Heppell, S.A.

Aquatic Commons

 INTRODUCTION 
Groupers (Family Serranidae) of the southeast United 
States and Caribbean exhibit an array of reproductive 
strategies, from pair-spawning while in small aggregations 
of a few individuals to mass spawning in groups of tens of 
thousands, at least historically (Smith 1972, Colin et al. 
1987, Gilmore and Jones 1992, Sadovy et al. 1994, Cole-
man et al. 1996).   Group spawning groupers tend to be 
non-aggressive (while spawning), while pair-spawning 
species court females and defend territories against other 
males.  More generally this reflects a sperm competition 
vs. mate competition life history strategy.  The majority of 
grouper species studied have also been shown to be proto-
gynous hermaphrodites.  This means that there is a natural 
skew to sex ratio, with females being the dominant sex. 
Reproductive strategy is reflected in relative testes size 
(gonadosomatic index, GSI). Males with high GSI tend to 
be the non-territorial and non-aggressive type, while males 
with low GSI are often territorial and aggressive.  This 
relationship is seen across a wide range of vertebrate spe-
cies (Harcourt et al. 1981; Cardwell and Liley 1991; Ku-
Behavior, Physiology, and Life History Comparisons in Four Species of Grouper: What do they 
mean for Grouper Management? 
 
SELINA, A. HEPPELL 
Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University, Corvallis, OR, 97330 USA, (541) 737-1086 
phone, (541) 737-3590 FAX, Scott.Heppell@oregonstate.edu 
 
ABSTRACT 
The objective of this study was to conduct a preliminary investigation of the interplay between reproductive behavior 
and spawning strategy in territorial (E. morio, E. guttatus, and M. microlepis) and non-territorial (E. striatus) grouper spe-
cies.  Non-territorial males tend to have high gonadosomatic index (GSI) and are sperm competitors, while territorial males 
tend to have low GSI's and are resource (mate) competitors.  Epinephelus striatus has a substantially higher GSI than the 
other three species, indicating its strategy as a sperm competitor.  The physiology/anatomy/behavior relationship has been 
shown elsewhere between males within a species, but has not before been described across related species in which each 
species exhibits only one reproductive type.  This relationship becomes important when we consider decreased overall male 
densities and associated skews of sex ratio in some groupers.  This may lead to a disruption of the positive feedback loops 
and a physiological explanation for depensation/Allee affects in certain grouper species. 
 
KEYWORDS: grouper, reproduction, physiology, life history, depensation 
 
Comparaciones de Comportamiento, Fisiología, e Historia de Vida entre Cuatro Especies de 
“meros”: ¿Cuál es su significado para manejo? 
 
El objetivo de este estudio fue el de conducir una investigación preliminar sobre la interacción entre el comportamiento 
reproductivo y las estrategias de desove en especies de meros territoriales (E. morio, E. guttatus, y M. microlepis) y no-
territoriales (E. striatus). Los machos no-territoriales tienden a tener un alto índice gonadosomático (IGS) y son competido-
res de esperma, mientras que los machos territoriales tienden a tener un bajo IGS y compiten (se aparean) por recursos. E. 
striatus tiene un IGS sustancialemente más alto que las otras tres especies, lo que demuestra su estrategia como competidor 
de esperma. La relación entre fisiología / anatomía / comportamiento ha sido demostrada otras veces entre machos de una 
misma especie, pero hasta ahora no ha sido descrita entre especies relacionadas, donde cada especie presenta únicamente un 
tipo de reproducción. Esta relación es importante cuando se consideran disminuciones en las densidades totales e inclinacio-
nes asociadas a la proporción sexual en algunos meros. Esto puede llevar a la disrupción del circuito de refuerzos positivos, 
y a una explicación fisiológica de los efectos de decompensación /Allée en ciertas especies de meros. 
 
PALABRAS CLAVES: mero, reproducción, fisiología, historia de vida,  decompensación.   
sano et al. 1991; Jennions and Passimore 1993; Harcourt et 
al. 1995). 
Androgens, primarily testosterone and its derivatives, 
play a key role in these behaviors.  In addition to stimulat-
ing the proliferation and maturation of gametes and the 
development of secondary sexual characteristics, andro-
gens induce various reproductive behaviors including terri-
torial displays and aggressive interactions (reviewed in 
Borg 1994).  The trend is for androgen levels in territorial 
and aggressive males to be elevated above those in males 
that are subordinate or non-territorial.  According to the 
challenge hypothesis (Wingfield 1984), dominant males 
experience positive feedback in the form of increased an-
drogen levels upon successful defense of a territory.  This 
positive feedback loop may be necessary for complete re-
productive success in males. 
Problems may arise when the natural spawning struc-
ture is disrupted through fishing.  In addition to potential 
direct disruption of behavior on the aggregation, loss of 
males through compression of age structure (Huntsman and 
Schaaf 1992, Heppell et al. 2006) may result in a decrease 
Page 172  59th Gulf and Caribbean Fisheries Institute  
 
