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Syngnathids are found in temperate and tropical seas across the world. Most species inhabit shallow, coastal waters, but a few are known from the open ocean, especially in association with [[sargassum]] mats. They are characterised by their elongated snouts, fused jaws, the absence of [[pelvic fin]]s, and by thick plates of bony armour covering their bodies. The armour gives them a rigid body, so they swim by rapidly fanning their fins. As a result, they are relatively slow compared with other fish but are able to control their movements with great precision, including hovering in place for extended periods.<ref name=EoF>{{cite book |editor=Paxton, J.R. |editor2=Eschmeyer, W.N. |author1=Orr, J.W |author2=Pietsch, T.W. |name-list-style=amp |year=1998|title=Encyclopedia of Fishes|publisher= Academic Press|location=San Diego|pages= 168–169|isbn= 0-12-547665-5}}</ref>
Syngnathids are found in temperate and tropical seas across the world. Most species inhabit shallow, coastal waters, but a few are known from the open ocean, especially in association with [[sargassum]] mats. They are characterised by their elongated snouts, fused jaws, the absence of [[pelvic fin]]s, and by thick plates of bony armour covering their bodies. The armour gives them a rigid body, so they swim by rapidly fanning their fins. As a result, they are relatively slow compared with other fish but are able to control their movements with great precision, including hovering in place for extended periods.<ref name=EoF>{{cite book |editor=Paxton, J.R. |editor2=Eschmeyer, W.N. |author1=Orr, J.W |author2=Pietsch, T.W. |name-list-style=amp |year=1998|title=Encyclopedia of Fishes|publisher= Academic Press|location=San Diego|pages= 168–169|isbn= 0-12-547665-5}}</ref>


Uniquely, after syngnathid females lay their [[egg (biology)|eggs]], the male then fertilizes and [[male pregnancy|carries the eggs]] during incubation, using one of several methods. Male seahorses have a specialized ventral [[Brood pouch (Syngnathidae)|pouch]] to carry the eggs, male sea dragons attach the eggs to their tails, and male pipefish may do either, depending on their species.<ref>{{cite web |url=http://www.fisheries.nsw.gov.au/threatened_species/general/synganathids |publisher=NSW Department of Primary Industries - Fisheries |title=Seahorses and their relatives |access-date=2008-06-13 |archive-url = https://web.archive.org/web/20080501212219/http://www.fisheries.nsw.gov.au/threatened_species/general/synganathids |archive-date = 2008-05-01}}</ref> The most fundamental difference between the different lineages of the family Syngnathidae is the location of male brood pouch.<ref>Hamilton, H., N. Saarman, G. Short, A. B. Sellas, B. Moore, T. Hoang, C. L. Grace, M. Gomon, et al. 2016. Molecular phylogeny and patterns of diversification in syngnathid fishes. Molecular Phylogenetics and Evolution. In press. <nowiki>http://dx.doi.org/10.1016/j.ympev.2016.10.003</nowiki>.</ref> The two locations are on the tail (Urophori) and on the abdomen (Gastrophori).<ref name=":0">Wilson, A. B., I. Ahnesjö, A. C. J. Vincent, and A. Meyer. 2003. The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (Family Syngnathidae). Evolution 57:1374–1386.</ref> There is also variation in Syngnathid pouch complexity with brood pouches ranging from simple ventral gluing areas to fully enclosed pouches.<ref>Dawson, C. E. 1985. Indo-Pacific pipefishes (Red Sea to the Americas). Gulf Coast Research Laboratory, Ocean Springs, MS. [as cited by Wilson et al. (2003)]</ref> In species with more developed, enclosed pouches it has been demonstrated that males directly provide their brood with not only nutrients<ref>Ripley, J. L., and C. M. Foran. 2008. Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). Journal of Comparative Physiology B 179:325–333.</ref> but also immunity to pathogens.<ref>Roth, O., V. Klein, A. Beemelmanns, J. P. Scharsack, and T. B. H. Reusch. 2012. Male pregnancy and biparental immune priming. The American Naturalist 180:802–814.</ref> Syngnathids with more developed brood pouches are also known to be able to partially or completely abort a brood from a female with low fitness.<ref>Paczolt, K. A., and A. G. Jones. 2010. Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464:401–404.</ref>
Uniquely, after syngnathid females lay their [[egg (biology)|eggs]], the male then fertilizes and [[male pregnancy|carries the eggs]] during incubation, using one of several methods. Male seahorses have a specialized ventral [[Brood pouch (Syngnathidae)|brood pouch]] to carry the embryos, male sea dragons attach the eggs to their tails, and male pipefish may do either, depending on their species.<ref>{{cite web |url=http://www.fisheries.nsw.gov.au/threatened_species/general/synganathids |publisher=NSW Department of Primary Industries - Fisheries |title=Seahorses and their relatives |access-date=2008-06-13 |archive-url = https://web.archive.org/web/20080501212219/http://www.fisheries.nsw.gov.au/threatened_species/general/synganathids |archive-date = 2008-05-01}}</ref> The most fundamental difference between the different lineages of the family Syngnathidae is the location of male brood pouch.<ref>Hamilton, H., N. Saarman, G. Short, A. B. Sellas, B. Moore, T. Hoang, C. L. Grace, M. Gomon, et al. 2016. Molecular phylogeny and patterns of diversification in syngnathid fishes. Molecular Phylogenetics and Evolution. In press. <nowiki>http://dx.doi.org/10.1016/j.ympev.2016.10.003</nowiki>.</ref> The two locations are on the tail (Urophori) and on the abdomen (Gastrophori).<ref name=":0">Wilson, A. B., I. Ahnesjö, A. C. J. Vincent, and A. Meyer. 2003. The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (Family Syngnathidae). Evolution 57:1374–1386.</ref> There is also variation in Syngnathid pouch complexity with brood pouches ranging from simple ventral gluing areas to fully enclosed pouches.<ref>Dawson, C. E. 1985. Indo-Pacific pipefishes (Red Sea to the Americas). Gulf Coast Research Laboratory, Ocean Springs, MS. [as cited by Wilson et al. (2003)]</ref> In species with more developed, enclosed pouches it has been demonstrated that males directly provide their brood with not only nutrients<ref>Ripley, J. L., and C. M. Foran. 2008. Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). Journal of Comparative Physiology B 179:325–333.</ref> but also immunity to pathogens.<ref>Roth, O., V. Klein, A. Beemelmanns, J. P. Scharsack, and T. B. H. Reusch. 2012. Male pregnancy and biparental immune priming. The American Naturalist 180:802–814.</ref> Syngnathids with more developed brood pouches are also known to be able to partially or completely abort a brood from a female with low fitness.<ref>Paczolt, K. A., and A. G. Jones. 2010. Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464:401–404.</ref>


