same as in

Fig. 2. Each scale bar ¼100 mm. *, ‘ﬁrst-year’ male; note presence of isolated perinucleolar oocytes.

1284 R. S. MCBRIDE AND M. R. JOHNSON

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decreased from class 3 to 7*, as ovaries became restructured into functioning

testes (Fig. 6). Even though males grew to a much larger size than females,

whole ovaries were still much heavier (maximum ¼93 g) than whole ‘testes’

(maximum ¼14 g).

There was no indication of a sub-group of males with larger testes, which

would be indicative of sperm competition or an alternative male mating strat-

egy. Speciﬁcally, the frequency distribution of I

for classes 8 and 9 was not

signiﬁcantly different than a log-normal distribution (Shapiro–Wilk test for

normality, n¼141, P>005); nor did male size correlate with I

of class 8

and 9 ﬁsh; r

¼01, n¼141, P>005.

DICHROMATISM AND DIMORPHISM

Three colour phases of L.maximus were observed. Juvenile phase colouration

appeared on immature females as a dense, mottled pattern of rusty brown,

although the exact colour or intensity could vary depending on the environ-

ment [Fig. 2(a)]. The initial phase colouration appeared on mature females as

a solid reddish orange [Fig. 2(c)]. The terminal phase colouration appeared

on mature males as whitish or pale pink [Fig. 7(a)].

There were additional dichromatic characters in mature ﬁsh. Mature females

had a light brown mask covering their snout; mature males had a dark brown

mask. Males also had a continuous strip of reddish-brown pigment along the

medial ﬁns and a dash behind their pectoral ﬁns (Fig. 8). Based on laboratory

observations of dead ﬁsh, many ﬁsh of classes 5, 6, 7*, 8* and 7 did not have

all the pigmentation characteristic of a terminal male.

The snout became longer relative to L

as L. maximus changed from female

to male (Fig. 9). This character was not completely diagnostic, because the

snouts of smaller (<300 mm L

) males, and some larger males as well, were

not typically longer than those of females.

DISCUSSION

Lachnolaimus maximus are protogynous hermaphrodites, which was evident

from earlier reports of males with degenerating oocytes (Davis, 1976; Claro

et al., 1989). In the present study, a clear linear progression of sex development

was evident, with major transitions in L

and age occurring between: immature

(class 1) and mature females (classes 2–4); females and the ﬁrst year of

sex change (classes 5, 6, 7*, 8* and 9*); and ﬁrst-year males and older males

(classes 7–10).

Lachnolaimus maximus are monandric, which was evident from earlier reports

of testes with a central lumen (Davis, 1976; Claro et al., 1989). No alternative

male types were observed in this study. The male I

measured (i.e. c. 02 during

the spawning season) was similar to that measured for male L. maximus in the

Florida Keys, Puerto Rico and Cuba (Davis, 1976; Colin, 1982; Claro et al.,

1989), demonstrating geographic consistency. Similarly low I

values are re-

ported for secondary males of other labrids (Warner & Robertson, 1978).

Habitat migration was associated with female maturation. Class 1 females

were principally composed of age 0 year ﬁsh that grew to a size by autumn that

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was effectively collected by the small trawls towed in shallow, inshore habitats

(McBride & Richardson, 2007). Class 2 females, particularly those ranging in

size from 250 to 299 mm L

, were developing juveniles of a size known to move

from inshore seagrass beds or patch reefs to deeper, more offshore reefs during

autumn (Davis, 1976); this migratory behaviour may make class 2 vulnerable

to capture during this time of year.

100

123456 910787*8*9*

roductive class

Frequency

FIG. 8. Percentage of Lachnolaimus maximus in 13 reproductive classes, with different pigment patterns

(, head mask; , caudal band; , pectoral’ dash; , dorsal band) that are hypothesized

to be characteristic of terminal phase colouration. Classes are presented in the order of sexual

development and reproductive seasonality. The number of ﬁsh examined (n) are: 55 (class 1), 62

(class 2), 68 (class 3), 13 (class 4), 1 (class 5), 10 (class 6), 4 (class 7*), 7 (class 8*), 3 (class 9*), 15

(class 7), 41 (class 8), 36 (class 9) and 14 (class 10).

100

125

150

175

200

225

100 200 300 400 500 600 700 800

LF (mm)

Upper jaw length (mm)

FIG. 9. Relationship between head morphology (upper jaw length) and fork length (L

) for different

sexual phases of Lachnolaimus maximus: immature females ( ; class 1), mature females ( ; classes

2–4), ﬁrst-year males ( ; classes 5, 6, 7*, 8* and 9*) and mature males ( ; classes 7–10) (see Fig. 8

for sample sizes).

