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Marine Mammal Reproduction and Mating Systems

MikeCarlo
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Marine Mammal Reproduction and Mating Systems

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    1. Marine Mammal Reproduction and Mating Systems

    2. Life History Theory Individual animals behave to maximize their reproductive success (RS) over their lifetime. Influenced by: decisions individuals make to maximize fitness phenotypic variation adaptations Constraints phylogenetic ecological

    3. Marine Mammals All forage at sea (or in water) Amphibious species vs. completely aquatic Pinnipeds: most-all reproduction on land Challenges Breathe air; live in water Thermoregulation ? selection for larger size Seasonal food availability/ advantages of fasting ? lipid storage Preparing offspring for weaning in dynamic (e.g., ice-breeding seals) or fully aquatic habitat

    4. Reproductive Anatomy Sirenia Pinnipeds Cetaceans

    7. Walrus - the largest bacula (penis bones) of the animal kingdom Walrus - the largest bacula (penis bones) of the animal kingdom

    13. TESTES ARE in abdominal cavity; penis is fibroelastic TESTES ARE in abdominal cavity; penis is fibroelastic

    14. Reproductive Anatomy: MALE Remnant pelvic bones are attached to retractro muscleRemnant pelvic bones are attached to retractro muscle

    15. Females: Mammalian Uteri Duplex: lagomorphs, rodents, aarvarks, hyraxes 2 uteri, each with cervix opening into vagina Bipartite: whales & most carnivore Uterus separate, single cervix Bicornuate: widespread (insectivores, some carnivores, ungulates etc.) Uterine horn Y-shaped Single cervix Simplex: single uterus, single cervix Bats, higher primates, xenathransDuplex: lagomorphs, rodents, aarvarks, hyraxes 2 uteri, each with cervix opening into vagina Bipartite: whales & most carnivore Uterus separate, single cervix Bicornuate: widespread (insectivores, some carnivores, ungulates etc.) Uterine horn Y-shaped Single cervix Simplex: single uterus, single cervix Bats, higher primates, xenathrans

    16. Cetacean Reproductive Anatomy: FEMALE Synapomorphes with Artiodactyls: 3) pseudocervical folds Pseudocervix (also in artiodactyls) Toothed whales: have deep ovarian pouches, in mysticetes ovaries are more exposed to body cavity Fetus usually develops in one of horns Left ovary in many/most odontocetes is active early; right later in life or if left is damagedPseudocervix (also in artiodactyls) Toothed whales: have deep ovarian pouches, in mysticetes ovaries are more exposed to body cavity Fetus usually develops in one of horns Left ovary in many/most odontocetes is active early; right later in life or if left is damaged

    18. (From Harrison and Bryden, 1988.) (From Harrison and Bryden, 1988.)

    19. Joke: “We haven’t come very far from early beliefs…”Joke: “We haven’t come very far from early beliefs…”

    22. Artiodactyl --> Cetacean

    23. Reproductive Anatomy shared with Artiodactyls MALES: fibroelastic penis (i.e. no baculum) muscle (vs. vasodilation) FEMALES: bicornuate uterus* pseudocervix (folds in vaginal wall)* diffuse placental attachment to uterus*

    24. Reproductive Physiology

    25. Ovarian Cycle

    26. In cetaceans corpora albicans persist throughout lifeIn cetaceans corpora albicans persist throughout life

    28. Calcluating age using corpora albicantia in cetaceans What variables need to be known?

    29. Hormones of Pregnancy and Lactation Similar to other mammals Progesterone and Estradiol Prolactin

    30. Ovulation and Estrus estrus vs. estrous What defines estrus? Types of ovulation spontaneous Induced Monoestrous vs. Polyestrous Estrus = behavioral receptivit and ovulation B.Dolphins reported as spontaneous ovulatorsEstrus = behavioral receptivit and ovulation B.Dolphins reported as spontaneous ovulators

    31. Potential Mysticete Reproductive Cycle

    32. Gestation Period (months) Baird’s beaked whale 17 Killer Whale 15 Sperm Whale 15-16 Beluga >11 LF & SF Pilot Wl (Globicephala spp) 14.5 - 15 Bottlenose dolphin 12 Harbor Porpoise 10-11 Dalls Porpoise 11-11.4 Balaenoptera musculus 11-12 Balaenoptera acutorostrata 10 M. novaeangliae 11-12 Eschrichtius robustus 13-14 Balaena mysticetus 13-14

