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<mods:title id="2E2869535C96173C6B9E331C6E5004C3">Protandric simultaneous hermaphroditism in Salmoneus carvachoi Anker, 2007 (Decapoda: Alpheidae): a new sexual system in alpheid shrimps</mods:title>
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<heading id="D0B2686EFF87FFB9FEAFD751FDA2B825" box="[332,543,1326,1353]" centered="true" fontSize="9" level="2" pageId="9" pageNumber="10" reason="2">
<taxonomicName id="4C45A481FF87FFB9FEAFD751FDA2B825" ID-CoL="85XZX" box="[332,543,1326,1353]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="species" species="carvachoi">
<emphasis id="B9310310FF87FFB9FEAFD751FDA2B825" bold="true" box="[332,543,1326,1353]" italics="true" pageId="9" pageNumber="10">Salmoneus carvachoi</emphasis>
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<paragraph id="8BFADF02FF87FFB9FF92D72AFAFABC6A" blockId="9.[113,763,1295,1609]" lastBlockId="9.[810,1459,144,1609]" pageId="9" pageNumber="10">
Sex determination based on the presence/absence of the
<emphasis id="B9310310FF87FFB9FD39D729FE9CB8E1" italics="true" pageId="9" pageNumber="10">ap&amp; pendio masculina</emphasis>
is not possible in some alpheid genera, in contrast to most caridean shrimps* For instance, the
<emphasis id="B9310310FF87FFB9FD43D7EBFF6EB8A7" italics="true" pageId="9" pageNumber="10">appendio masculina</emphasis>
(AM) is absent in all individuals in the alpheid genera
<taxonomicName id="4C45A481FF87FFB9FF92D7ACFED7B887" authority="De Man, 1888" authorityName="De Man" authorityYear="1888" box="[113,362,1491,1515]" class="Malacostraca" family="Alpheidae" genus="Automate" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="genus">
<emphasis id="B9310310FF87FFB9FF92D7ACFF6DB886" box="[113,208,1491,1514]" italics="true" pageId="9" pageNumber="10">Automate</emphasis>
De Man, 1888
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and
<taxonomicName id="4C45A481FF87FFB9FE78D7ACFF25BB66" pageId="9" pageNumber="10">
<emphasis id="B9310310FF87FFB9FE78D7ACFDB4B887" box="[411,521,1491,1515]" italics="true" pageId="9" pageNumber="10">Synalpheus</emphasis>
Spence Bate, 1888 species
</taxonomicName>
(Banner and Banner 1973, Felder 1982,
<bibRefCitation id="EFD4A2F3FF87FFB9FDBDD78DFD48BB66" author="Dardeau MR" box="[606,757,1522,1546]" pageId="9" pageNumber="10" pagination="1 - 125" refId="ref12584" refString="Dardeau MR * Synalpheus shrimps (Crustacea: Decapoda: Alpheidae) * I * Ne gambarelloides group, with a description of a new species * Memoirs of the Hourglass Cruises 1984; 2: 1 - 125 *" type="journal article" year="1984">Dardeau 1984</bibRefCitation>
,
<bibRefCitation id="EFD4A2F3FF87FFB9FF92D46EFEADBB45" author="Carvacho A" box="[113,272,1553,1577]" pageId="9" pageNumber="10" pagination="253 - 6" refId="ref12414" refString="Carvacho A * Sur l'appendix masculina chez Salmoneus (Decapoda, Alpheidae) * Crustaceana 1989; 57: 253 - 6 *" type="journal article" year="1989">Carvacho 1989</bibRefCitation>
,
<bibRefCitation id="EFD4A2F3FF87FFB9FEFED46EFE41BB45" author="Toth E &amp; Bauer RT" box="[285,508,1553,1577]" pageId="9" pageNumber="10" pagination="1875 - 86" refId="ref13750" refString="Toth E, Bauer RT * Gonopore sexing technique allows determination of sex ratios and helper composition in eusocial shrimps * Marine Biology 2007; 151: 1875 - 86 *" type="journal article" year="2007">Tóth and Bauer 2007</bibRefCitation>