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Spawning by female L. maximus is seasonal, prolonged and frequent. Batch

spawning was evident from the presence of postovulatory follicles in all months

except August and September. Oocytes in ﬁnal maturation were commonly

found together with postovulatory follicles [in 210 of 408 class 3 females

(51%)], which indicated that spawning frequency may be quite high, even daily,

during the spawning period. Spawning by L. maximus was observed during

winter and spring in the Florida Keys (September to April; Davis, 1976), in Puerto

Rico (December to April; Colin, 1982) and south-western Cuba (November

to January; Claro et al., 1989). Protracted spawning periods are typical of

tropical wrasses (Gillanders, 1995). Daily spawning frequencies have been noted

for other ﬁshes (Matsuyama et al., 1990), even other wrasses (Warner, 1998), but

such high spawning rates are not common for other large coral reef ﬁsh species

(Petersen & Warner, 2002).

Spawning by male L. maximus is also seasonal, prolonged and frequent. Class

8* males may have been capable of spawning, but female spawning activity was

low during October to December, whereas class 8 males were found nearly year-

round and were most abundant during winter and spring, when females were

spawning. At least some of the class 9* males appeared to transform into class

9 before regressing into class 10 (Fig. 10). This suggested that class 9* males

were capable of fertilizing eggs (as ﬁrst-year males), although it is unknown if

they would have been as effective at fertilizing eggs as older, more experienced

males. Colin (1982) estimated that male L. maximus spawn daily and that they

successfully engage in as many as 50–100 spawning rushes in an afternoon.

Sex change by L. maximus is postmaturation. Sex change (¼class 5 and 6)

initiated principally among individuals 300–400 mm L

(or 3–5 years-old)

but was also observed in ﬁsh as large as 694 mm L

(and as old as 13 years).

Most males, including transitional ﬁsh and ﬁrst-year males, were larger and

older than the modal size and age of mature females (c. 275 mm L

, age 2

years). Transitional ﬁsh (class 5) arose seasonally after peak seasonal occur-

rence of both class 3 and 4. Thus, sex change occurred after one or more

spawning (as a female) seasons. Postmaturation sex change is common among

wrasses (Warner & Robertson, 1978) and was noted by Claro et al. (1989) for

L. maximus in Cuba.

Sex change by L. maximus requires several months to complete. This was

demonstrated by the orderly progression from a mature, postspawning female,

class 4 (peaking in June), to class 5 (July), to class 6 (September), to class 7*

(September to October), to class 8* (November), to a mature and probably

active male, class 9* (November to December), and then possibly becoming

indistinguishable with class 9 (April) before regressing into an inactive male

class 10 (April). Rate of sex change may be related to social system. Rapid

replacement of harvested terminal males, usually by the largest females, is com-

mon in ﬁshes with permanent social groups (Robertson, 1972; Shapiro, 1980;

Ross, 1990). In contrast, Davis (1976) noted that aggregations of L. maximus

are more common during the spawning season. The seasonal patterns of sex

change and social structure of L. maximus are likely to be similar to those of larger

sea basses, such as Mycteroperca microlepis (Goode & Bean), which initiate sex

change after the spawning season, when males and females separate into different

habitats until the following spawning season (McGovern et al., 1998).

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Lachnolaimus maximus conformed generally to Moe’s (1969) life-history

model (Fig. 1), but the data ﬁt better when the model was expanded to include

three additional ﬁrst-year male classes 7*, 8* and 9*, between class 6 and 9

(Fig. 10). This is the ﬁrst study to speciﬁcally include such ﬁrst-year classes,

even though Moe (1969) foresaw this possibility when he noted that ‘Early

and old males can be separated by the presence or absence of early oocytes

in the testicular tissue’. Moe (1969) believed that E. morio could spawn as

a female, change sex and spawn as a male all within a single season. He did

not document the rate of sex change for E. morio, however, so this remains

as an untested hypothesis for this serranid. In contrast, L. maximus began to

change sex at the end of the spawning season, and the process unfolded over

several weeks (from class 5 to 6) or months (from class 5 to 9* or 9). Such

a slow rate of sex change is not unusual for protogynous species (Sadovy &

Shapiro, 1987), and although there is probably some individual variability in

the rate of sex change, these ﬁndings do not agree with those of Claro et al.

