Lectures 9 & 10: Reproductive Biology and Behavior in fish Biology 450: Fish Week Lectures 9 & 10: Reproductive Biology and Behavior in fish Scott Heppell Department of Fisheries and Wildlife Oregon State University 042 Nash Hall 737-1086, Scott.Heppell@oregonstate.edu

Fish Reproduction

The H-P-G axis Hypothalamus GnRH PIT GTH I/GTH II Testis Ovary Sex steroids

The HPG Feedback loops

Steroid biosynthesis

Hormonal control of oocyte maturation

Stages of maturation STAGE DESCRIPTION COMMENTS Stage 0 Immature Not capable of producing viable gametes Stage 1 Primary growth Resting or recently mature Stage 2 Secondary growth Vitellogenin independent, cortical alveoli present Stage 3 Early vitellogenesis Vitellogenin granules present, oocyte increasing in diameter Stage 4 Late vitellogenesis Strong presence of vitellogenin in oocyte, gametes approaching maximum pre-spawning diameter Stage 5 Mature/spawning/ Running ripe Hydrated oocytes, final maturation of gametes Stage 6 Spent High rates of atresia, gonad loosely organized

Stages of gonad maturation (female) Heppell and Sullivan FP&B 1999

The two-cell model

Vitellogenesis Hypothalamus GnRH PIT GTH I Ovary Vitellogenin Liver Estradiol Vitellogenin GTH I GnRH

Female final maturation

The female hormonal cycle

Water hardening

Hormonal control of sperm maturation

The male hormonal cycle

Male reproductive development

Quirks in reproductive assessment

Maternal effects Bobko and Berkeley 2004

Maternal effects Bobko and Berkeley 2004

Maternal effects Berkeley et al 2004

Maternal effects Berkeley et al 2004

Male mating strategies Group spawning –Sperm competitors Territoriality –Mate competitors Leks Nest guarding Sneaker, streakers, and satellite spawners

Nest guarding –Lingcod

Phase shifts in male reproductive tactics Immature Mature ♀ ♂ ♀ ♂ ♂ Initial phase Immature ♂ Initial phase ♂ Terminal phase ♂

♂ Initial phase Immature ♂ Initial phase ♂ Terminal phase ♂

Group spawning

Group spawning

Territoriality

Territoriality

Sex change

Types of hermaphroditism Protogyny- Female first Protandry –Male first Simultaneous –Can spawn as both at the same time

♂/♀ ♂ ♀ ♂/♀ Sex change patterns ♀ ♂ U Immature Mature Immature Mature

Social control of sex change

Social control of sex change Warner and Swearer (1991) Behaviors exhibited within minutes Color changes within a day Mature sperm within 8 days Semsar, Godwin, Grober, Bass Linked to Arginine Vasotosin production in the brain Not necessarily linked to gonad production of steroids Warner and Swearer 1991

Marlin explains to Nemo the sociological aspects of sexuality and parental role patterns within the context of the identity model for transgender and intersex inclusion

Sex ratio = 1:1 female:male

Sex ratio = 1.5:1 female:male

Sex ratio = 1:1 female:male

Sex ratio = 13:1 female:male

Department of Fisheries and Wildlife Oregon State University Behavior, physiology, and life history comparisons in four species of grouper: What do they mean for grouper management? Scott A. Heppell Department of Fisheries and Wildlife Oregon State University

Marine fisheries ecology at multiple scales of biological organization Grand unifying theory Molecule Cell Physiology Behavior Individual fitness Populations Species Communities Habitats Ecosystems Integration Management

Male reproductive tactics, disruption of mating strategies, and “The Challenge Hypothesis” Multiple strategies for reproductive success Primary/territorial males Aggressive High androgen levels Small testes Secondary males (Sneakers, streakers, and satellite males) Non-aggressive Low androgen levels Large testes Also the tactic of group spawners The challenge hypothesis (Wingfield 1984) Territoriality Aggression Mate competition Hormone positive feedback loops

Environmental input Behavioral interaction Sensory transduction Testis GTH Behavioral interaction Sensory transduction brain 11KT + Gene regulation Behavior Environmental input

A tale of four groupers

Male grouper reproductive life history analysis Collect gonad and plasma samples from males of three different species of grouper (Nassau, red hind, and gag, with an extant dataset for red grouper) Confirm stage of maturation w/histology Measure androgens (Testosterone, 11-ketotestosterone) Evaluate general patterns of androgens, sex ratio, gonadosomatic index, and spawning strategy to determine general life history patterns –identify implications for population level effects

Non-territorial, group Spawning strategy Species Spawning strategy Agg. size E. striatus Non-territorial, group 1,000-10,000's E. guttatus Territorial, pair 100-1000’s E. morio 10's+ M. microlepis

Gonadosomatic index Species GSI Reference E. striatus 9.4 Tucker et al. 1993 (from figure) 10 Sadovy and Colin 1995 E. guttatus 0.66 Sadovy et al. 1994 E. morio 0.38 Alan Collins, unpublished 0.3 Johnson 1995 M. Microlepis 1.83 Hood and Schleider 1992   0.56 Collins et al. 1998

Sex ratio Species Sex ratio (M:F) Location Source E. striatus ~2:1 to 1-1.4 Various Caribbean Sadovy and Colin 1995 E. guttatus 1:4 to 1:115 Puerto Rico Sadovy et al. 1994 1:4 to 1:8 Shapiro et al. 1993a E. morio 1:2 to 1:6 NE Gulf of Mexico Coleman et al. 1996 M. microlepis 1:5 to 1:76 Collins et al. 1998

Role of androgens in male reproduction Testosterone 11-ketotestosterone Sex differentiation and development Stimulates the pituitary to induce spermatogenesis Precursor to E2 and KT Territoriality Nest building Aggression Secondary sex characteristics Spermatogenesis and sperm maturation Tactic switching

Testosterone ANOVA p = 0.23 A A A A

11-ketotestosterone (Belize) ANOVA p <0.0001 Tukey HSD A B B B

11-ketotestosterone (Cayman) ANOVA p <0.0001 Tukey HSD A B B B

T:KT ratio (pooled samples) ANOVA p <0.001 LSD test A A A/B B

Environmental input Behavioral interaction Sensory transduction Testis GTH Behavioral interaction Sensory transduction brain 11KT + Gene regulation Behavior Environmental input

Decreased Individual Reproductive Success Population level Environmental input Behavioral interaction Decreased Individual Reproductive Success Sensory transduction Gene regulation Behavior + brain Population level (Allee) effects? Down-regulated GTH Testis + 11KT

Conclusions Anatomy, behavior, and physiology, correlate with spawning strategy across four species of grouper This work presents a possible mechanism for depensation, at least in territorial species A wider variety of species should be investigated to see whether it holds true across the majority of grouper species For some species we should manage for sex ratio as well as overall spawning stock biomass Critical minimum population sizes may be necessary for patterned behaviors and effective spawning Assessing biological/resource issues across multiple scales of biological organization is important