A wide variety of mate choice and mating competition has been observed in Syngnathidae.<ref>Rosenqvist, G., and A. Berglund. 2011. Sexual signals and mating patterns in Syngnathidae. Journal of Fish Biology 78:1647-1661.</ref> For example, [[hippocampus kuda|''Hippocampus fuscus'']] exhibits conventional sex roles of males competing for female access<ref>Vincent, A. C. J. 1994. Seahorses exhibit conventional sex roles in mating competition, despite male pregnancy. Behaviour 128:135–151.</ref> while [[Messmate pipefish|''Corythoichthys haematopterus'']] is completely sex role reversed.<ref>Sogabe, A., and Y. Yanagisawa. 2007. Sex-role reversal of a monogamous pipefish without higher potential reproductive rate in females. Proceedings of the Royal Society B: Biological Sciences 274:2959–2963.</ref> Most conventional sex role syngnathids are monogamous whereas sex role reversed species mostly exhibit polygamous behavior.<ref name=":0" />
A wide variety of mate choice and mating competition has been observed in Syngnathidae.<ref>Rosenqvist, G., and A. Berglund. 2011. Sexual signals and mating patterns in Syngnathidae. Journal of Fish Biology 78:1647-1661.</ref> For example, [[hippocampus kuda|''Hippocampus fuscus'']] exhibits conventional sex roles of males competing for female access<ref>Vincent, A. C. J. 1994. Seahorses exhibit conventional sex roles in mating competition, despite male pregnancy. Behaviour 128:135–151.</ref> while [[Messmate pipefish|''Corythoichthys haematopterus'']] is completely sex role reversed.<ref>Sogabe, A., and Y. Yanagisawa. 2007. Sex-role reversal of a monogamous pipefish without higher potential reproductive rate in females. Proceedings of the Royal Society B: Biological Sciences 274:2959–2963.</ref> Most conventional sex role syngnathids are monogamous whereas sex role reversed species mostly exhibit polygamous behavior.<ref name=":0" />