)* On the other hand, in
<taxonomicName id="4C45A481FF87FFB9FF92D44EFF64BB25" authorityName="Holthuis" authorityYear="1955" box="[113,217,1585,1609]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="genus">
<emphasis id="B9310310FF87FFB9FF92D44EFF64BB25" box="[113,217,1585,1609]" italics="true" pageId="9" pageNumber="10">Salmoneus</emphasis>
</taxonomicName>
and
<taxonomicName id="4C45A481FF87FFB9FEEAD44EFDB6BB25" authority="Kensley, 1988" authorityName="Kensley" authorityYear="1988" box="[265,523,1585,1609]" class="Malacostraca" family="Alpheidae" genus="Yagerocaris" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="genus">
<emphasis id="B9310310FF87FFB9FEEAD44EFECBBB24" box="[265,374,1585,1608]" italics="true" pageId="9" pageNumber="10">Yagerocaris</emphasis>
Kensley, 1988
</taxonomicName>
, the AM is present in all
<pageTitle id="CBDA0765FF87FFB9FCC9D2EFFA0EBDC4" box="[810,1459,144,168]" pageId="9" pageNumber="10">individuals regardless of the presence or absence of eggs brooded</pageTitle>
in their pleon (
<bibRefCitation id="EFD4A2F3FF87FFB9FC2ED2D0FB21BDAB" author="Christoffersen ML" box="[973,1180,175,199]" pageId="9" pageNumber="10" pagination="93 - 112" refId="ref12540" refString="Christoffersen ML * Distribution of warm water alpheoid shrimps (Crustacea, Caridea) on the continental shelf of eastern South America between 23 ° and 35 ° Lat * S * Boletim do Instituto Oceanografico 1982; 31: 93 - 112 *" type="journal article" year="1982">Christoffersen 1982</bibRefCitation>
,
<bibRefCitation id="EFD4A2F3FF87FFB9FB48D2D0FAF7BDAB" author="Carvacho A" box="[1195,1354,175,199]" pageId="9" pageNumber="10" pagination="253 - 6" refId="ref12414" refString="Carvacho A * Sur l'appendix masculina chez Salmoneus (Decapoda, Alpheidae) * Crustaceana 1989; 57: 253 - 6 *" type="journal article" year="1989">Carvacho 1989</bibRefCitation>
,
<bibRefCitation id="EFD4A2F3FF87FFB9FABAD2D0FCE3BD8B" author="Holthuis LB" pageId="9" pageNumber="10" pagination="109 - 13" refId="ref12971" refString="Holthuis LB * Notes on Salmoneus arubae (Schmiu, 1936) (Crustacea, Decapoda, Caridea) * Beaufortia 1990; 41: 109 - 13 *" type="journal article" year="1990">Holthuis 1990</bibRefCitation>
,
<bibRefCitation id="EFD4A2F3FF87FFB9FC89D2B0FC48BD8B" author="Fransen CHJM" box="[874,1013,207,231]" pageId="9" pageNumber="10" pagination="171 - 9" refId="ref12744" refString="Fransen CHJM * Salmoneus sketi, a new species of alpheid shrimp (Crustacea: Decapoda: Caridea) from a submarine cave in the Adriatic * Zoologische Mededelingen 1991; 65: 171 - 9 *" type="journal article" year="1991">Fransen 1991</bibRefCitation>
, Anker and Marin 2006, Anker 2007, 2010, 2011a, b, Olivera
<emphasis id="B9310310FF87FFB9FC3FD290FBB8BC6A" box="[988,1029,238,262]" italics="true" pageId="9" pageNumber="10">et al</emphasis>
* 2015, Vera-Caripe
<emphasis id="B9310310FF87FFB9FB2CD290FB4ABC6A" box="[1231,1271,238,262]" italics="true" pageId="9" pageNumber="10">et al</emphasis>
* 2015)*
</paragraph>
<paragraph id="8BFADF02FF87FFB9FCA6D372FBE5BEF4" blockId="9.[810,1459,144,1609]" pageId="9" pageNumber="10">
<bibRefCitation id="EFD4A2F3FF87FFB9FCA6D372FC41BC49" author="Carvacho A" box="[837,1020,269,293]" pageId="9" pageNumber="10" pagination="253 - 6" refId="ref12414" refString="Carvacho A * Sur l'appendix masculina chez Salmoneus (Decapoda, Alpheidae) * Crustaceana 1989; 57: 253 - 6 *" type="journal article" year="1989">Carvacho (1989)</bibRefCitation>