(1989), who concluded that the rate of sex change by L. maximus was rapid

(days) and occurred primarily during the spawning season. Like Moe (1969),

Claro et al. (1989) did not present speciﬁc evidence to support their conclusion.

The present recognition of the special ﬁrst-year male classes (7*, 8* and 9*)

aided in identifying the rate of sex change in L. maximus, and this approach

may be useful for doing so in other sequential hermaphrodites.

All females change sex if they live long enough. The largest individuals with

diagnostic histology were all males (645–820 mm L

;n¼27). The oldest

known male (class 8) was age 21 years (670 mm L

). The oldest and largest

known female (class 2) was age 12 years (640 mm L

). Altogether, such evi-

dence does not suggest that size- or age-dependent processes are completely

First maturation

Sex change

Final

oocyte

maturation

Second maturation

Recrudesence

Regression

Recrudesence

First-spawning as a male

(winter–spring)

(summer–autumn)

FIG. 10. The sexual and reproductive development of Lachnolaimus maximus as observed in this study.

Reproductive classes 1–4 are female, classes 7–10 are male and classes 5–9* represent transitional,

immature and other ﬁrst-year males (see Table I).

1288 R. S. MCBRIDE AND M. R. JOHNSON

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controlling L. maximus sex change. This is notable because sex change over

a wide size range is more related to group spawners (Petersen & Warner,

2002), whereas L. maximus is a harem spawner (Colin, 1982).

Male L. maximus have long been noted to have more conspicuous pigmenta-

tion than females (Longley & Hildebrand, 1941), but changes in pigmentation

associated with sex change have not been rigorously tested in terms of speciﬁc

gonad classes. Colin (1982) identiﬁed juvenile colouration as early as 13 days

post-hatch, at c. 7mmL

. This juvenile colouration persisted among the much

larger but still immature females observed in this study. Among mature ﬁsh,

pigment changes were rapid in association with sex change. Class 6, 7* and 8*

males had a mix of the initial (female) and terminal (male) colour phases (Davis,

1976; present data), which suggested that these ﬁrst-year males may be difﬁcult

to distinguish from mature females in the ﬁeld, at least without careful inspec-

tion. This was true also for class 7 males. Otherwise, pigmentation should be

a simple and accurate way to distinguish female from male L. maximus.

The elongated snout of male L. maximus has also been long noted (Catesby,

1754; Breder & Rosen, 1966; Colin, 1982). As associated with sex change,

snout growth proceeded more slowly than changes in pigmentation. The dis-

tinctive snout morphology of males appears to take 1–2 years to develop fully;

this is reasonable considering that new bone growth will be required to achieve

this dimorphic character state. Claro et al. (1989) suggested that L. maximus’

sexual dimorphism diminishes by the time ﬁsh are 500–550 mm L

, but this

was not observed in the present study.

This detailed account of sexual development of L. maximus provides informa-

tion comparable with accounts available for other sympatric, co-familial species

(Warner & Robertson, 1978). Evolutionary mechanisms are often evident in

such comparisons because phylogenetic relationships of hermaphroditic genera

are congruent with sexuality and mating patterns (Streelman et al., 2002). The

widely varying patterns of sexual development and mating systems of wrasses

in the western North Atlantic were largely uniﬁed by Ghiselin’s size-advantage

hypothesis (Ghiselin, 1969; Warner, 1975; Warner & Robertson, 1978), and this

appears to be true for L. maximus as well. Davis (1976), Claro et al. (1989) and

the present study demonstrate that L. maximus is a monandric, protogynous

hermaphrodite. Observations of L. maximus spawning behaviour demonstrate

a polygynic mating system, although considerable variations in aggregate size

and sex ratio have been noted: Parker (2000) observed a single male courting

a single female in North Carolina; Davis (1976) observed that males occurred

alone more often than single females when densities were low, and at the other

extreme, he observed an aggregation of c. 100 L. maximus, including several

males, within a 30 m diameter area. Nonetheless, Davis (1976) and Colin (1982)

concluded that typically one male maintains a harem of up to 15 females.

Thus, according to Ghiselin’s (1969) size-advantage hypothesis, monandric pro-

togyny by L. maximus should be adaptive because a single terminal male can

monopolize a harem of several females (Warner, 1984).