Seahorses and pipefish also have a unique feeding mechanism, known as [[elastic recoil feeding]]. Although the mechanism is not well understood, seahorses and pipefish appear to have the ability to store energy from contraction of their [[epaxial]] muscles (used in upward head rotation), which they then release, resulting in extremely fast head rotation to accelerate their mouths towards unsuspecting prey.<ref>Van Wassenbergh et al., J. R. Soc. Interface 5:285(2008)</ref><ref>Van Wassenbergh et al., Biol. Lett. 5:200 (2009)</ref>
Seahorses and pipefish also have a unique feeding mechanism, known as [[elastic recoil feeding]]. Although the mechanism is not well understood, seahorses and pipefish appear to have the ability to store energy from contraction of their [[epaxial]] muscles (used in upward head rotation), which they then release, resulting in extremely fast head rotation to accelerate their mouths towards unsuspecting prey.<ref>Van Wassenbergh et al., J. R. Soc. Interface 5:285(2008)</ref><ref>Van Wassenbergh et al., Biol. Lett. 5:200 (2009)</ref>

== Evolution ==
Phylogenetic analysis implies that the most recent common ancestor of all syngnathids was likely pouchless. The family ''Solenostomidae'' (ghost pipefish) is a family in the order Syngnathiformes. Female ghost pipefish incubate their developing embryos inside fused pelvic fins. Evolutionary transitions from female to male care are practically nonexistent in teleosts, so brood pouches were likely not ancestral<ref name=":1">{{Cite journal|last=Whittington|first=Camilla M.|last2=Friesen|first2=Christopher R.|date=2020-10|title=The evolution and physiology of male pregnancy in syngnathid fishes|url=https://onlinelibrary.wiley.com/doi/10.1111/brv.12607|journal=Biological Reviews|language=en|volume=95|issue=5|pages=1252–1272|doi=10.1111/brv.12607|issn=1464-7931}}</ref>. Genome sequencing supports this, revealing multiple different origins across and within different brood pouch types<ref name=":2">{{Cite journal|last=Hamilton|first=Healy|last2=Saarman|first2=Norah|last3=Short|first3=Graham|last4=Sellas|first4=Anna B.|last5=Moore|first5=Beth|last6=Hoang|first6=Tinya|last7=Grace|first7=Christopher L.|last8=Gomon|first8=Martin|last9=Crow|first9=Karen|last10=Brian Simison|first10=W.|date=2017-02|title=Molecular phylogeny and patterns of diversification in syngnathid fishes|url=https://linkinghub.elsevier.com/retrieve/pii/S1055790316302652|journal=Molecular Phylogenetics and Evolution|language=en|volume=107|pages=388–403|doi=10.1016/j.ympev.2016.10.003}}</ref>. Oviparity was the ancestral trait, and the evolution of viviparity must have relied on the evolution and integration of multiple complex traits such as morphology, physiology, and behavior.


Syngnathidae was historically divided into two major lineages based on brood pouch location: ''Neophinae'' (located on the trunk) and ''Syngnathinae'' (located on the tail)<ref name=":1" />. Genome sequencing shows a parallel increase in brood pouch complexity in both ''Neophinae'' and ''Syngnathinae<ref name=":2" />''. Some species may have also independently evolved to have trunk brooding phenotypes, separate from the ''Neophinae''. One example of this convergent evolution arises in pygmy seahorses (''Hippocampus bargibanti, Hippocampus denise, Hippocampus pontohi''). Pygmy seahorses are very small (about 1-2cm tall) trunk brooders, phylogenetically surrounded by tail brooders. It’s likely that the pygmy seahorse once had their brood pouch on their tail. The brood pouch may have moved locations when there was strong a correlated selection for a prehensile tail and diminutive size, resulting in a very small, trunk brooding organism<ref name=":1" />.