stated that if the presence of the AM in
<taxonomicName id="4C45A481FF87FFB9FCC9D352FC2FBC29" authorityName="Holthuis" authorityYear="1955" box="[810,914,301,325]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="genus">
<emphasis id="B9310310FF87FFB9FCC9D352FC2FBC29" box="[810,914,301,325]" italics="true" pageId="9" pageNumber="10">Salmoneus</emphasis>
</taxonomicName>
was an expression of protandry, then, a gradual regression of this structure should be expected asser sexual inversion* Otherwise, it could not be a character indicating the sex of an individual in
<taxonomicName id="4C45A481FF87FFB9FC13D3F4FBE5BCCF" authority="Here" authorityName="Holthuis" authorityYear="1955" box="[1008,1112,395,419]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="genus">
<emphasis id="B9310310FF87FFB9FC13D3F4FBE5BCCF" box="[1008,1112,395,419]" italics="true" pageId="9" pageNumber="10">Salmoneus</emphasis>
</taxonomicName>
* Here we confirm that the AM is not useful for sex determination (e*g*, male-phase or hermaphrodite) in
<taxonomicName id="4C45A481FF87FFB9FC98D3B5FC52BC8D" box="[891,1007,457,481]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="species" species="carvachoi">
<emphasis id="B9310310FF87FFB9FC98D3B5FC52BC8D" box="[891,1007,457,481]" italics="true" pageId="9" pageNumber="10">S. carvachoi</emphasis>
</taxonomicName>
, as it is in most carideans (see: Bauer 2004)* Asser sex change, there is no reduction in size or changes in the shape of the AM in this species* Our results showed that despite the negative allometric growth of the AM in both sexual phases, hermaphrodite shrimps have a longer AM than male-phase individuals* Experimental studies in gonochoric caridean species, in which pleopodal rami, presumably possessing copulatory function (e*g*, AM), have been ablated in males, have demonstrated the importance of the AM in sperm transfer (Bauer 1976,
<bibRefCitation id="EFD4A2F3FF87FFB9FA60D0BBFC5ABF97" author="Berg ABV &amp; Sandifer PA" pageId="9" pageNumber="10" pagination="417 - 24" refId="ref12219" refString="Berg ABV, Sandifer PA * Mating behavior of the grass shrimp Palaemonetes pugio Holthuis, 1949 (Decapoda, Caridea) * Journal of Crustacean Biology 1984; 4: 417 - 24 *" type="journal article" year="1984">Berg and Sandifer 1984</bibRefCitation>
)* In the aforementioned experiments, males that had their AM ablated did not transfer spermatophores as efficiently as normal males with intact AM* However, there is still no experimental evidence that the maintenance of the AM in the hermaphrodite phase of
<taxonomicName id="4C45A481FF87FFB9FBC4D11EFB20BE14" box="[1063,1181,864,888]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="species" species="carvachoi">
<emphasis id="B9310310FF87FFB9FBC4D11EFB20BE14" box="[1063,1181,864,888]" italics="true" pageId="9" pageNumber="10">S. carvachoi</emphasis>
</taxonomicName>
is related to more efficient sperm transfer during mating*
</paragraph>
<paragraph id="8BFADF02FF87FFB9FCA6D1E0FCD6B887" blockId="9.[810,1459,144,1609]" pageId="9" pageNumber="10">
Ŋe determination of different sexual forms based on secondary sexual characters in the studied species was only possible through the visualization of the gonopores using SEM* We noted that the visualization of the gonopores using a stereomicroscope is impractical in