These ﬁndings also have implications for the management of this ﬁshery

species. Males are larger than females, and sex change arises mostly in the

range of 300–400 L

, which is at or only slightly larger than the minimum size

limit (305 mm L

) allowed by ﬁshing regulations. Thus, in areas of high ﬁshing

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mortality, there is the potential to repeatedly remove the single, terminal male

from a spawning group of several females (McBride & Murphy, 2003). If sex

changes initiated around the end of the spawning season take several months

to complete, then there are three probable outcomes when a male is removed

from a spawning harem: (1) a new, lone male invades the undefended territory

to re-establish the harem, (2) the females disperse and join a nearby harem or

(3) the females remain in the territory until one of them changes sex and re-

establishes the harem. There are examples of lone males persisting among other

harem-spawning ﬁshes (Mun

˜oz & Warner, 2003). The existence of such ‘bach-

elor males’ or the rapid dispersal of females, however, is not documented for

L. maximus. Thus, reproduction by the entire harem may be interrupted when

a male is harvested or otherwise dies, seriously reducing reproductive output

(i.e. up to 15 remaining females stop spawning, at least temporarily). A further

option may be: a female within the harem changes sex and spawning resumes

the following year. If this female is the largest (and most fecund) female, then

the reproductive output of the harem may actually decline as a function of the

size-fecundity relationship of the remaining females; if this new male is har-

vested again and again, then this would serve as a mechanism to serially reduce

reproductive output of a harem. Future behavioural research of L. maximus’s

spawning harems, particularly in response to instances where a terminal male

is removed, is necessary to examine this process and its application for manage-

ment of this valuable, but vulnerable, ﬁshery species.

Samples were obtained with the assistance of L. Bullock, J. Colvocoresses, D. DeMaria,

K. DeMaria, T. Dunmire, J. Hunt, M. Larkin, D. Merryman, D. Murie, D. Snodgrass,

P. Steele and J. Styer. P. Nagle, C. Plybon, F. Stengard and P. Thurman assisted in the

laboratory. R. Ruiz-Carus assisted in translation of Cuban hogﬁsh research. A. Collins

and J. Colvocoresses provided helpful comments to improve the manuscript. Funding

for sampling and life-history research was provided by Marine Fisheries Initiative

[MARFIN, National Oceanic and Atmospheric Administration (NOAA)] Grant No.

NA87FF0422. Collections were also made as part of sampling funded by Florida

Saltwater Fishing License sales, as well as by award NA36FI0125 from NOAA to the

Florida Department of Natural Resources. Administration of this latter award and its

study products was subsequently transferred to the Florida Department of Environment

Protection and then to the Florida Fish and Wildlife Conservation Commission. The

statements, ﬁndings, conclusions and recommendations are those of the authors and

do not necessarily reﬂect the views of the Department of Commerce or NOAA or any

of its subagencies. We are grateful for everyone’s help in this study.

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Length-Based Spawning Potential Ratio (LB-SPR) for Red Grouper (Epinephelus morio) and Associated Species in the Commercial Fishery of the Yucatan Peninsula, Mexico

Article

Full-text available

Apr 2024
J APPL ICHTHYOL

The study calculated the Length-Based Spawning Potential Ratio (LB-SPR) for several species, including red grouper (Epinephelus morio), black grouper (Mycteroperca bonaci), gag grouper (M. microlepis), yellowtail snapper (Ocyurus chrysurus), lane snapper (Lutjanus synagris), hogfish (Lachnolaimus maximus), and white grunt (Haemulon plumierii). Data were obtained from the small-scale commercial fleet operating in the red grouper fishery on the Campeche Bank within the Yucatan Peninsula. Monthly records of total length (cm) from April 2017 to May 2018, totaling 10,182 fish, were collected from five fishing ports along the Yucatan Peninsula coast. Biological data, such as growth and reproductive patterns and exploitation parameters were gathered from scientific literature. The LB-SPR package on the R Core Team platform was utilized for analysis. Despite being the largest, groupers exhibited immaturity (SL50 < L50) and low Spawning Potential Ratio (SPR). Red and black groupers showed particularly low SPR values (0.10 and 0.05, respectively), indicating a looming risk of local extinction. The gag grouper achieved the highest SPR value (0.26) among groupers, although it was very close to the minimum critical value (i.e., 0.20). Snappers, hogfish, and white grunt were generally captured in the adult state (SL50 > L50). Yellowtail, hogfish, and white grunt displayed high SPR values (0.44, 0.72, and 0.98, respectively). Lane snapper had a low SPR (0.28) but fell within the range for maintaining satisfactory stock productivity, albeit with reduced yields. The findings emphasize the urgent need to adjust the current management framework for the red grouper fishery, focusing on improving fishing gear selectivity to address heightened pressure on both juvenile groupers and adult lane snapper. Implementing these measures is crucial to mitigate the risks of local extinction and population decline for each species.