Viviparity and male-pregnancy in Syngnathidae have a complex evolutionary history with many independent origins of similar traits. Early members of the family developed traits to limit the presence of deleterious mutations, allowing for more rapid evolution<ref>{{Cite journal|last=Wang|first=Xin|last2=Zhang|first2=Yanhong|last3=Zhang|first3=Huixian|last4=Qin|first4=Geng|last5=Lin|first5=Qiang|date=2019-12|title=Complete mitochondrial genomes of eight seahorses and pipefishes (Syngnathiformes: Syngnathidae): insight into the adaptive radiation of syngnathid fishes|url=https://bmcevolbiol.biomedcentral.com/articles/10.1186/s12862-019-1430-3|journal=BMC Evolutionary Biology|language=en|volume=19|issue=1|pages=119|doi=10.1186/s12862-019-1430-3|issn=1471-2148|pmc=PMC6560779|pmid=31185889}}</ref>. The advantage of a more controlled and protected embryonic development seemed to be enough to enact evolutionary development throughout Syngnathidae to varying degrees. In species with the most complex brood pouch systems, many traits (behavioral, physiological, morphological, and immunological) coevolved to allow for male pregnancy, greatly increasing the fitness of those individuals’ offspring. The evolution of these traits resulted in a sex-role reversal in which females may exhibit competitive behavior for a mate<ref>{{Cite journal|last=Goncalves|first=Ines Braga|last2=Mobley|first2=Kenyon B.|last3=Ahnesjö|first3=Ingrid|last4=Sagebakken|first4=Gry|last5=Jones|first5=Adam G.|last6=Kvarnemo|first6=Charlotta|date=2010-05-22|title=Reproductive compensation in broad-nosed pipefish females|url=https://royalsocietypublishing.org/doi/10.1098/rspb.2009.2290|journal=Proceedings of the Royal Society B: Biological Sciences|language=en|volume=277|issue=1687|pages=1581–1587|doi=10.1098/rspb.2009.2290|issn=0962-8452|pmc=PMC2871843|pmid=20106851}}</ref><ref>{{Cite journal|last=Silva|first=K.|last2=Almada|first2=V.C.|last3=Vieira|first3=M.N.|last4=Monteiro|first4=N.M.|date=2009|title=Female reproductive tactics in a sex-role reversed pipefish: scanning for male quality and number|url=https://academic.oup.com/beheco/article-lookup/doi/10.1093/beheco/arp058|journal=Behavioral Ecology|language=en|volume=20|issue=4|pages=768–772|doi=10.1093/beheco/arp058|issn=1465-7279}}</ref>. Recent research, especially whole-genome sequencing<ref name=":2" />, has allowed for a much greater understanding of the evolutionary history of Syngnathidae, but there is still plenty of room for the field to grow. Further investigations into the genetic mechanisms and selective motivation for the evolution of these traits in Syngnathidae can provide insight into the evolution of pregnancy separate from the female reproductive system.


==Classification==
==Classification==

Revision as of 23:33, 15 November 2021

Syngnathidae
Alligator pipefish, Syngnathoides biaculeatus
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Actinopterygii
Clade: Percomorpha
Order: Syngnathiformes
Superfamily: Syngnathoidea
Family: Syngnathidae
Rafinesque, 1810
Subfamilies and genera

See text

The Syngnathidae is a family of fish which includes seahorses, pipefishes, and seadragons (Phycodurus and Phyllopteryx). The name is derived from Greek, σύν (syn), meaning "together", and γνάθος (gnathos), meaning "jaw".[1] This fused jaw trait is something the entire family has in common.[2]

Description and biology

Syngnathids are found in temperate and tropical seas across the world. Most species inhabit shallow, coastal waters, but a few are known from the open ocean, especially in association with sargassum mats. They are characterised by their elongated snouts, fused jaws, the absence of pelvic fins, and by thick plates of bony armour covering their bodies. The armour gives them a rigid body, so they swim by rapidly fanning their fins. As a result, they are relatively slow compared with other fish but are able to control their movements with great precision, including hovering in place for extended periods.[3]

Uniquely, after syngnathid females lay their eggs, the male then fertilizes and carries the eggs during incubation, using one of several methods. Male seahorses have a specialized ventral brood pouch to carry the embryos, male sea dragons attach the eggs to their tails, and male pipefish may do either, depending on their species.[4] The most fundamental difference between the different lineages of the family Syngnathidae is the location of male brood pouch.[5] The two locations are on the tail (Urophori) and on the abdomen (Gastrophori).[6] There is also variation in Syngnathid pouch complexity with brood pouches ranging from simple ventral gluing areas to fully enclosed pouches.[7] In species with more developed, enclosed pouches it has been demonstrated that males directly provide their brood with not only nutrients[8] but also immunity to pathogens.[9] Syngnathids with more developed brood pouches are also known to be able to partially or completely abort a brood from a female with low fitness.[10]