in circulating androgen levels, a change in behavior, and a 
decrease in sperm production levels or quality. This would 
then indirectly impact reproductive success and the long 
term productivity of the population. 
The objective of this study was to conduct a prelimi-
nary comparative analysis of life history, spawning behav-
ior, morphology and physiology across four species of 
grouper.  Results are considered in light of similar correla-
tions seen in other fish species and in terms of the implica-
tions spawning life history strategy might have on the vul-
nerability to overexploitation of different grouper species.  
This work follows on modeling efforts to explore the im-
pact of fishing on protogynous species and evaluation of 
potential management strategies for sex ratio recovery 
(Heppell et al. 2006). 
 
METHODS 
Samples (blood and gonad) from male gag 
(Mycteroperca microlepis) were collected between Decem-
ber 1995 and March 1996 between Jacksonville, FL and 
Cape Canaveral, FL.  Nassau grouper (Epinephelus stria-
tus) and red hind (E. guttatus) samples were collected in 
early February, 1996 near the spawning aggregation on 
Glover's Reef, Belize.  All samples were collected from 
fish caught in the course of commercial fishing operations. 
Androgen and gonadosomatic index (GSI) data for red 
grouper (E. morio) were taken from Johnson (1995). 
Gonads were fixed, embedded, and then sectioned on a 
rotary microtome.  Sections were H&E stained, and staged 
at 100X magnification on a light microscope (Jackson and 
Sullivan 1995; Heppell and Sullivan 2000). 
Blood was collected to measure circulating levels of 
androgens. Testosterone (T) and 11-ketotestosterone 
(11KT) were determined following the protocols of Woods 
and Sullivan (1993) and Heppell and Sullivan (2000).  Data 
were analyzed by ANOVA followed by Tukey's Honest 
Significant Difference (HSD) Test at an alpha level of 
0.05. 
Published data on gonadosomatic index, spawning 
style, and sex ratio were assembled from the literature and 
author observations.  
 
RESULTS 
Males of all four species were at similar stages of go-
nadal development (data not shown).  Plasma T levels 
showed a significant difference between the four species 
(ANOVA p < 0.05), and further analysis showed a slight 
elevation in T for E. guttatus relative to E. striatus (p < 
0.05), but no significant differences were seen between the 
other species.  Levels of 11KT also showed a significant 
difference among means between the four species (p < 
0.05).  11-ketotestosterone levels were significantly lower 
in E. striatus than in the other three species (p < 0.05, Fig-
ure), but there were no differences in 11KT levels between 
the latter three species (p>0.05). 
Gonadosomatic indices (from published data) demon-
strate that E. striatus has substantially larger testes than the 
other three species (Hood and Schleider 1992, Tucker et al. 
1993, Sadovy et al. 1994, Sadovy and Colin 1995, Johnson 
1995, Collins et al. 1998, Alan Collins, NOAA Fisheries, 
unpublished).  Epinephelus striatus is a documented group 
spawner while the other three species are territorial 
11KT
0
2
4
6
8
10
12
0 1 2 3 4
1
1
K
T
 (
n
g
/m
l)
E. striatus E. morio E. guttatus M. microlepis
1
1
K
T
 (
n
g
/m
l)
Figure 1.  11-ketotestosterone levels in four species of grouper. 
    Heppell, S.A. GCFI:59  (2007)             Page 173 
 
(Coleman et al. 1996 and references therein).  Sex ratios 
are more skewed towards females in the territorial species 
than in the group spawning E. striatus (data not shown). 
 