Life history of the endemic Hawaiian hogfish Bodianus albotaeniatus: age, growth and reproduction

Article

Full-text available

May 2023
J FISH BIOL

Growth rate, longevity, maturity and spawning seasonality were estimated for the endemic Hawaiian hogfish Bodianus albotaeniatus. The sex‐specific von Bertalanffy growth parameters are L∞ = 339 mm fork length (LF) and K = 0.66 year⁻¹ for females and L∞ = 417 mm LF and K = 0.33 year⁻¹ for males. The maximum age is 22 years. Histological gonad analysis and the absence of small and young males indicate a monandric protogynous hermaphrodite. Size and age at maturity for combined sexes are L50 = 238 mm LF and A50 = 1.6 years.

A unified framework and terminology for reproductive traits integral to understanding fish population productivity

Article

Full-text available

Dec 2023

Objective This paper highlights the complexity of marine fish spawner–recruit systems and how they vary across species and ecosystems while providing a universal terminology and framework to evaluate fish reproduction. We emphasize the gonadal development important to assess maturity, fecundity, where and when fish spawn, and transition and sex assignment in protogynous species. Methods We review and compare reproductive traits in warmwater and coldwater fishes. Reproductive phases for both sexes and protogynous species are defined and histological micrographs presented. New methods are developed to assess maturity; spawning seasonality; peak spawning; and, for protogynous species, sex assignment. Result Protogyny, extended spawning seasons, and indeterminate fecundity are more common in warmwater than coldwater systems. The following reproductive phases are defined as immature, transitional (sex change), early developing (the first stage of entrainment in the reproductive cycle), late developing (stages needed to complete maturational competence), spawning, regressing (spawning season termination), and regenerating (fish that are mature but outside of the spawning season). A method to assess the certainty of maturity assignment based on reproductive phase and the age and size range sampled is presented, as are best practices to estimate size and age at maturity. To remove the subjectivity from current methods to estimate spawning seasonality, we present a new quantitative method to identify the core spawning season and peak spawning months. Conclusion A species’ ability to adapt to fishing and climate change varies with their reproductive strategy. Improving our understanding of fish reproduction necessitates standardizing methodology and terminology.

Dynamic light filtering over dermal opsin as a sensory feedback system in fish color change

Article

Full-text available

Aug 2023

Dynamic color change has evolved multiple times, with a physiological basis that has been repeatedly linked to dermal photoreception via the study of excised skin preparations. Despite the widespread prevalence of dermal photoreception, both its physiology and its function in regulating color change remain poorly understood. By examining the morphology, physiology, and optics of dermal photoreception in hogfish (Lachnolaimus maximus), we describe a cellular mechanism in which chromatophore pigment activity (i.e., dispersion and aggregation) alters the transmitted light striking SWS1 receptors in the skin. When dispersed, chromatophore pigment selectively absorbs the short-wavelength light required to activate the skin’s SWS1 opsin, which we localized to a morphologically specialized population of putative dermal photoreceptors. As SWS1 is nested beneath chromatophores and thus subject to light changes from pigment activity, one possible function of dermal photoreception in hogfish is to monitor chromatophores to detect information about color change performance. This framework of sensory feedback provides insight into the significance of dermal photoreception among color-changing animals.

Life history characteristics of the protogynous hermaphroditic areolate grouper Epinephelus areolatus in Kagoshima Bay, southern Japan

