modes

Reproductive Modes in Chondrichthyan Fishes: 

Reproductive Modes in Chondrichthyan Fishes Ashley Greenley Moss Landing Marine Laboratories

Objectives: 

Objectives Characteristics of Chondrichthyan reproduction Clarify Terminology Discuss Various Reproductive Modes Review reproductive modes of Lamnoid Sharks

Characteristics of Chondrichthyan Reproduction? : 

Characteristics of Chondrichthyan Reproduction?

Characteristics of Chondrichthyan Reproduction: 

Characteristics of Chondrichthyan Reproduction Internal fertilization

Characteristics of Chondrichthyan Reproduction: 

Characteristics of Chondrichthyan Reproduction Internal fertilization High maternal investment

Characteristics of Chondrichthyan Reproduction: 

Characteristics of Chondrichthyan Reproduction Internal fertilization High maternal investment Small numbers of relatively large young

Characteristics of Chondrichthyan Reproduction: 

Characteristics of Chondrichthyan Reproduction Internal fertilization High maternal investment Small numbers of relatively large young Oviparous (some sharks, skates, and chimaeras)

Characteristics of Chondrichthyan Reproduction: 

Characteristics of Chondrichthyan Reproduction Internal fertilization High maternal investment Small numbers of relatively large young Oviparous (some sharks, skates, and chimaeras) Viviparous (sharks and rays)

Characteristics of Chondrichthyan Reproduction: 

Characteristics of Chondrichthyan Reproduction Internal fertilization High maternal investment Small numbers of relatively large young Viviparous Oviparous Young are born or hatched as miniature versions of the adult (no larval stage)

Slide10: 

Francis and Stevens, 1999

Internal fertilization: 

Internal fertilization High maternal investment Relatively low fecundity Departs from simple oviparity Involves complex behavioural, morphological, and physiological mechanisms Contributes to the overall evolutionary success of chondrichthyans (Gelsleichter in Carrier, et. al., 2004)

Terminology: 

Terminology traditional classifications: oviparous, ovoviviparous, or viviparous species

Terminology: 

Terminology Traditional classifications: oviparous, ovoviviparous, or viviparous species But artificial distinction between viviparity and ovoviviparity

Terminology: 

Terminology traditional classifications: oviparous, ovoviviparous, or viviparous species But artificial distinction between viviparity and ovoviviparity Budker (1958) subdivided viviparous fishes into two categories: placental and aplacental.

The continuum of elasmobranch reproductive adaptations: 

The continuum of elasmobranch reproductive adaptations elasmobranchs are a diverse group spectrum of reproductive adaptations Gelsleichter, 2004; Wourms, 1977 Budker, 1958 Fetal/Maternal Dependency Range

Oviparity vs. Viviparity : 

Oviparity vs. Viviparity Depends on amount of time fertilized eggs are retained in the mother

Oviparity vs. Viviparity : 

Oviparity vs. Viviparity Depends on amount of time fertilized eggs are retained in the mother Oviparity results in smaller young than viviparity

Oviparity vs. Viviparity : 

Oviparity vs. Viviparity Depends on amount of time fertilized eggs are retained in the mother Oviparity results in smaller young than viviparity Oviparity is ancestral to viviparity (Dulvey et al., 1997)

Oviparity (egg laying): 

Oviparity (egg laying) 40% of sharks and rays (Dulvy, et al., 1997) Shark Families: Heterondontidae, Scyliorhinidae, Orectolobidae All Skates All Chimaeras

Oviparous Characteristics: 

Oviparous Characteristics relatively large eggs (Hamlett, 1999)

Oviparous Characteristics: 

Oviparous Characteristics relatively large eggs development completed outside of the mother (Hamlett, 1999)

Oviparous Characteristics: 

Oviparous Characteristics relatively large eggs development completed outside of the mother Embryo contained within durable and structurally complex shells (Hamlett, 1999)

Oviparous Characteristics: 

Oviparous Characteristics relatively large eggs development completed outside of the mother Embryo contained within durable and structurally complex shells incubation period lasting from months to over a year (Hamlett, 1999)

Oviparous Characteristics: 

Oviparous Characteristics once hatched, juvenile continues to nourish from internal yolk sac for the first few weeks after hatching (Hamlett, 1999)

Capsules: 

Capsules Photo credit: Hamlett, 1999

Capsules: 