<taxonomicName id="4C45A481FF87FFB9FBBAD662FB6CB958" box="[1113,1233,1052,1076]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="species" species="carvachoi">
<emphasis id="B9310310FF87FFB9FBBAD662FB6CB958" box="[1113,1233,1052,1076]" italics="true" pageId="9" pageNumber="10">S. carvachoi</emphasis>
</taxonomicName>
due to the small size of the species, which prevents reliable sex identification from simple protocols commonly used in other carideans (
<bibRefCitation id="EFD4A2F3FF87FFB9FAB5D623FC02B9FF" author="Berg ABV &amp; Sandifer PA" pageId="9" pageNumber="10" pagination="417 - 24" refId="ref12219" refString="Berg ABV, Sandifer PA * Mating behavior of the grass shrimp Palaemonetes pugio Holthuis, 1949 (Decapoda, Caridea) * Journal of Crustacean Biology 1984; 4: 417 - 24 *" type="journal article" year="1984">Berg and Sandifer 1984</bibRefCitation>
, Bauer 2004)* Male-phase individuals possess only male gonopores, whereas simultaneous hermaphrodites exhibit both male and female gonopores* Such a paưern has also been observed in other PSH species belonging to the families
<taxonomicName id="4C45A481FF87FFB9FCC9D687FBA3B87C" authority="Dana, 1852" authorityName="Dana" authorityYear="1852" box="[810,1054,1272,1296]" class="Malacostraca" family="Lysmatidae" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="family">Lysmatidae Dana, 1852</taxonomicName>
and
<taxonomicName id="4C45A481FF87FFB9FBB0D687FA0EB87C" authority="Christoffersen, 1987" authorityName="Christoffersen" authorityYear="1987" box="[1107,1459,1272,1296]" class="Malacostraca" family="Barbouriidae" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="family">Barbouriidae Christoffersen, 1987</taxonomicName>
(
<bibRefCitation id="EFD4A2F3FF87FFB9FCD6D767FBA4B843" author="Bauer RT &amp; Holt GJ" box="[821,1049,1303,1327]" pageId="9" pageNumber="10" pagination="223 - 35" refId="ref12103" refString="Bauer RT, Holt GJ * Simultaneous hermaphroditism in the marine shrimp Lysmata wurdemanni (Caridea: Hippolytidae): an undescribed sexual system in the decapod Crustacea * Marine Biology 1998; 132: 223 - 35 *" type="journal article" year="1998">Bauer and Holt 1998</bibRefCitation>
,
<bibRefCitation id="EFD4A2F3FF87FFB9FBCAD767FB1EB843" author="Bauer RT" box="[1065,1187,1303,1327]" pageId="9" pageNumber="10" pagination="430 - 8" refId="ref12039" refString="Bauer RT * Same sexual system but variable sociobiology: evolution of protandric simultaneous hermaphroditism in Lysmata shrimps * Integrative and Comparative Biology 2006; 46: 430 - 8 *" type="journal article" year="2006">Bauer 2006</bibRefCitation>
, Baeza 2009, Braga
<emphasis id="B9310310FF87FFB9FA63D767FA10B843" box="[1408,1453,1303,1327]" italics="true" pageId="9" pageNumber="10">et al</emphasis>
* 2009, Onaga
<emphasis id="B9310310FF87FFB9FC51D748FC66B822" box="[946,987,1334,1358]" italics="true" pageId="9" pageNumber="10">et al</emphasis>
* 2012)* It is important to mention that we observed spermatophore residues containing spermatozoa in the male gonopore of a hermaphrodite that was brooding eggs* Ŋis observation supports the hypothesis that the male reproductive system in simultaneous hermaphrodites of
<taxonomicName id="4C45A481FF87FFB9FB0AD7CBFAE2B8A0" box="[1257,1375,1460,1484]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="species" species="carvachoi">