Article

Full-text available

May 2023
ENVIRON BIOL FISH

Epinephelus areolatus is a commercially important small-sized grouper widely distributed in the Indo-Pacific region. Its age, growth, and reproductive biology were studied in Kagoshima Bay, southern Japan. The maximum size and age were 494 mm total length (TL) and 19 years, respectively. The von Bertalanffy growth parameters were estimated as follows: L∞ = 456.4 mm TL, K = 0.334 year⁻¹, and t0 = − 0.553 year. The size and age at 50% female maturity were estimated to be 300 mm TL and 2.9 years, respectively. This species grows faster and attains sexual maturity earlier than other small-sized Epinephelus species inhabiting Japanese coastal waters. The sex ratio was significantly biased toward females (male:female = 1:6.6; P < 0.001). Males (410 ± 55.7 mm TL, 7.8 years) were significantly larger and older than females (268 ± 70.8 mm TL, 2.2 years) (size and age, P < 0.001). The size and age at 50% sex change were 412 mm TL and 5.6 years, respectively. Bisexual-phase gonads were observed in individuals that did not first reach sexual maturity as females, suggesting that all juveniles develop an ovarian phase first and then enter a bisexual-phase gonad. These results strongly suggest that E. areolatus exhibits monandric protogynous hermaphroditism, but primary males may also exist. We determined that active spawning occurred between July and September. Transitional individuals occurred over a prolonged period regardless of the spawning season.

Habitat specific trade-offs in growth and survival by hogfish Lachnolaimus maximus in southeast Florida

Article

Jul 2021
B MAR SCI

The hogfish Lachnolaimus maximus , an economically important, reef-associated protogynous teleost, has gained additional interest from fisheries managers due to evidence of overfishing in the southeastern United States. This study collected data on age and growth of hogfish in southeast Florida (SEFL), an understudied part of the species’ range. Hogfish ( n = 227) were collected from three reef tracts at different depths between January 2016 and August 2017. The average maximum potential length ( L ∞) was 414 mm overall and showed evidence of Lee’s Phenomenon occurring relative to the eastern Gulf of Mexico, an area of presumed lower fishing pressure, where L ∞ was 920 mm. Hogfish growth was also found to vary significantly by reef location in SEFL. Otolith-based aging revealed that SEFL hogfish growth past age 3 significantly decreased as reef depth increased between the three reef tracts [length at age 9 ( L 9 ) = 564, 405, 351 mm FL]. By L 9 , hogfish from the shallowest reef tract (4–6 m) were on average 61% longer and four times the weight of individuals collected from the deepest reef tract (15–25 m). Annual survival also increased with depth (42%, 65%, 73%), with a linear relationship to growth at L 9 where R ² = 1.0, indicating there are inherent trade-offs between growth and longevity in hogfish of southeast Florida.

Latitudinal variation in the demography and life history of a temperate marine herbivorous fish Odax pullus (Labridae)

Thesis

Full-text available

Jan 2009

Elizabeth D. L. Trip

This thesis examined latitudinal variation in the demography and life history of a temperate marine herbivorous fish, Odax pullus (Labridae). Over 1000 individuals were collected at six locations across ~13 o of latitude, and an age-based approach was used to establish the patterns of variation in growth rate, size-at-age, development rate (size-and age-at-maturity and-at-sex change), life span, and rate of physiological ageing. Firstly, an otolith-based ageing procedure was developed following successful validation of the daily and annual periodicity of opaque zone formation, and histological analysis of the reproductive biology of O. pullus was combined with sex-specific demographic information to establish a diagnosis of monandric protogynous sex change. Secondly, a "biota-environment linkage" approach was used to explore the patterns of geographic variation in life history and the effects of potential underlying environmental factors (sea surface temperature, species density, habitat and food availability, exposure, and extrinsic mortality). Significant latitudinal trends in growth, body size, development, and longevity were identified along a broad North-South gradient, with individuals growing slower, maturing and changing sex later, achieving larger body sizes and living longer at higher latitudes. The main effects of latitude on the phenotypic response of life histories were related to the latitudinal gradient in environmental temperature. Species density and habitat (food) availability also affected the responses in body size and development, and these effects were detected on a local spatial scale. Comparison with a temperate carnivorous labrid, Notolabrus fucicola, revealed no differences in the response of growth, body size, development and life span to temperature in the two species with contrasting diets, thus providing no support for the hypothesis of a temperature constraint on herbivory at high latitudes in O. pullus. Lastly, the processes underlying latitudinal changes in life span were investigated in the context of the oxidative stress hypothesis of ageing and of the predictions of the Metabolic Theory of Ecology, and the age-pigment neurolipofuscin was quantified in older O. pullus individuals to assess the rate of oxidative damage accumulation across latitudes. Neurolipofuscin accumulation rate increased with temperature, indicating that a slower rate of ageing contributed to greater life expectancies at colder temperatures. iii Acknowledgements