A wide variety of mate choice and mating competition has been observed in Syngnathidae.[11] For example, Hippocampus fuscus exhibits conventional sex roles of males competing for female access[12] while Corythoichthys haematopterus is completely sex role reversed.[13] Most conventional sex role syngnathids are monogamous whereas sex role reversed species mostly exhibit polygamous behavior.[6]

Seahorses and pipefish also have a unique feeding mechanism, known as elastic recoil feeding. Although the mechanism is not well understood, seahorses and pipefish appear to have the ability to store energy from contraction of their epaxial muscles (used in upward head rotation), which they then release, resulting in extremely fast head rotation to accelerate their mouths towards unsuspecting prey.[14][15]

Evolution

Phylogenetic analysis implies that the most recent common ancestor of all syngnathids was likely pouchless. The family Solenostomidae (ghost pipefish) is a family in the order Syngnathiformes. Female ghost pipefish incubate their developing embryos inside fused pelvic fins. Evolutionary transitions from female to male care are practically nonexistent in teleosts, so brood pouches were likely not ancestral[16]. Genome sequencing supports this, revealing multiple different origins across and within different brood pouch types[17]. Oviparity was the ancestral trait, and the evolution of viviparity must have relied on the evolution and integration of multiple complex traits such as morphology, physiology, and behavior.


Syngnathidae was historically divided into two major lineages based on brood pouch location: Neophinae (located on the trunk) and Syngnathinae (located on the tail)[16]. Genome sequencing shows a parallel increase in brood pouch complexity in both Neophinae and Syngnathinae[17]. Some species may have also independently evolved to have trunk brooding phenotypes, separate from the Neophinae. One example of this convergent evolution arises in pygmy seahorses (Hippocampus bargibanti, Hippocampus denise, Hippocampus pontohi). Pygmy seahorses are very small (about 1-2cm tall) trunk brooders, phylogenetically surrounded by tail brooders. It’s likely that the pygmy seahorse once had their brood pouch on their tail. The brood pouch may have moved locations when there was strong a correlated selection for a prehensile tail and diminutive size, resulting in a very small, trunk brooding organism[16].


Viviparity and male-pregnancy in Syngnathidae have a complex evolutionary history with many independent origins of similar traits. Early members of the family developed traits to limit the presence of deleterious mutations, allowing for more rapid evolution[18]. The advantage of a more controlled and protected embryonic development seemed to be enough to enact evolutionary development throughout Syngnathidae to varying degrees. In species with the most complex brood pouch systems, many traits (behavioral, physiological, morphological, and immunological) coevolved to allow for male pregnancy, greatly increasing the fitness of those individuals’ offspring. The evolution of these traits resulted in a sex-role reversal in which females may exhibit competitive behavior for a mate[19][20]. Recent research, especially whole-genome sequencing[17], has allowed for a much greater understanding of the evolutionary history of Syngnathidae, but there is still plenty of room for the field to grow. Further investigations into the genetic mechanisms and selective motivation for the evolution of these traits in Syngnathidae can provide insight into the evolution of pregnancy separate from the female reproductive system.

Classification

Images

Wikimedia Commons has media related to Syngnathidae.