Capsules Formation occurs in oviducal gland Photo credit: Hamlett, 1999

oviducal gland : 

oviducal gland capsule formation and sperm storage occurs

oviducal gland : 

oviducal gland capsule formation and sperm storage occurs gland located in the anterior region of the female reproductive tract

oviductal gland : 

oviductal gland capsule formation and sperm storage occurs gland located in the anterior region of the female reproductive tract forms capsules in a relatively rapid process (12-24 hours) (Hamlett,1999)

oviducal gland : 

oviducal gland capsule formation and sperm storage occurs gland located in the anterior region of the female reproductive tract forms capsules in a relatively rapid process (12-24 hours) (Hamlett,1999) almost all elasmobranchs encapsulate fertilized eggs

oviductal gland: 

oviductal gland shape of gland corresponds to size and complexity of capsules very prominent in oviparous species max size moments before ovulation

Capsules: 

Capsules formation oviposition Photo credit: Hamlett, 1999

Capsules: 

Capsules formation oviposition post-ovipostion Photo credit: Hamlett, 1999

Capsule Predators: 

Capsule Predators Other fish and sharks

Capsule Predators: 

Capsule Predators Other fish and sharks Marine mammals: elephant seals

Capsule Predators: 

Capsule Predators Other fish and sharks Marine mammals: elephant seals Sperm Whales????? Cox and Koob, 1993

Capsule Predators: 

Capsule Predators most renown predators: ferocious gastropods Cox and Koob, 1993

Capsule Predators: 

Capsule Predators most renown predators: ferocious gastropods unknown how this predation affects elasmobranch populations Cox and Koob, 1993

Capsule Predators: 

Capsule Predators most renown predators: ferocious gastropods unknown how this predation affects elasmobranch populations evolutionary pressure for intrauterine development? Cox and Koob, 1993

Viviparity (live birth): 

Viviparity (live birth) Embryo carried to term inside mother

Viviparity (live birth): 

Viviparity (live birth) Embryo carried to term inside mother More widespread than ovoparity

Viviparity (live birth): 

Viviparity (live birth) Embryo carried to term inside mother More widespread than ovoparity Evolved from prolongation of the amount of time spent inside the mother? (Carrier, et al. 2004)

Viviparity (live birth): 

Viviparity (live birth) Embryo carried to term inside mother More widespread than ovoparity Evolved from prolongation of the amount of time spent inside the mother? (Carrier, et al. 2004) Benefits: embryos protected throughout gestation Diverse modes based on amount of nutritional

Viviparity (live birth): 

Viviparity (live birth) Embryo carried to term inside mother More widespread than ovoparity Evolved from prolongation of the amount of time spent inside the mother? (Carrier, et al. 2004) Benefits: embryos protected throughout gestation Diverse modes based on amount of nutritional input from mother…

Modes of Viviparity: 

Modes of Viviparity Placental Aplacental viviparity (no placental connection with mother) aplacental yolk sac viviparity aplacental with trophonemata aplacental with oophagy and uterine cannibalism

Viviparous Capsules: 

Viviparous Capsules Oviductal gland not as prominent Fate of capsule depends on reproductive strategy -aplacental: embryo breaks capsule and completes development in utero -placental: capsule incorportated into the placenta thin capsules are an adaptation for absorbing uterine secretions

Placental Viviparity: 

Placental Viviparity 10% of extant sharks (note only sharks) Early phases embryo encapsulated and nourished by yolk Capsule reduced,… more of a filmy membrane than an egg case (altered function of the oviductal gland) Later placenta forms from where yolk sac touches uterine

Slide48: 

Hamlett, 1999

Aplacental yolk-sac viviparity: 

Aplacental yolk-sac viviparity formerly termed ovoviviparity ¼ of extant sharks

Aplacental Viviparity: 

Aplacental Viviparity Aplacental yolk sac viviparity Aplacental with trophonemata Aplacental with oophagy*

Aplacental yolk-sac viviparity: 

Aplacental yolk-sac viviparity formerly termed ovoviviparity ¼ of extant sharks dependent solely on yolk reserves

Aplacental yolk-sac viviparity: 

Aplacental yolk-sac viviparity formerly termed ovoviviparity ¼ of extant sharks dependent solely on yolk reserves Initial development in capsule

Aplacental yolk-sac viviparity: 