Protogyny in Fishes

Chapter

Dec 2022

Yoichi Sakai

Of approximately 480 hermaphroditic fish species, over 300 have been confirmed to undergo protogynous (female-to-male) sex changes. The occurrence of protogyny is strongly related to polygynous mating systems and follows the prediction of the size-advantage model based on the concept of life history strategies that maximize lifetime reproductive success. Sex change in females often occurs in a situation where females become dominant after the disappearance of dominant males in the local group. However, females are also observed to change their sex even in the presence of a dominant male (i.e., bachelor sex change and harem-fission sex change). Female tactics associated with sex change, for example, intergroup movement to improve the social condition and fast growth at the expense of spawning, are also known. This chapter introduces the results of widely studied protogynous sex changes in fish hermaphroditism and focuses on functional contexts and individual-level social mechanisms.KeywordsBachelor sex changeDiandry and monandryHarem-fission sex changeMating systemsSex change processSocial control

Database of Hermaphroditic Fish Species and References

Chapter

Dec 2022

This chapter provides a database of hermaphroditic fishes and references. The database includes, for each species, the type of hermaphroditism, method of confirmation (evidence), mating system, habitat, references, and remarks. Kuwamura et al. (2020) reported 461 species as functional hermaphroditic fishes; 21 species were added, and one species was deleted in this database.KeywordsBidirectional sex changeFunctional hermaphroditismProtandryProtogynyReversed sex changeSimultaneous hermaphroditismTeleost fish

Commercial species of artisanal fishing in the Yucatan Peninsula

Book

Full-text available

Oct 2021

La pesca es la única actividad del sector productivo primario donde no hay incentivos para incrementar la capacidad de producción, esto es, se depende de la capacidad natural de producción de las poblaciones silvestres. Esto significa que hay un límite para la producción, y por lo mismo riesgos de agotamiento si no hay controles. Esto es lo que hace necesario delinear esquemas de ordenamiento orientados a la sostenibilidad no solo de la producción sino socioeconómica, entendiendo siempre que la gestión está orientada en beneficio del usuario, incluida la conservación. Uno de los principales problemas de la pesca artesanal es la falta de información, y por lo tanto de conocimiento, para soportar científicamente el ordenamiento y la toma de decisiones. Es también evidente que muy pocas de las especies objetivo de la pesca artesanal son de alto valor económico; y menos aún, el sostén de una actividad a nivel industrial. Las razones de esto último son variadas pero tal vez la principal sea la riqueza específica propia de nuestros ecosistemas; lo cual, desde el punto de vista industrial, significa una materia prima altamente heterogénea. Estas condiciones conducen a un bajo financiamiento de la ciencia aplicada a generar el conocimiento necesario. Este es un fenómeno de escala mundial dada la naturaleza de la actividad, pero se reconoce la importancia de abordar esta problemática por la gran cantidad de personas que dependen directa e indirectamente de la pesca artesanal. Actualmente la ciencia pesquera ha mostrado gran preocupación e interés en esta condición evidenciado por la gran cantidad de investigación generada hacia la última década definida como evaluación del estado de los recursos pesqueros en condiciones de limitada disponibilidad de datos e información. Esto es, dado que son típicamente recursos donde no hay monitoreo consistente y se genera muy poca información biológico-pesquera, la ciencia está intentando abordar la generación de conocimiento robusto y consistente para soportar el ordenamiento con la poca información disponible. Este último aspecto es donde surge la importancia de la presente obra sobre “Especies Comerciales de la Pesca Artesanal en la península de Yucatán”, contribuye que la brecha sobre la limitación o ausencia de datos hacia el conocimiento de los recursos pesqueros se reduzca considerablemente. Cabe destacar en este sentido que los datos aportados en cada ficha son la base para la aplicación de muchos de los métodos para estimar parámetros e información necesaria para el análisis de la dinámica de poblaciones y evaluación de las pesquerías; lo cual, en conjunto con el contenido de información en cada ficha, permitirá, en un futuro próximo, tener una muy buena idea del estado de explotación de los recursos pesqueros de la Península de Yucatán, y generar pautas informadas para el ordenamiento de la pesca. Felicito a Julia, Miguel Ángel, Silvia, Jorge y Domingo por esta iniciativa y, como mencioné en un inicio, por el grupo de trabajo que han conformado, no sólo por su capacidad científica, sino porque contagian su entusiasmo, pasión y forma de colaboración a terceros. Seguramente esta conjunción de situaciones motivará un mayor número de contribuciones para beneficio del sector pesquero y la academia.

Current and potential yield per recruit of hogfish, Lachnolaimus maximus, in Florida.

