Pregnancy in fish

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A pregnant Southern platyfish Pregnant x. maculatus.jpg
A pregnant Southern platyfish

Pregnancy has been traditionally defined as the period of time eggs are incubated in the body after the egg-sperm union. [1] Although the term often refers to placental mammals, it has also been used in the titles of many international, peer-reviewed, scientific articles on fish, e.g. [2] [3] [4] [5] Consistent with this definition, there are several modes of reproduction in fish, providing different amounts of parental care. In ovoviviparity, there is internal fertilization and the young are born live but there is no placental connection or significant trophic (feeding) interaction; the mother's body maintains gas exchange but the unborn young are nourished by egg yolk. There are two types of viviparity in fish. In histotrophic viviparity, the zygotes develop in the female's oviducts, but she provides no direct nutrition; the embryos survive by eating her eggs or their unborn siblings. In hemotrophic viviparity, the zygotes are retained within the female and are provided with nutrients by her, often through some form of placenta.

Contents

In seahorses and pipefish, it is the male that becomes pregnant.

Types of reproduction and pregnancy

Birth of guppy fry

Pregnancy has been traditionally defined as the period during which developing embryos are incubated in the body after egg-sperm union. Despite strong similarities between viviparity in mammals, researchers have historically been reluctant to use the term "pregnancy" for non-mammals because of the highly developed form of viviparity in eutherians. Recent research into physiological, morphological and genetic changes associated with fish reproduction provide evidence that incubation in some species is a highly specialized form of reproduction similar to other forms of viviparity. [1] Although the term "pregnancy" often refers to eutherian animals, it has also been used in the titles of many international, peer-reviewed, scientific articles on fish, e.g. [2] [3] [4] [5]

Five modes of reproduction can be differentiated in fish based on relations between the zygote(s) and parents: [6] [7]

There are two types of viviparity among fish.


Diagram

Fish reproduction types

Ovoviviparous fish

Examples of ovoviviparous fish are many of the squaliform sharks, which include sand sharks, mackerel sharks, nurse sharks, requiem sharks, dog sharks and hammerheads, among others, and the lobe finned coelacanth. Some species of rockfish ( Sebastes ) and sculpins (Comephoridae) produce rather weak larvae with no egg membrane and are also, by definition, ovoviviparous. [8] [9] Ovoviviparity occurs in most live-bearing bony fishes (Poeciliidae).

Viviparous fish

Viviparous fish include the families Goodeidae, Anablepidae, Jenynsiidae, Poeciliidae, Embiotocidae and some sharks (some species of the requiem sharks, Carcharinidae and the hammerheads, Sphyrnidae, among others). The halfbeaks, Hemiramphidae, are found in both marine and freshwaters and those species that are marine produce eggs with extended filaments that attach to floating or stationary debris, while those that are found in freshwater are viviparous with internal fertilization. The Bythitidae are also viviparous although one species, Dinematichthys ilucoeteoides , is reported to be ovoviviparous. [8]

Aquarists commonly refer to ovoviviparous and viviparous fish as "livebearers". Examples include guppies, mollies, moonfish, platys, four-eyed fish and swordtails. All of these varieties exhibit signs of their pregnancy before the live fry are born. As examples, the female swordtail and guppy will both give birth to anywhere from 20 to 100 live young after a gestation period of four to six weeks, and mollies will produce a brood of 20 to 60 live young after a gestation of six to 10 weeks. [10]

Nutrition during pregnancy

Other terms relating to pregnancy in fish relate to the differences in the mode and extent of support the female gives the developing offspring.

"Lecithotrophy" (yolk feeding) occurs when the mother provisions the oocyte with all the resources it needs prior to fertilization, so the egg is independent of the mother. Many members of the fish family Poeciliidae are considered to be lecithotrophic, however, research is increasingly showing that others are matrotrophic. [11]

"Aplacental viviparity" occurs when the female retains the embryos during the entire time of development but without any transfer of nutrients to the young. The yolk sac is the only source of nutrients for the developing embryo. There are at least two exceptions to this; some sharks gain nourishment by eating unfertilized eggs produced by the mother (oophagy or egg eating) or by eating their unborn siblings (intra-uterine cannibalism).