    33. Reproductive Cycles: Mystictes 2 – 3 year birth interval (in most) breeding – migration – feeding – calving – lactation – weaning – resting Possibly longer in bowheadsPossibly longer in bowheads

    34. Mysticete Reproductive Cycle (fin whale) Breeding Migration Feeding From Fig. 6-19 Reynolds: S. Hemisphere female fin ehale. Fins have a 2 yr cycle with gestation about 11 mos and lcataion 6-7 montsh then anestrusFrom Fig. 6-19 Reynolds: S. Hemisphere female fin ehale. Fins have a 2 yr cycle with gestation about 11 mos and lcataion 6-7 montsh then anestrus

    37. Fastest growing mammalsFastest growing mammals

    39. Birth of an Irawaddy Dolphin (Orcaella brevirostris)

    40. Cetacean Neonates Size relative to female Thermoregulatory considerations higher metabolic rate higher caloric intake rapid deposition of fat

    41. Maternal Care and Lactation Fasting: Phocids and Mysticetes Foraging Cycle: Otariids Aquatic Nursing (no fasting): Walrus and Odontocetes

    42. Pinnipeds: Lactation Dichotomy Phocids -- short lactation (4-50 days) Otariids & Odobenids – longer (4-36 months)

    43. Lactation and Milk Fat Duration (d) %Fat %Protein H. Porpoise 240-360 46 11 Spinner Dolphin 390-810 22 7 Sperm Whale 600-1200 26 8-10 Fin 180-210 33 4-13 Minke 150-180 30 14 Humpback 300-330 44 13

    44. Factors that affect Duration of Dependence Nutritional/Physiological needs (temperature) Physical maturation Social development

    45. Reproductive Cycles: Pinnipeds 1 year birth interval – Phocids 1-2 year birth interval – Otariids 2-3 year birth interval – Odobenids

    46. 13.12. Generalized pinniped annual reproductive cycle, including durations of delayed implantation (dark) and developmental gestation (light). (Adapted from Sumich, 1996.) 13.12. Generalized pinniped annual reproductive cycle, including durations of delayed implantation (dark) and developmental gestation (light). (Adapted from Sumich, 1996.)

    47. Delayed Implantation What is DI? What marine mammals exhibit DI? Sea otters, Polar Bears, and Pinnipeds

    48. Delayed implantation Benefits? Natural selection for? Multiple derivations

    49. Otariid Reproductive Cycle

    50. Phocid Reproductive Cycle

    51. Mating Systems MS influenced by: Breeding habitat / space Defensible resources (if any) Behavior of females (aggregating vs dispersed)

    52. What determines a mammal’s mating system? need for biparental care ratio of reproductive females to reproductive males = OPERATIONAL SEX RATIO degree of estrous synchrony among females male access to estrous females

    53. What predictions would you make about cetacean mating systems? Polyandry: males and females have multiple partners; requires multiple offspring per clutch; doesn’t apply to cetaceans PromiscuityPolyandry: males and females have multiple partners; requires multiple offspring per clutch; doesn’t apply to cetaceans Promiscuity

    54. Much less known about cetacean mating systems and strategies compared to pinnipeds. WHY?

    55. Eubalaena glacialis Females mate with multiple males No aggression between competing males Courting bouts 1 – 2 hrs Largest testes of any living mammal weigh up to about 525 kg.) suggests sperm competition E.g.: copulates from December to March, when most of the young are born. After much nuzzling and caressing, mating right whales roll about randomly exposing flippers, flukes, backs, bellies, and portions of their heads. It has been noted that the male would sometimes begin precopulatory behavior by placing his chin on the exposed hindquarters of the female. It is believed that most right whales are polygamous and no permanent pair bonds are formed. Females probably mate with multiple males. No aggression has been observed between competing males, which is a rare behavior in mammals. Courting bouts may last for an hour or two, after which participants go their own way. Both males and females are seen on their back at the water's surface but females may show this posture to move her genitalia away from a pursuing male. E.g.: copulates from December to March, when most of the young are born. After much nuzzling and caressing, mating right whales roll about randomly exposing flippers, flukes, backs, bellies, and portions of their heads. It has been noted that the male would sometimes begin precopulatory behavior by placing his chin on the exposed hindquarters of the female. It is believed that most right whales are polygamous and no permanent pair bonds are formed. Females probably mate with multiple males. No aggression has been observed between competing males, which is a rare behavior in mammals. Courting bouts may last for an hour or two, after which participants go their own way. Both males and females are seen on their back at the water's surface but females may show this posture to move her genitalia away from a pursuing male.