References

  1. ^ Hentschel, E., & Wagner, G. (1990). Zoologisches Wörterbuch. Tiernamen, allgemeinbiologische, anatomische, physiologische Termini und biographische Daten (4th edition). Stuttgart: Gustav Fischer.
  2. ^ Sara A. Lourie, Amanda C.J. Vincent and Heather J. Hall: Seahorses: An Identification Guide to the World's Species and their Conversation. London: Project Seahorse, 1999
  3. ^ Orr, J.W & Pietsch, T.W. (1998). Paxton, J.R. & Eschmeyer, W.N. (eds.). Encyclopedia of Fishes. San Diego: Academic Press. pp. 168–169. ISBN 0-12-547665-5.
  4. ^ "Seahorses and their relatives". NSW Department of Primary Industries - Fisheries. Archived from the original on 2008-05-01. Retrieved 2008-06-13.
  5. ^ Hamilton, H., N. Saarman, G. Short, A. B. Sellas, B. Moore, T. Hoang, C. L. Grace, M. Gomon, et al. 2016. Molecular phylogeny and patterns of diversification in syngnathid fishes. Molecular Phylogenetics and Evolution. In press. http://dx.doi.org/10.1016/j.ympev.2016.10.003.
  6. ^ a b Wilson, A. B., I. Ahnesjö, A. C. J. Vincent, and A. Meyer. 2003. The dynamics of male brooding, mating patterns, and sex roles in pipefishes and seahorses (Family Syngnathidae). Evolution 57:1374–1386.
  7. ^ Dawson, C. E. 1985. Indo-Pacific pipefishes (Red Sea to the Americas). Gulf Coast Research Laboratory, Ocean Springs, MS. [as cited by Wilson et al. (2003)]
  8. ^ Ripley, J. L., and C. M. Foran. 2008. Direct evidence for embryonic uptake of paternally-derived nutrients in two pipefishes (Syngnathidae: Syngnathus spp.). Journal of Comparative Physiology B 179:325–333.
  9. ^ Roth, O., V. Klein, A. Beemelmanns, J. P. Scharsack, and T. B. H. Reusch. 2012. Male pregnancy and biparental immune priming. The American Naturalist 180:802–814.
  10. ^ Paczolt, K. A., and A. G. Jones. 2010. Post-copulatory sexual selection and sexual conflict in the evolution of male pregnancy. Nature 464:401–404.
  11. ^ Rosenqvist, G., and A. Berglund. 2011. Sexual signals and mating patterns in Syngnathidae. Journal of Fish Biology 78:1647-1661.
  12. ^ Vincent, A. C. J. 1994. Seahorses exhibit conventional sex roles in mating competition, despite male pregnancy. Behaviour 128:135–151.
  13. ^ Sogabe, A., and Y. Yanagisawa. 2007. Sex-role reversal of a monogamous pipefish without higher potential reproductive rate in females. Proceedings of the Royal Society B: Biological Sciences 274:2959–2963.
  14. ^ Van Wassenbergh et al., J. R. Soc. Interface 5:285(2008)
  15. ^ Van Wassenbergh et al., Biol. Lett. 5:200 (2009)
  16. ^ a b c Whittington, Camilla M.; Friesen, Christopher R. (2020-10). "The evolution and physiology of male pregnancy in syngnathid fishes". Biological Reviews. 95 (5): 1252–1272. doi:10.1111/brv.12607. ISSN 1464-7931. {{cite journal}}: Check date values in: |date= (help)
  17. ^ a b c Hamilton, Healy; Saarman, Norah; Short, Graham; Sellas, Anna B.; Moore, Beth; Hoang, Tinya; Grace, Christopher L.; Gomon, Martin; Crow, Karen; Brian Simison, W. (2017-02). "Molecular phylogeny and patterns of diversification in syngnathid fishes". Molecular Phylogenetics and Evolution. 107: 388–403. doi:10.1016/j.ympev.2016.10.003. {{cite journal}}: Check date values in: |date= (help)
  18. ^ Wang, Xin; Zhang, Yanhong; Zhang, Huixian; Qin, Geng; Lin, Qiang (2019-12). "Complete mitochondrial genomes of eight seahorses and pipefishes (Syngnathiformes: Syngnathidae): insight into the adaptive radiation of syngnathid fishes". BMC Evolutionary Biology. 19 (1): 119. doi:10.1186/s12862-019-1430-3. ISSN 1471-2148. PMC 6560779. PMID 31185889. {{cite journal}}: Check date values in: |date= (help)CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  19. ^ Goncalves, Ines Braga; Mobley, Kenyon B.; Ahnesjö, Ingrid; Sagebakken, Gry; Jones, Adam G.; Kvarnemo, Charlotta (2010-05-22). "Reproductive compensation in broad-nosed pipefish females". Proceedings of the Royal Society B: Biological Sciences. 277 (1687): 1581–1587. doi:10.1098/rspb.2009.2290. ISSN 0962-8452. PMC 2871843. PMID 20106851.{{cite journal}}: CS1 maint: PMC format (link)
  20. ^ Silva, K.; Almada, V.C.; Vieira, M.N.; Monteiro, N.M. (2009). "Female reproductive tactics in a sex-role reversed pipefish: scanning for male quality and number". Behavioral Ecology. 20 (4): 768–772. doi:10.1093/beheco/arp058. ISSN 1465-7279.

External links

Wikispecies has information related to Syngnathidae.
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