"Matrotrophy" (mother feeding) occurs when the embryo exhausts its yolk supply early in gestation and the mother provides additional nutrition. [12] Post-fertilization transfer of nutrients has been reported in several species within the genera Gambusia and Poecilia, specifically, G. affinis, G. clarkhubbsi, G. holbrooki, G. gaigei, G. geiseri, G. nobilis, P. formosa, P. latipinna, and P. mexicana. [11]

Viviparous fish have developed several ways of providing their offspring with nutrition. "Embryotrophic" or "histrotrophic" nutrition occurs by the production of nutritive fluid, uterine milk, by the uterine lining, which is absorbed directly by the developing embryo. "Hemotrophic" nutrition occurs through the passing of nutritive substances between blood vessels of the mother and embryo that are in close proximity, i.e. a placenta-like organ similar to that found in mammals. [8]

Comparison between species

There is considerable variation between species in the length of pregnancy. At least one group of fish has been named after its pregnancy characteristics. The surfperch, genus Embiotoca , is a saltwater fish with a gestation period of three to six months. [13] This lengthy period of pregnancy gives the family its scientific name from the Greek "embios" meaning "persistent" and "tokos" meaning "birth".

The table below shows the gestation period and number of young born for some selected fish.[ citation needed ]

SpeciesReproduction

method

Gestation period

(Days)

Number of young

(Average)

Atlantic sharpnose shark [14] (Rhizoprionodon terraenovae)Viviparous300-3304-6
Barbeled houndshark [15] (Leptocharias smithii)Viviparousa>1207
Blackspot shark [16] (Carcharhinus sealei)Viviparousb2701-2
Blue shark [17] (Prionace glauca)Viviparous270-3664-135
Bonnethead shark(Sphyrna tiburo)Viviparousc4-12 [18]
Bull shark [19] (Carcharhinus leucas)Viviparous3664-10
Butterfly goodeid [20] ( Ameca splendens )Viviparous55-606-30
Caribbean sharpnose shark (Rhizoprionodon porosus)Viviparous2-6 [21]
Daggernose shark [22] (Isogomphodon oxyrhynchus)Viviparous3662-8
Lemon shark [23] (Negaprion brevirostris)Viviparous36618 (max)
Oceanic whitetip shark [24] (Carcharhinus longimanus)Viviparous3661-15
Dwarf seahorse [25] (Hippocampus zosterae)Ovoviviparous3-5510
Sandbar shark [26] (Carcharhinus plumbeus)Viviparous3668
Spadenose shark [22] (Scoliodon laticaudus)Viviparousd150-1806-18
Viviparous eelpout [27] (Zoarces viviparus)Viviparouse18030-400
Basking shark [28] (Cetorhinus maximus)Ovoviviparous>366unknownf
Bat ray [29] (Myliobatis californica)Ovoviviparous270-3662-10
Coelacanth (g. Latimeria)Ovoviviparous>366 [30]
Blue stingray (Dasyatis chrysonota)Ovoviviparous2701-5
Bluespotted stingray [31] (Neotrygon kuhlii)Ovoviviparous90-1501-7
Carpet sharks(f. Ginglymostomatidae)Ovoviviparous18030-40
Knifetooth sawfish [32] (Anoxypristis cuspidata)Ovoviviparous1506-23
Nurse shark ( Ginglymostoma cirratum ),Ovoviviparous15021-29
Sailfin molly (Poecilia latipinna)Ovoviviparous21-2810-140
Salmon shark [33] (Lamna ditropis)Ovoviviparous2702-6
Sand tiger shark [34] (Carcharias taurus)Ovoviviparous270-3662g
School shark [35] (Galeorhinus galeus)Ovoviviparous36628-38
Shortfin mako shark [36] (Isurus oxyrinchus)Ovoviviparous450-5404-18
Spotted eagle ray [37] (Aetobatus narinari)Ovoviviparous3664
Tiger shark [38] (Galeocerdo cuvier)Ovoviviparous430-48010-80
Tawny nurse shark [39] : 195–199 (Nebrius ferrugineus)Aplacental viviparity1-2

Poeciliopsis

Members of the genus Poeciliopsis (amongst others) show variable reproductive life history adaptations. P. monacha can be considered to be lecithotrophic because the female does not really provide any resources for her offspring after fertilization. P. lucida shows an intermediate level of matrotrophy, meaning that to a certain extent, the offspring's metabolism can actually affect the mother's metabolism, allowing for increased nutrient exchange. P. prolifica is considered to be highly matrotrophic, and almost all of the nutrients and materials needed for foetal development are supplied to the oocyte after it has been fertilized. This level of matrotrophy allows Poeciliopsis to carry several broods at different stages of development, a phenomenon known as superfetation. [42]