Conference Paper

Jan 2003

Hogfish (Lachnolaimus maximus) is a valuable fishery species that lives on reefs of the Gulf of Mexico, Caribbean Sea, and Atlantic Ocean north to the Carolinas. In Florida, hogfish landings have been declining in recent years. Moreover, maximum size of hogfish landed in south Florida, where landings are greatest, is only half the maximum size of those landed in the eastern Gulf of Mexico. These trends in landings and fish size suggest continuing problems for the fishery. In this paper we explore some of the costs and benefits of increasing the minimum legal size at which hogfish can be captured in order to increase the yield per recruit of hogfish. We also comment on the potential additional benefit, in terms of increased recruitment, that could result from this management option.

Methods of assessing ovarian development in fishes: A review

Article

Jan 1990

G. West

Spawning and larval development of the hogfish, Lachnolaimus maximus (Pisces: Labridae)

Article

Jan 1982

Patrick L Colin

A list of fishes of Alligator Reef, Florida with comments on the nature of the Florida reef fish fauna

Article

Jan 1968

W.A. Starck

Systematic catalogue of the fishes of Tortugas, Florida

Article

Intersexuality in fishes

Article

R. Reinboth

Spontaneous and hormone-induced sex-inversion in wrasses (Labridae)

Article

Jan 1975

R. Reinboth

An annotated checklist of the species of the Labroid fish families Labridae and Scaridae

Article

Jan 2000

Changes in the sex ratio and size at maturity of gag, Mycteroperca microlepis, from the Atlantic coast of the southeastern United States during 1976-1995

Article

Oct 1998
FISH B-NOAA

Gag, Mycteroperca microlepis, is a large, slow-growing, protogynous grouper that probably makes annual migrations to specific locations to aggregate for spawning. During 1976-82, male gag constituted 19.6% of the sexually mature individuals taken during fishery-dependent and fishery-independent sampling along the southeast coast of the United States. A similar percentage of males was found in the Gulf of Mexico from 1977 to 1980; however, males made up only 1.9% of the population in the Gulf of Mexico during 1992. To assess the current sex ratio of gag along the southeast U.S. coast, an emergency rule was enacted by the Department of Commerce in January 1995 that required commercial vessels from North Carolina to southeast Florida to land gag with gonads intact. Histological examination of 2613 gonads of sexually mature gag collected from 18 January through 18 April 1995 revealed that 5.5% of the gag from the southeast Atlantic were male. There was a weak trend indicating that females reached maturity at a smaller size in 1994-95 than in 1976-82. Very few transitional specimens were collected during the spawning season. Most transitional individuals (79%) were taken during April through June immediately after the 1995 spawning season. Gag in spawning condition were landed during December through mid-May by fishermen working offshore from North Carolina to southeast Florida. In addition, gag in spawning condition were taken during research cruises documenting the occurrence of spawning north of Florida (off South Carolina and Georgia at depths ranging from 49 to 91 m).

The Ecological Context of Reproductive Behavior

Chapter

Dec 2002

This chapter focuses on the reproductive behavior of coral reef fishes. Over the past 20 years, population-level studies of coral reef fishes have shifted from simple comparisons between coral reefs and terrestrial systems, to the patterns unique to marine and coral reef communities. This shift in attention of coral reef ecologists is reflected in the development of marine ecological theory that currently emphasizes the dynamics of open populations and the sources of recruitment fluctuations, including the possibility of recruitment limitation on population size. Coral reef fishes add some interesting variations and confirmations to the basic rules of mating systems as there can be dramatic differences within species from place to place because of changes in resource distribution and population density, and individuals often have the option of changing sex or sexual allocation over the course of their lives. One of the first generalizations to come out of studies in behavioral ecology of reef fishes was the importance of local density in determining mating systems. It demonstrated the importance of density in spawning site defense by individual males, and the switch from monogamous to more polygynous mating systems with increasing density. Population density also appears to interact with female spawning locations, especially whether females migrate to spawn or spawn within feeding territories. For small reef fishes that free-spawn (release pelagic eggs), two general patterns emerge. For many species, individuals migrate daily to the downcurrent edge of the reef to spawn for a limited time, determined by tide, time of day, or both. For some species, especially on patch reefs, if the number of individuals is relatively small, this group operates as a harem, with one dominant male and a group of females. Moreover, in families capable of hermaphroditism, protogyny—sex change from female to male—is often observed.

Sexual development and reproductive seasonality of hogfish (Labridae: Lachnolaimus maximus), an hermaphroditic reef fish

Abstract

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