    56. It is likely that Bowhead and other Baleen whales are monogamous (Lockyer 1984) and the extremely large testes of Bowhead, Right and Gray whales indicate a multimale, multifemale system which may have in turn led to a well developed form of sperm competition (Brownell and Ralls 1986). Often the female will role or swim away from the males exposing her belly above the surface thereby making copulation difficult and exerting a form of mate choice (Norris et al. 1983.) since only the largest most aggressive male is able to pursue her and copulate. Females that have copulated already may often copulate with other males suggesting that the system is not purely polygynous where one male inseminates several females. Right, bowhead and gray whales have extremely large testes, capable of producing large quantities of sperm, and as suggested previously it is likely that they practice a form of sperm competition. On the other hand humpback whales have relatively small testes and hence more aggression amongst males directly competing for females is observed and only one male mates with the female. It is likely that Bowhead and other Baleen whales are monogamous (Lockyer 1984) and the extremely large testes of Bowhead, Right and Gray whales indicate a multimale, multifemale system which may have in turn led to a well developed form of sperm competition (Brownell and Ralls 1986). Often the female will role or swim away from the males exposing her belly above the surface thereby making copulation difficult and exerting a form of mate choice (Norris et al. 1983.) since only the largest most aggressive male is able to pursue her and copulate. Females that have copulated already may often copulate with other males suggesting that the system is not purely polygynous where one male inseminates several females. Right, bowhead and gray whales have extremely large testes, capable of producing large quantities of sperm, and as suggested previously it is likely that they practice a form of sperm competition. On the other hand humpback whales have relatively small testes and hence more aggression amongst males directly competing for females is observed and only one male mates with the female.

    57. It is likely that Bowhead and other Baleen whales are monogamous (Lockyer 1984) and the extremely large testes of Bowhead, Right and Gray whales indicate a multimale, multifemale system which may have in turn led to a well developed form of sperm competition (Brownell and Ralls 1986). Often the female will role or swim away from the males exposing her belly above the surface thereby making copulation difficult and exerting a form of mate choice (Norris et al. 1983.) since only the largest most aggressive male is able to pursue her and copulate. Females that have copulated already may often copulate with other males suggesting that the system is not purely polygynous where one male inseminates several females. Right, bowhead and gray whales have extremely large testes, capable of producing large quantities of sperm, and as suggested previously it is likely that they practice a form of sperm competition. On the other hand humpback whales have relatively small testes and hence more aggression amongst males directly competing for females is observed and only one male mates with the female. It is likely that Bowhead and other Baleen whales are monogamous (Lockyer 1984) and the extremely large testes of Bowhead, Right and Gray whales indicate a multimale, multifemale system which may have in turn led to a well developed form of sperm competition (Brownell and Ralls 1986). Often the female will role or swim away from the males exposing her belly above the surface thereby making copulation difficult and exerting a form of mate choice (Norris et al. 1983.) since only the largest most aggressive male is able to pursue her and copulate. Females that have copulated already may often copulate with other males suggesting that the system is not purely polygynous where one male inseminates several females. Right, bowhead and gray whales have extremely large testes, capable of producing large quantities of sperm, and as suggested previously it is likely that they practice a form of sperm competition. On the other hand humpback whales have relatively small testes and hence more aggression amongst males directly competing for females is observed and only one male mates with the female.