<emphasis id="B9310310FF87FFB9FB0AD7CBFAE2B8A0" box="[1257,1375,1460,1484]" italics="true" pageId="9" pageNumber="10">S. carvachoi</emphasis>
</taxonomicName>
is functional*
</paragraph>
<paragraph id="8BFADF02FF87FFB9FCA6D78DFA0EBB25" blockId="9.[810,1459,144,1609]" pageId="9" pageNumber="10">
Although we provide considerable evidence that supports PSH in
<taxonomicName id="4C45A481FF87FFB9FC9CD46DFC4BBB46" box="[895,1014,1554,1578]" class="Malacostraca" family="Alpheidae" genus="Salmoneus" higherTaxonomySource="GBIF" kingdom="Animalia" order="Decapoda" pageId="9" pageNumber="10" phylum="Arthropoda" rank="species" species="carvachoi">
<emphasis id="B9310310FF87FFB9FC9CD46DFC4BBB46" box="[895,1014,1554,1578]" italics="true" pageId="9" pageNumber="10">S. carvachoi</emphasis>
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, experimental studies are necessary to test that the simultaneous hermaphrodites are functional, i*e*, capable
</paragraph>
<paragraph id="8BFADF02FF87FFB9FF93D4F4FC5FBAD7" blockId="9.[112,1457,1675,1979]" pageId="9" pageNumber="10">
with spermatozoa immersed in the secretion
<typeStatus id="54FE61A0FF87FFB9FDF5D4F4FDFDBBCF" box="[534,576,1675,1699]" pageId="9" pageNumber="10">type</typeStatus>
I surrounded by the secretion
<typeStatus id="54FE61A0FF87FFB9FC82D4F4FC36BBCF" box="[865,907,1675,1699]" pageId="9" pageNumber="10">type</typeStatus>
II (arrow)* G, detail of the spermatozoon with tack morphology and a long spike* Ŋe secretion
<typeStatus id="54FE61A0FF87FFB9FDF1D4D8FD81BBD3" box="[530,572,1703,1727]" pageId="9" pageNumber="10">type</typeStatus>
I shows small granules, thin fibrils and some larger droplets (arrow)* H, thick musculature of the ampoule with many muscular fibres* Ŋe primordial spermatophore shows small amount of seminal fluid of the secretion
<typeStatus id="54FE61A0FF87FFB9FAC3D4BCFAF7BBB7" box="[1312,1354,1731,1755]" pageId="9" pageNumber="10">type</typeStatus>
I and is surrounded by a thin layer of secretion
<typeStatus id="54FE61A0FF87FFB9FE03D4A0FDB7BB9B" box="[480,522,1759,1783]" pageId="9" pageNumber="10">type</typeStatus>
II (arrow)* I, male phase individual showing ovaries and testes forming the ovotestes, surrounded by blood capillaries (arrow)* Ŋe ovaries are filled with oogonia forming the germinal centre at the inner periphery of the ovarian lobe close the testes* Ŋe primary oocytes occupy the rest of the lobule while the spermatogenesis is still producing spermatozoa (arrowhead)* J, detail of the oogonia and primary oocytes arrested in the previtellogenic stage surrounded by follicle cells (black arrowhead)* Notice primary spermatocytes and spermatozoa (white arrowhead) in the testes* K, primordial ovaries found in male phase individuals* Ŋe ovarian wall cells are arranged in different strata around the ovary lumen forming a mandibulate
<typeStatus id="54FE61A0FF87FFB9FC61D514FC11BAEF" box="[898,940,1899,1923]" pageId="9" pageNumber="10">type</typeStatus>
ovary* Detail of the ovarian wall cells showing long microvilli (arrowhead)* Ŋese cells are laying on the connective tissue shared with the testes* IL, haematoxylin and eosin stain* M, ovarian wall cells with nucleus with mitotic prophase chromosome (arrow heads)* Toluidine blue stain* A *
</paragraph>
</subSubSection>
</treatment>
</document>