Aplacental yolk-sac viviparity formerly termed ovoviviparity ¼ of extant sharks dependent solely on yolk reserves Initial development in capsule Intrauterine fluid composition changes throughout gestation

Aplacental yolk-sac viviparity: 

Aplacental yolk-sac viviparity Whale shark Rhinocodon typus

Aplacental viviparity with uterine villi or trophonemata: 

Aplacental viviparity with uterine villi or trophonemata Also known as: aplacental with uterine milk

Aplacental viviparity with uterine villi or trophonemata: 

Aplacental viviparity with uterine villi or trophonemata trophonemata= elongate villi in the uterine epithelium Photo credit: Hamlett, 1999 Figure 15-10

Aplacental viviparity with trophonemata: 

Aplacental viviparity with trophonemata characteristic in rays

Aplacental viviparity with trophonemata: 

Aplacental viviparity with trophonemata characteristic in rays organically rich histotroph secreted into uterine lumen via trophonemata

Aplacental viviparity with trophonemata: 

Aplacental viviparity with trophonemata characteristic in rays organically rich histotroph secreted into uterine lumen via trophonemata Histotroph consumed by embryo or absorbed via gill filaments

Aplacental viviparity with trophonemata: 

Aplacental viviparity with trophonemata characteristic in rays organically rich histotroph secreted into uterine lumen via trophonemata Histotroph consumed by embryo or absorbed via gill filaments Enables embryos to grow to large size

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM : 

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM Oophagy: After yolk depleted, embryos rely on supply of yolk in ovulated eggs (oophagy)

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM : 

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM Oophagy: After yolk depleted, embryos rely on supply of yolk in ovulated eggs (oophagy) Characteristic of Lamnoid sharks

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM : 

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM Oophagy: After yolk depleted, embryos rely on supply of yolk in ovulated eggs (oophagy) Characteristic of Lamnoid sharks First recognized in 1907 by Swenander

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM : 

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM Oophagy: After yolk depleted, embryos rely on supply of yolk in ovulated eggs (oophagy) Characteristic of Lamnoid sharks First recognized in 1907 by Swenander Early development in capsule

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM : 

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM Oophagy: After yolk depleted, embryos rely on supply of yolk in ovulated eggs (oophagy) Characteristic of Lamnoid sharks First recognized in 1907 by Swenander Early development in capsule Embryo consumes ovulated eggs

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM : 

APLACENTAL VIVIPARITY WITH OOPHAGY AND INTRAUTERINE CANNIBALISM Oophagy: After yolk depleted, embryos rely on supply of yolk in ovulated eggs (oophagy) Characteristic of Lamnoid sharks First recognized in 1907 by Swenander Early development in capsule Embryo consumes ovulated eggs -Two months before parturition, ovulation ceases

Additional nutritional inputs in oophagous sharks: 

Additional nutritional inputs in oophagous sharks Comments about Isurus oxyrinchus Embryonic nutrition may also include egg jelly absorbed through the external gill filaments in prehatching phase Possibly uterine milk in posthatching phase Mollet, et al. 1999

Stomach Distention: 

Stomach Distention subdermal muscle layers split along the ventral midline. Stomach protrudes between the muscle layers. distinct scar remains (Francis and Stevens, 2000) theory Alopiids…

Slide69: 

Francis and Stevens, 1999

Embryonic dentition: 

Embryonic dentition dentition distinct from adult teeth Allows embryo to break capsule Allows embryo to consume eggs Allows embryo to consume siblings…

ADELPHOPHAGY : 

ADELPHOPHAGY actual intrauterine cannibalism, embryos seek and kill other siblings for nutrition

ADELPHOPHAGY : 

ADELPHOPHAGY actual intrauterine cannibalism, embryos seek and kill other siblings for nutrition After eating siblings, feeds on egg capsules with unfertilized ova…

ADELPHOPHAGY : 

ADELPHOPHAGY actual intrauterine cannibalism, embryos seek and kill other siblings for nutrition After eating siblings, feeds on egg capsules with unfertilized ova… predicted # of capsules consumed for C. taurus during gestation:1000-1700 with 17000 ova (Hamlett, 1983)

Reproductive modes in Lamniformes: 

Reproductive modes in Lamniformes R. G. Gilmore states “It is likely that all lamnoid sharks are oophagous yet not necessarily embryophagous.” (Gilmore, 1993)