    58. Sperm Competition Balaenidae Balaena mysticetus bowhead Eubalaena glacialis n. right whale Eubalaena australis s. right whale Eschrichtiidae From MarMam: In studies on ground squirrels on average the first male to mate with the female sires on average 60% of the offspring and the second 30% and the third only 10%. Hence the males do not guard the females but instead leave to copulate with as many receptive females as they can as is often the case with most of the delphinid species. In other species the male will guard the female for several hours until the female is no longer receptive thus ensuring 100% paternity but lessening the chances of mating with other females. There is no direct evidence for this in cetaceans although some species do have male 'escorts' when traveling as a pod. From MarMam: In studies on ground squirrels on average the first male to mate with the female sires on average 60% of the offspring and the second 30% and the third only 10%. Hence the males do not guard the females but instead leave to copulate with as many receptive females as they can as is often the case with most of the delphinid species. In other species the male will guard the female for several hours until the female is no longer receptive thus ensuring 100% paternity but lessening the chances of mating with other females. There is no direct evidence for this in cetaceans although some species do have male 'escorts' when traveling as a pod.

    59. Mating Systems in Pinnipeds Much more known Why? Polygyny most common, but wide range of details

    60. Otariids All are polygynous Varying degrees

    61. Phocids Extreme polygyny to __________________

    62. Grey sealGrey seal

    63. Grey seal Halichoerus grypus (polygyny to serial monogamy)

    64. Inflatable nose (hood) and extrudabble nasal sac (bladder) in an adult male; males larger than females; Nasal septum can be kinflated and extruded through one nostriol to form large, red balloon-like structureInflatable nose (hood) and extrudabble nasal sac (bladder) in an adult male; males larger than females; Nasal septum can be kinflated and extruded through one nostriol to form large, red balloon-like structure

    65. Mirounga leonina and angustirostris (Southern and Northern Elephant Seals) What factors have selected for extreme polygyny in this phocid? How does their breeding system compare to that of other phocids? What factors seem to have been most important in shaping their breeding system?

    66. Monachus schauinslandi (Hawaiian monk seal)

    67. 11.17. Spatial and vocal structure of a single courting display of a male walrus, with eight discrete phonations: b=bell phonation; bk=bell knock phonation; dk=double knock phonation; dkb=double knock bell phonation; dv=diving phonation; k=knock phonation; st=strum phonation; t=tap phonation; w=whistle; numerals=number of repetitions. (Redrawn from Stirling et al., 1987.) 11.17. Spatial and vocal structure of a single courting display of a male walrus, with eight discrete phonations: b=bell phonation; bk=bell knock phonation; dk=double knock phonation; dkb=double knock bell phonation; dv=diving phonation; k=knock phonation; st=strum phonation; t=tap phonation; w=whistle; numerals=number of repetitions. (Redrawn from Stirling et al., 1987.)

    68. 13.16. A simplified model of the evolution of polygyny in pinnipeds, with emphasis on male characteristics.  Black arrows relate the major attributes of typical polygynous pinnipeds; the colored arrows indicate positive (solid) and negative (dashed) feedback loops.  (Adapted partly from Bartholomew, 1970.) 13.16. A simplified model of the evolution of polygyny in pinnipeds, with emphasis on male characteristics.  Black arrows relate the major attributes of typical polygynous pinnipeds; the colored arrows indicate positive (solid) and negative (dashed) feedback loops.  (Adapted partly from Bartholomew, 1970.)

    69. Post-reproductive females

    70. Post-reproductive females females that spend up to 30% of their life as non-reproducers and exist in matrilineal or matrifocal groups What are the physiological signs? What is the evolutionary significance of post-reproductive females?

    71. What cetaceans species have post-reproductive females? short-finned pilot whales (Globicephala macrorhynchus) killer whales (Orcinus orca) Long-finned pilot whales (G. melaena) and sperm whales (Physeter macrocephalus) do not appear to have PRFs Sara and Jim Heimlich-Boran's _Killer Whales: "Using a variety of estimates, it appears that half of all killer whale females older than 39 have stopped giving birth and by the age of 55, all females are post-reproductive. Although there is no direct proof that ovulation has ceased, biological studies on short-finned pilot whales, a closely related species, have shown a lack of ovulation in females over the age of 40. This strongly supports the existence of this later life stage in female killer whales. It has been estimated that one-third of all adult females in the Pacific Northwest resident communities are post-reproductive." Sara and Jim Heimlich-Boran's _Killer Whales: "Using a variety of estimates, it appears that half of all killer whale females older than 39 have stopped giving birth and by the age of 55, all females are post-reproductive. Although there is no direct proof that ovulation has ceased, biological studies on short-finned pilot whales, a closely related species, have shown a lack of ovulation in females over the age of 40. This strongly supports the existence of this later life stage in female killer whales. It has been estimated that one-third of all adult females in the Pacific Northwest resident communities are post-reproductive."