DISCUSSION 
Reproductive strategies evolve to maximize the repro-
ductive fitness of the individual, and comparative life his-
tory analysis shows that there is more than one strategy to 
solve the fitness equation.  Male M. microlepis defend ter-
ritories and display aggressive behavior within the confines 
of a localized spawning aggregation (Gilmore and Jones 
1992).  Male E. guttatus cluster into groups of several fe-
males and a male (Shapiro et al. 1993), and males actively 
defend territories while on the spawning aggregation 
(Colin et al. 1987).  Epinephelus morio aggregates in small 
polygynous groups (Sadovy et al. 1994).  While the data 
are less clear for E. morio (Sadovy et al. 1994, Coleman et 
al. 1996), these observations are more in line with behav-
iors for M. microlepis, and E. guttatus than for E. striatus, 
which is a non-territorial group spawning species (Sadovy 
and Eklund 1999). 
Epinephelus striatus males have substantially larger 
testes than any of the other three groupers examined here 
(Hood and Schleider 1992, Tucker et al. 1993, Sadovy et 
al. 1994, Sadovy and Colin 1995, Johnson 1995, Collins et 
al. 1998, Alan Collins, NOAA Fisheries, unpublished).  An 
increase in gonad size allows production of larger quanti-
ties of gametes, which potentially allows a male to swamp 
his competitors’ sperm in mass spawning events.  Evalua-
tion of GSI has been suggested as a means of identifying 
the occurrence of sperm competition in fish (Sadovy et al. 
1994).  On the other hand, E. guttatus, E. morio, and M. 
microlepis, all have GSI values that rarely exceed 2%, sug-
gesting sperm competition is less important for these spe-
cies.  In these three species males compete to establish and 
defend territories and therefore monopolize access to fe-
males, potentially limiting the importance of sperm compe-
tition (Taborsky 1998). 
Epinephelus striatus males have significantly lower 
levels of 11KT than male E. guttatus, E. morio, or M. mi-
crolepis, while T levels differ only between E. striatus and 
E. guttatus.  This is consistent with what has been observed 
within other species, where 11KT levels are correlated with 
male reproductive tactics in fish while the pattern of T lev-
els between male reproductive types is more variable 
(Brantley et al. 1993). 
These results demonstrate, for the first time, that the 
relationship between androgens, morphology, and male 
reproductive tactics holds between closely-related species 
with different spawning behaviors.  Epinephelus striatus, 
E. guttatus, and M. microlepis all aggregate to spawn (and 
E. morio may do so), while male E. striatus are the only 
one of the four species that do not establish or defend terri-
tories while spawning.  This difference in reproductive 
behavior is correlated with significantly elevated levels of 
11KT in the plasma of males from territorial species, and 
with substantial differences in GSI between the reproduc-
tive types. 
Finally, sex ratios differ between E. striatus and the 
other three species.  Sex ratios are naturally skewed in fa-
vor of females for E. guttatus, E. morio and M. microlepis, 
while the sex ratio in E. striatus approaches unity or skews 
slightly  towards males.  A female skew is in part a func-
tion of protogynous reproductive development in the first 
three species.  Problems arise because this female-skewed 
sex ratio can become significantly amplified in the pres-
ence of increased mortality through fishing (Huntsman and 
Schaaf. 1992, Coleman et al. 1996, Heppell et al. 2006), 
and there exists the potential for sperm limitation in these 
populations.  Furthermore, a disruption in the number (and 
therefore density) of males setting up territories on spawn-
ing aggregations may remove the androgen positive feed-
back loop because of decreased intra-specific aggressive 
interactions.  This could subsequently lead to adverse af-
fects on sperm development and maturation.  Ultimately 
this has the potential to reduce reproductive capacity below 
that which would be predicted simply based on estimates 
of spawning stock biomass. 
 
ACKNOWLEDGMENTS 
I would like to thank: C. Koenig (FSU) and personnel 
at the NMFS Panama City Laboratory, the staff of the 
WCS Glover's Reef Marine Research Station, R. Chapman 
and J. McGovern (South Carolina Marine Resources Re-
search Institute), M. Paz (Belize Department of Fisheries), 
and two commercial fishermen, J. Zazenski and V. Lloyd.  
This work was supported in part by a NMFS MARFIN 
grant to Craig Sullivan (NCSU). 
 
LITERATURE CITED 
Borg, B.  1994.  Androgens in teleost fishes.  Comparative 
Biochemistry and Physiology 109: 219-245. 
Brantley, RK, JC Wingfield, and AH Bass.  1993.  Sex 
steroid levels in Porichthys notatus, a fish with alter-
native reproductive tactics, and a review of the hormo-
nal bases for male dimorphism among teleost fishes.  
Hormones and Behavior. 27: 332-347. 
Cardwell, JR, and NR Liley.  1991.  Androgen control of 
social status in males of a wild population of stoplight 
parrotfish, Sparisoma viride (Scaridae).  Hormones 
and Behavior. 25: 1-18. 
Coleman, FC, CC Koenig, and LA Collins.  1996.  Repro-
ductive styles of shallow-water grouper 
(Pisces:Serranidae) in the eastern Gulf of Mexico and 
the consequences of fishing spawning aggregations. 
Environmental Biology of Fish 47: 129-141. 
Colin, P.  1992.  Reproduction of the Nassau grouper, Epi-
nephelus striatus (Pisces: Serranidae) and its relation-
ship to environmental conditions. Environmental Biol-
ogy of Fish 34: 357-377. 
Gilmore, RG, and RS Jones. 1992. Color variation and 
associated behavior in the Epinepheline groupers, 
Page 174  59th Gulf and Caribbean Fisheries Institute  
 