P. elongata, P. turneri and P. presidionis form another clade which could be considered an outgroup to the P. monacha, P.lucida, and P. prolifica clade. These three species are very highly matrotrophic – so much so that in 1947, C. L. Turner described the follicular cells of P. turneri as "pseudo-placenta, pseudo-chorion, and pseudo-allantois".[ citation needed ]

Guppy

Guppies are highly prolific livebearers [43] giving birth to between five and 30 fry, though under extreme circumstances, she may give birth to only one or two or over 100. The gestation period of a guppy is typically 21–30 days, but can vary considerably. The area where a pregnant guppy's abdomen meets the tail is sometimes called the "gravid patch", or "gravid spot". When pregnant, there is a slight discoloration that slowly darkens as the guppy progresses through pregnancy. The patch first has a yellowish tinge, then brown and become deep orange as the pregnancy develops. This patch is where the fertilized eggs are stored and grow. The darkening is actually the eyes of the developing baby guppies and the orange tinge is their jelly-like eggs.[ citation needed ]

Elasmobranchs

The majority of elasmobranchs are viviparous and show a wide range of strategies to provide their offspring with nourishment and respiratory requirements. Some sharks simply retain their young in the dilated posterior segment of the oviduct. In its simplest form, the uterus does not provide any additional nutrients to the embryos. However, other elasmobranchs develop secretory uterine villi that produce histotroph, a nutrient which supplements the yolk stores of the oocyte. Uterine secretions are perhaps most advanced in the stingrays. Following depletion of the yolk, the uterine lining hypertrophies into secretory appendages termed "trophonemata". The process by which the uterine secretions (also known as uterine milk or histotroph) are produced resembles that of breast milk in mammals. Furthermore, the milk is rich in protein and lipid. As the embryo grows, vascularisation of the trophonemata enlarges to form sinusoids that project out to the surface to form a functional respiratory membrane. In lamnoid sharks, following yolk use, the embryos develop teeth and eat eggs and siblings within the uterus. There is usually one fetus per uterus and it grows to enormous proportions of up to 1.3 m in length. In placental sharks, the yolk sac is not withdrawn to become incorporated into the abdominal wall. Rather, it lengthens to form an umbilical cord and the yolk sac becomes modified into a functional epitheliochorial placenta. [9]

Male pregnancy

Pregnant male seahorse Tehotny morsky konik.jpg
Pregnant male seahorse

The male fishes of seahorses, pipefishes, weedy and leafy sea dragons (Syngnathidae) are unusual as the male, rather than the female, incubates the eggs before releasing live fry into the surrounding water. To achieve this, male seahorses protect eggs in a specialized brood pouch, male sea dragons attach their eggs to a specific area on their bodies, and male pipefish of different species may do either.

When a female's eggs reach maturity, she squirts them from a chamber in her trunk via her ovipositor into his brood pouch or egg pouch, sometimes called a "marsupium". During a mammalian pregnancy, the placenta allows the female to nourish her progeny in the womb, and remove their waste products. If male pipefish and seahorses provide only a simple pouch for fish eggs to develop and hatch, it might not fully qualify as bona-fide pregnancy. However, current research suggests that in syngnathid species with well developed brood pouches, males do provide nutrients, osmoregulation and oxygenation to the embryos they carry. [44]

Seahorse

When mating, the female seahorse deposits up to 1,500 (average of 100 to 1,000) eggs in the male's pouch, located on the ventral abdomen at the base of the tail. Male juveniles develop pouches when they are 5–7 months old. The male carries the eggs for 9 to 45 days until the seahorses emerge fully developed, but very small. The number born maybe as few as five for smaller species, or 2,500 for larger species. A male seahorse's body has large amounts of prolactin, the same hormone that governs milk production in pregnant mammals and although the male seahorse does not supply milk, his pouch provides oxygen as well as a controlled-environment.

When the fry are ready to be born, the male expels them with muscular contractions, sometimes while attaching himself to seaweed with his tail. Birth typically occurs during the night, and a female returning for the routine morning greeting finds her mate ready for the next batch of eggs. [45]

The table below shows the gestation period and number of young born for some selected seahorses.