    72. Globicephala melaena short-finned pilot whale “Globi” =round, “cephala” =head Long-finned Pectoral flippers = 1/5 of body Short-finned Pectoral flippers = 1/6 of body

    73. Globicephala malaena short-finned pilot whale

    74. Habitat and Diving Deep water (1000 m +) Steep slopes upwelling areas (e.g., underwater canyons) usually short dives; can dive ? 1 hr Maximum depths: Long-finned pilot whale 650 m Short-finned pilot whale 500 m

    75. Food Cephalopods (squid) Fish (e.g., mackerel)

    76. Mass strandings Form cohesive social groups Studies of social structure: Photo – identification Mass strandings (Kasuya & Marsh) Drive fisheries

    77. Genetic Data from Drive Fisheries Matrileal groups, but often > 1 matriline 2-4 generations together Males in groups related and not fathers of offspring Neither males nor females (G. spp.) appear to disperse from natal group Polygynous mating system

    78. Long-finned pilot whales, Cape Breton, Nova Scotia (Ottensmeyer, C.A ) Photo-ID

    79. Long-finned pilot whales (Ottensmeyer, C.A ) Form stable matrilineal “units” or “pods” not segregated by age or sex Exhibit natal philopatry (rare among mammals) mate when different family groups interact

    80. Sotalia fluviatilis, F. Delphinidae tucuxi dolphin; eastern South and Central America REPRODUCTION OF THE ESTUARINE DOLPHIN (SOTALIA GUIANENSIS) ON THE COAST OF PARANÁ, SOUTHERN BRAZIL Issn: 1545-1542 Journal: Journal of Mammalogy Volume: 83 Issue: 2 Pages: 507-515 Authors: Weber Rosas, Fernando C., Monteiro-Filho, Emygdio L. A. DOI: 10.1644/1545-1542(2002)083<0507:ROTEDS>2.0.CO;2 ABSTRACT The estuarine dolphin (Sotalia guianensis) is common along most of the Brazilian coast, but little is known about its reproduction. We analyzed the gonads of 50 individuals incidentally caught in fishing nets on the coast of Paraná, southern Brazil, between 1997 and 1999. Testes of adult males were 31.9 cm in length and 11.6 cm in width and 3.3% of the total body mass. Relative size of testes suggests a multimale mating system with sperm competition. Females ovulate in both ovaries, although the left ovary matures earlier than the right. Males reached sexual maturity at 7 years and at body lengths estimated at 170–175 cm. Females matured at 5–8 years of age and at body lengths of 164–169 cm. The reproductive cycle was estimated at 2 years, with no marked seasonality in ovulation or timing of birth. Gestation was about 12 months, fetal growth rate was 9 cm/month, and length at birth was estimated at 92.2 cm. Females older than 25 years had senescent ovaries. REPRODUCTION OF THE ESTUARINE DOLPHIN (SOTALIA GUIANENSIS) ON THE COAST OF PARANÁ, SOUTHERN BRAZILIssn: 1545-1542 Journal: Journal of Mammalogy Volume: 83 Issue: 2 Pages: 507-515Authors: Weber Rosas, Fernando C., Monteiro-Filho, Emygdio L. A.DOI: 10.1644/1545-1542(2002)083<0507:ROTEDS>2.0.CO;2 ABSTRACT The estuarine dolphin (Sotalia guianensis) is common along most of the Brazilian coast, but little is known about its reproduction. We analyzed the gonads of 50 individuals incidentally caught in fishing nets on the coast of Paraná, southern Brazil, between 1997 and 1999. Testes of adult males were 31.9 cm in length and 11.6 cm in width and 3.3% of the total body mass. Relative size of testes suggests a multimale mating system with sperm competition. Females ovulate in both ovaries, although the left ovary matures earlier than the right. Males reached sexual maturity at 7 years and at body lengths estimated at 170–175 cm. Females matured at 5–8 years of age and at body lengths of 164–169 cm. The reproductive cycle was estimated at 2 years, with no marked seasonality in ovulation or timing of birth. Gestation was about 12 months, fetal growth rate was 9 cm/month, and length at birth was estimated at 92.2 cm. Females older than 25 years had senescent ovaries.

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