 Mycteroperca microlepis (Goode and Bean) and M. 
phenax Jordan and Swain.  Bulletin of Marine Science. 
51: 83-103. 
Harcourt, AH, A Purvis, and L Liles.  1995.  Sperm com-
petition: mating system, not breeding season, affects 
testes size of primates.  Functional Ecology 49: 468-
476. 
Harcourt, AH, PH Harvey, SG Larson, and RV Short.  
1981.  Testis weight, body weight, and breeding sys-
tem in primates.  Nature 293: 55-57. 
Heppell, SA, and CV Sullivan.  2000.  Identification of 
gender and reproductive maturity in the absence of 
gonads: muscle tissue levels of sex steroids and vitel-
logenin in gag (Mycteroperca microlepis).  Canadian 
Journal of Fisheries and Aquatic Sciences 57:148-159. 
Heppell, SS, SA Heppell, FC Coleman and CC Koenig.  
2006.  Models to compare management scenarios for a 
protogynous fish.  Ecological Applications 16: 238-
249. 
Huntsman, GR, and WE Schaaf.  1994.  Simulation of the 
impact of fishing on reproduction of a protogynous 
grouper, the graysby.  North American Journal of 
Fisheries Management 14:41-52. 
Jackson, LF, and CV Sullivan. 1995. Reproduction of 
white perch: The annual gametogenic cycle. Transac-
tions of the American Fisheries Society 124: 563-577. 
Jennions, MD, and NI Passimore.  1993.  Sperm competi-
tion in frogs: testis size and a 'sterile male' experiment 
on Chiromantis xerampelina (Rhacophoridae).  Bio-
logical Journal of the Linnean Society 50: 211-220. 
Johnson, AK 1995. Comparison of gonadal histology and 
sex steroid levels over the seasonal reproductive cycle 
of red grouper, Epinephelus morio. Master's Thesis. 
University of South Florida, St. Petersburg. 
Kusano, T, M Toda, and K Fukuyama.  1991.  Testes size 
and breeding systems in Japanese anurans with special 
reference to large testes in the treefrog, Rhacophorus 
arboreus (Amphibia: Rhacophoridae).  Behavioral 
Ecology and Sociobiology 29: 27-31. 
Sadovy, Y and AM Eklund. 1999. Synopsis of biological 
information on Epinephelus striatus (Bloch 1972), the 
Nassau grouper, and E. itajara (Lichtenstein 1822) the 
jewfish, NOAA Technical Report NMS 146, US De-
partment of Commerce. 65 pp. 
Sadovy, Y, A Rosario, and A Roman.  1994.  Reproduction 
in an aggregating grouper, the red hind, Epinephelus 
guttatus.  Environmental Biology of Fish 41: 269-286. 
Shapiro, DY, Y Sadovy, and MA McGehee.  1993.  Size, 
composition, and spatial structure of the annual 
spawning aggregation of the red hind, Epinephelus 
striatus (Pisces: Serranidae). Copeia 2: 399-406. 
Smith, CL.  1972.  A spawning aggregation of Nassau 
grouper, Epinephelus striatus (Bloch). Transactions of 
the American Fisheries Society 101: 257-261. 
Taborsky, M.  1998.  Sperm competition in fish: bourgeois 
males and parasitic spawning.  Trends in Ecology and 
Evolution. 13: 222- 
Wingfield, JC.  1984.  Environmental and endocrine con-
trol of reproduction in the song sparrow, Melospiza 
melodia. General and Comparative Endocrinology 56: 
417-424. 
Woods, LC III and CV Sullivan.  1993.  Reproduction of 
striped bass (Morone saxatilis) broodstock: monitoring 
maturation and hormonal induction of spawning.  
Journal Aquaculture and Fisheries Management 24: 
213-224. 


Behavior, physiology, and life history comparisons in four species of grouper: What do they mean for grouper management?

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Behavior, physiology, and life history comparisons in four species of grouper: What do they mean for grouper management?

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