SpeciesReproduction

method

Gestation period

(Days)

Number of young
Big-belly seahorse [46] (Hippocampus abdominalis)Ovoviviparous28600-700
Lined seahorse [47] (Hippocampus erectus)Ovoviviparous20-21650 (max)
Long-snouted seahorse [48] (Hippocampus guttulatus)Ovoviviparous21581 (max)

Pipefish

The subcaudal pouch of the male black-striped pipefish Syngnathus abaster-22.jpg
The subcaudal pouch of the male black-striped pipefish

Pipefish brood their offspring either on distinct region of its body or in a brood pouch. Brood pouches vary significantly among different species of pipefish, but all contain a small opening through which the female's eggs can be deposited. The location of the brood pouch can be along the entire underside of the pipefish or just at the base of the tail, as with seahorses. [49] Pipefish in the genus Syngnathus have a brood pouch with a ventral seam that can completely cover all of their eggs when sealed. In males without these pouches, eggs adhere to a strip of soft skin on the ventral surface of their bodies that does not contain any exterior covering – a type of "skin brooding". [50]

At least two species of pipefish, Syngnathus fuscus and Syngnathus floridae , provide nutrients for their offspring. [51]

See also

Related Research Articles

<span class="mw-page-title-main">Gestation</span> Period during the carrying of an embryo

Gestation is the period of development during the carrying of an embryo, and later fetus, inside viviparous animals. It is typical for mammals, but also occurs for some non-mammals. Mammals during pregnancy can have one or more gestations at the same time, for example in a multiple birth.

<span class="mw-page-title-main">Livebearers</span> Fish that give birth to free swimming offspring

Livebearers are fish that retain their eggs inside the body and give birth to live, free-swimming young. They are especially prized by aquarium owners. Among aquarium fish, livebearers are nearly all members of the family Poeciliidae and include: guppies, mollies, platies and swordtails.

<span class="mw-page-title-main">Pregnancy (mammals)</span> Period of reproduction

In mammals, pregnancy is the period of reproduction during which a female carries one or more live offspring from implantation in the uterus through gestation. It begins when a fertilized zygote implants in the female's uterus, and ends once it leaves the uterus.

<span class="mw-page-title-main">Birth</span> Process of bearing offspring

Birth is the act or process of bearing or bringing forth offspring, also referred to in technical contexts as parturition. In mammals, the process is initiated by hormones which cause the muscular walls of the uterus to contract, expelling the fetus at a developmental stage when it is ready to feed and breathe.

<span class="mw-page-title-main">Seahorse</span> Genus of fishes

A seahorse is any of 46 species of small marine fish in the genus Hippocampus. "Hippocampus" comes from the Ancient Greek hippókampos (ἱππόκαμπος), itself from híppos (ἵππος) meaning "horse" and kámpos (κάμπος) meaning "sea monster" or "sea animal". Having a head and neck suggestive of a horse, seahorses also feature segmented bony armour, an upright posture and a curled prehensile tail. Along with the pipefishes and seadragons they form the family Syngnathidae.

<span class="mw-page-title-main">Viviparity</span> Development of the embryo inside the mother

In animals, viviparity is development of the embryo inside the body of the mother, with the maternal circulation providing for the metabolic needs of the embryo's development, until the mother gives birth to a fully or partially developed juvenile that is at least metabolically independent. This is opposed to oviparity, where the embryos develop independently outside the mother in eggs until they are developed enough to break out as hatchlings; and ovoviviparity, where the embryos are developed in eggs that remain carried inside the mother's body until the hatchlings emerge from the mother as juveniles, similar to a live birth.

<span class="mw-page-title-main">Ovoviviparity</span> Gestation type

Ovoviviparity, ovovivipary, ovivipary, or aplacental viviparity is a term used as a "bridging" form of reproduction between egg-laying oviparous and live-bearing viviparous reproduction. Ovoviviparous animals possess embryos that develop inside eggs that remain in the mother's body until they are ready to hatch.

<span class="mw-page-title-main">Egg</span> Organic vessel in which an embryo first begins to develop

An egg is an organic vessel grown by an animal to carry a possibly fertilized egg cell and to incubate from it an embryo within the egg until the embryo has become an animal fetus that can survive on its own, at which point the animal hatches.

<span class="mw-page-title-main">Syngnathidae</span> Family of fishes

The Syngnathidae is a family of fish which includes seahorses, pipefishes, and seadragons. The name is derived from Ancient Greek: σύν, meaning "together", and γνάθος, meaning "jaw". The fused jaw is one of the traits that the entire family have in common.