Reproductive modes in Lamniformes: 

Reproductive modes in Lamniformes R. G. Gilmore states “It is likely that all lamnoid sharks are oophagous yet not necessarily embryophagous.” (Gilmore, 1993) Embryonic cannibalism (adelphophagy) documented in Carcharias taurus

Reproductive modes in Lamniformes: 

Reproductive modes in Lamniformes More species exhibiting adelphophagy?

http://www.elasmo-research.org/education/topics/lh_intrauterine_cannibalism.htm: 

http://www.elasmo-research.org/education/topics/lh_intrauterine_cannibalism.htm Order Orectolobiformes Family Ginglymostomatidae Tawny Nurse Shark (Nebrius ferrigineus) Order Lamniformes Family Carchariidae Sandtiger Shark (Carcharias taurus) Family Pseudocarchariidae Crocodile Shark (Pseudocarcharias kamoharai) Family Alopiidae Pelagic Thresher Shark (Alopias pelagicus) Bigeye Thresher Shark (Alopias suprciliosus) Common Thresher Shark (Alopias vulpinus) Family Cetorhinidae Basking Shark (Cetorhinus maximus) Family Lamnidae Salmon Shark (Lamna ditropis) Porbeagle (Lamna nasus) White Shark (Carcharodon carcharias) Shortfin Mako (Isurus oxyrinchus) Longfin Mako (Isurus paucus) Order Carcharhiniformes Family Pseudotriakidae Slender Smoothhound Shark (Gollum attenuatus) False Catshark (Pseudotriakis microdon) “list of all sharks in which intrauterine cannibalism has been documented, or for which exists strong circumstantial evidence”:

evidence for adelphophagy : 

evidence for adelphophagy only one surviving embryo at parturition

evidence for adelphophagy : 

evidence for adelphophagy only one surviving embryo at parturition presence of functional erect embryonic teeth

evidence for adelphophagy : 

evidence for adelphophagy only one surviving embryo at parturition presence of functional erect embryonic teeth presence of an embryo with ingested embryos in its stomach

Carcharias taurus : 

Carcharias taurus extensively studied

Carcharias taurus : 

Carcharias taurus extensively studied Embryonic history: dentition develops 40-60mm Hatches from capsule at 60 mm, still consume yolk sac supplies 100 to 334mm seeks and attack other embryos After ingesting siblings, consumes unfertilized eggs Ovulation ceases, relies on yolk store

Carcharias taurus : 

Carcharias taurus extensively studied Embryonic history: dentition develops 40-60mm Hatches from capsule at 60 mm, still consume yolk sac supplies 100 to 334mm seeks and attack other embryos After ingesting siblings, consumes unfertilized eggs Ovulation ceases, relies on yolk store Single surviving embryo at birth

Carcharias taurus : 

Carcharias taurus extensively studied Embryonic history: dentition develops 40-60mm Hatches from capsule at 60 mm, still consume yolk sac supplies 100 to 334mm seeks and attack other embryos After ingesting siblings, consumes unfertilized eggs Ovulation ceases, relies on yolk store Single surviving embryo at birth Embryos found with remains of siblings in stomach

Other Laminforms…: 

Other Laminforms… Alopias vulpinus, A. pelagicus, A. superciliosus also found only one surviving embryo…

Other Laminforms…: 

Other Laminforms… Alopias vulpinus, A. pelagicus, A. superciliosus also found only one surviving embryo… evidence of embryonic teeth

Other Laminforms…: 

Other Laminforms… Alopias vulpinus, A. pelagicus, A. superciliosus also found only one surviving embryo… evidence of embryonic teeth BUT only yolk in stomach contents of embryos (Gilmore 1983)

http://www.elasmo-research.org/education/topics/lh_intrauterine_cannibalism.htm: 

http://www.elasmo-research.org/education/topics/lh_intrauterine_cannibalism.htm Order Orectolobiformes Family Ginglymostomatidae Tawny Nurse Shark (Nebrius ferrigineus) Order Lamniformes Family Carchariidae Sandtiger Shark (Carcharias taurus) Family Pseudocarchariidae Crocodile Shark (Pseudocarcharias kamoharai) Family Alopiidae Pelagic Thresher Shark (Alopias pelagicus) Bigeye Thresher Shark (Alopias suprciliosus) Common Thresher Shark (Alopias vulpinus) Family Cetorhinidae Basking Shark (Cetorhinus maximus) Family Lamnidae Salmon Shark (Lamna ditropis) Porbeagle (Lamna nasus) White Shark (Carcharodon carcharias) Shortfin Mako (Isurus oxyrinchus) Longfin Mako (Isurus paucus) Order Carcharhiniformes Family Pseudotriakidae Slender Smoothhound Shark (Gollum attenuatus) False Catshark (Pseudotriakis microdon) “list of all sharks in which intrauterine cannibalism has been documented, or for which exists strong circumstantial evidence”:

MULTIPLE EMBROS AT PARTURITION : 

MULTIPLE EMBROS AT PARTURITION isurid sharks: Lamna nasus (porbeagle), Lamna ditropis (salmon shark), Isurus oxyrinchus (mako), Isurus paucus (longfin mako), Pseudocharcharias kamaharai (crocodile shark). Possibly Charcharodon charcharias (Gilmore, 1993)

http://www.elasmo-research.org/education/topics/lh_intrauterine_cannibalism.htm: 

http://www.elasmo-research.org/education/topics/lh_intrauterine_cannibalism.htm Order Orectolobiformes Family Ginglymostomatidae Tawny Nurse Shark (Nebrius ferrigineus) Order Lamniformes Family Carchariidae Sandtiger Shark (Carcharias taurus) Family Pseudocarchariidae Crocodile Shark (Pseudocarcharias kamoharai) Family Alopiidae Pelagic Thresher Shark (Alopias pelagicus) Bigeye Thresher Shark (Alopias suprciliosus) Common Thresher Shark (Alopias vulpinus) Family Cetorhinidae Basking Shark (Cetorhinus maximus) Family Lamnidae Salmon Shark (Lamna ditropis) Porbeagle (Lamna nasus) White Shark (Carcharodon carcharias) Shortfin Mako (Isurus oxyrinchus) Longfin Mako (Isurus paucus) Order Carcharhiniformes Family Pseudotriakidae Slender Smoothhound Shark (Gollum attenuatus) False Catshark (Pseudotriakis microdon) “list of all sharks in which intrauterine cannibalism has been documented, or for which exists strong circumstantial evidence”:

Lamna nasus (porbeagle shark ): 

Lamna nasus (porbeagle shark ) nourished by oophagy, (Francis and Stevens, 1999)

Lamna nasus (porbeagle shark ): 

Lamna nasus (porbeagle shark ) nourished by oophagy, Distended yolk stomach (Francis and Stevens, 1999)

Lamna nasus (porbeagle shark ): 

Lamna nasus (porbeagle shark ) nourished by oophagy, Distended yolk stomach Oophagous, avg. 4 pups per litter (Francis and Stevens, 1999)

Lamna nasus (porbeagle shark ): 

Lamna nasus (porbeagle shark ) nourished by oophagy, Distended yolk stomach Oophagous, avg. 4 pups per litter Most embryos were equal size, but found some “runts” (Francis and Stevens, 1999)

Lamna nasus (porbeagle shark ): 

Lamna nasus (porbeagle shark ) nourished by oophagy, Distended yolk stomach Oophagous, avg. 4 pups per litter Most embryos were equal size, but found some “runts” -implications of competition ? (Francis and Stevens, 1999)

Lamna nasus (porbeagle shark ): 

Lamna nasus (porbeagle shark ) nourished by oophagy, Distended yolk stomach Oophagous, avg. 4 pups per litter Most embryos were equal size, but found some “runts” -implications of competition ? -implications for evolution of adelphophagy? (Francis and Stevens, 1999)

Order Orectolobiformes: 

Order Orectolobiformes Family Ginglymostomatidae Tawny Nurse Shark (Nebrius ferrigineus) Kazuyuki Teshima, TI:Reproductive mode of the tawny nurse shark, Nebrius ferrugineus (Elasmobranchii: Ginglymostomatidae) in Okinawa waters, with comments on individuals lacking the second dorsal fin 5th Indo-Pacific Fish Conference: Noumea - New Caledonia, 3-8 November 1997: proceedings. Societe Francaise d'Ichtyologie & Institut de Recherche pour le Developpement, Paris. 1999: i-xx, 1-866. Chapter pagination: 329-333

THANKS!!!: 

THANKS!!!