<span class="mw-page-title-main">Fish reproduction</span> Reproductive physiology of fishes

Fish reproductive organs include testes and ovaries. In most species, gonads are paired organs of similar size, which can be partially or totally fused. There may also be a range of secondary organs that increase reproductive fitness. The genital papilla is a small, fleshy tube behind the anus in some fishes, from which the sperm or eggs are released; the sex of a fish can often be determined by the shape of its papilla.

<span class="mw-page-title-main">Male pregnancy</span> Pregnancy in males

Male pregnancy is the incubation of one or more embryos or fetuses by organisms of the male sex in some species. Most species that reproduce by sexual reproduction are heterogamous—females producing larger gametes (ova) and males producing smaller gametes (sperm). In nearly all animal species, offspring are carried by the female until birth, but in fish of the family Syngnathidae, males perform that function.

<span class="mw-page-title-main">Oviparity</span> Animals that lay their eggs, with little or no other embryonic development within the mother

Oviparous animals are animals that reproduce by depositing fertilized zygotes outside the body in metabolically independent incubation organs known as eggs, which nurture the embryo into moving offsprings known as hatchlings with little or no embryonic development within the mother. This is the reproductive method used by most animal species, as opposed to viviparous animals that develop the embryos internally and metabolically dependent on the maternal circulation, until the mother gives birth to live juveniles.

<span class="mw-page-title-main">Pipefish</span> Subfamily of fishes

Pipefishes or pipe-fishes (Syngnathinae) are a subfamily of small fishes, which, together with the seahorses and seadragons, form the family Syngnathidae.

<span class="mw-page-title-main">Placentation</span> Formation and structure of the placenta

Placentation refers to the formation, type and structure, or arrangement of the placenta. The function of placentation is to transfer nutrients, respiratory gases, and water from maternal tissue to a growing embryo, and in some instances to remove waste from the embryo. Placentation is best known in live-bearing mammals (theria), but also occurs in some fish, reptiles, amphibians, a diversity of invertebrates, and flowering plants. In vertebrates, placentas have evolved more than 100 times independently, with the majority of these instances occurring in squamate reptiles.

<span class="mw-page-title-main">Black-striped pipefish</span> Species of fish

The black-striped pipefish is a species of fish in the family Syngnathidae. It is found in the eastern Atlantic from the southern Gulf of Biscay to Gibraltar, also in the Mediterranean and Black Seas. As the introduced species it is mentioned in the Caspian Sea and fresh waters of its basin.

<span class="mw-page-title-main">Broadnosed pipefish</span> Species of fish

The broadnosed pipefish or deepnosed pipefish is a fish of the family Syngnathidae. It is native to the Eastern Atlantic from Vardø in Norway, Baltic Sea and the British Isles at north to Morocco at south. It is also found in the Mediterranean Sea, Black Sea and Sea of Azov. It is common in the coastal shallow waters, usually on reefs with seagrasses. This species is notable for its "broad" snout, which is as deep as its body.

The dusky pipefish is a species of the pipefishes, widespread in the western Atlantic from the Bermuda, Chesapeake Bay, northern part of the Gulf of Mexico, Bahama, and the western Caribbean Sea to Panama in south. Marine subtropical demersal fish, which lives at the depth up to 22 metres (72 ft), usually up to 4 metres (13 ft). The maximal length of the fish is 25 centimetres (9.8 in).

The chain pipefish is a pipefish species. It inhabits the western Atlantic from Virginia, Bermuda and northern Gulf of Mexico to Campeche and Jamaica, but is absent from the Bahamas. It is a marine subtropical reef-associated fish, up to 38 cm length.

Polyandry in fishes is a mating system where females mate with multiple males within one mating season. This type of mating exists in a variety of animal species. Polyandry has been found in both oviparous and viviparous bony fishes and sharks. General examples of polyandry occur in fish species, such as green swordtails and Trinidadian guppies. Specific types of polyandry have also been classified, such as classical polyandry in pipefish cooperative polyandry in cichlids and convenience polyandry in sharks.

<span class="mw-page-title-main">Modes of reproduction</span>

Animals make use of a variety of modes of reproduction to produce their young. Traditionally this variety was classified into three modes, oviparity, viviparity, and ovoviviparity.

References

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