Environmental determination of sex in Apistogrammai (Cichlidae) and two other freshwater fishes (Teleostei)

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  • Journal of Fish Biology (1996) 48, 714725

    Environmental determination of sex in Apistogramma(Cichlidae) and two other freshwater fishes (Teleostei)

    U. Romer and W. BeisenherzUniversity of Bielefeld, Department of Biology, Postfach 100131, 33501 Bielefeld,

    Germany

    (Received 15 July 1994, Accepted 30 June 1995)

    Environmental sex determination by temperature could be revealed significantly in 33Apistogramma-species and in Poecilia melanogaster. In some, but not all, Apistogramma-speciespH also influences the sex ratio, whereas neither temperature nor pH aVect the sex ratio ofPseudocrenilabrus multicolor victoriae. The sex in oVspring of A. trifasciata is determinedwithin a sensitive period of about 30 to at least 40 days after spawning.

    ? 1996 The Fisheries Society of the British Isles

    Key words: Apistogramma; Cichlidae; environmental sex determination; pH; sex ratio;temperature.

    INTRODUCTION

    Sex is determined in reptiles by at least two diVerent mechanisms, one genotypicand the other environmental (Bull, 1980). In fish a genetic mechanism for sexdetermination was proposed long ago by Aida (1921). Since then it has beenestablished for most species which have been examined (Price, 1984). Determi-nation of sex by environmental factors after conception seems to be rare.Environmental factors such as pH in some cichlids and a poecilid (Rubin, 1985),and temperature in Menidia menidia (L.) (Conover & Kynard, 1981), M.peninsula Goode & Bean (Middaugh & Hemmer, 1987) and Poeciliopsis lucidaMiller (Sullivan & Schultz, 1986; Schultz, 1993) have been shown to influence sexratio, too. Hints in the aquarium literature motivated our investigations of theinfluence of temperature and pH on sex ratio in Apistogramma (Teleostei,Cichlidae). The objective of this article is to present further data in regard toenvironmental sex determination (ESD) in fish as this seems to be more commonthan currently appreciated.

    MATERIALS AND METHODS

    Thirty-seven species of Apistogramma, a genus of neotropical cichlids, Pseudo-crenilabrus multicolor victoriae Seegers, an African mouth-breeding cichlid, and Poecilia(Limia) melanogaster (Gnther), a Jamaican live-bearing poecilid (Table I), were used forthis study. Nomenclature of Apistogramma-species follows Ufermann et al. (1987). Allfish were of known geographical origin which might be of special importance for furtherecological investigation.Generally, specimens taken from the wild and their F1-progeny were used for the

    experiments with Apistogramma-species. There was no significant diVerence in sex ratioof oVspring in specimens from diVerent imports or strains of long-time inbred laboratory-stocks (F12 up to F15). Pseudocrenilabrus m. victoriae were F1-progeny of specimens

    714

    00221112/96/040714+12 $18.00/0 ? 1996 The Fisheries Society of the British Isles

  • TableI.Meanpercentageofmaleswithinbroodsof39Teleostei

    Species

    23)C

    26)C

    29)C

    pH45

    pH55

    pH65

    pH45

    pH55

    pH65

    pH45

    pH55

    pH65

    Apistogramma

    agassizii(Steindachner)

    422

    (1)

    773

    (7)

    602

    (1)

    901

    (1)

    730

    (6)

    borellii(Regan)

    396

    (1)

    371

    (3)

    328

    (1)

    684

    (2)

    539

    (2)

    684

    (2)

    854

    (1)

    736

    (4)

    614

    (1)

    cacatuoidesHoedeman

    198

    (5)

    843

    (5)

    627

    (5)

    433

    (5)

    830

    (5)

    caeteiKullander

    599

    (5)

    533(12)

    38(1)

    437

    (3)

    480(14)

    145

    (8)

    375

    (3)

    520

    (9)

    44(10)

    diplotaeniaKullander

    554

    (1)

    439

    (3)

    530

    (2)

    988

    (1)

    799

    (4)

    eunotusKullander

    447

    (2)

    385

    (2)

    311

    (2)

    634

    (1)

    534

    (3)

    412

    (2)

    766

    (2)

    641

    (2)

    668

    (2)

    geisleriMeinken

    287

    (2)

    509

    (3)

    824

    (2)

    gephyraKullander

    458

    (3)

    406

    (3)

    355

    (3)

    657

    (3)

    561

    (3)

    392

    (3)

    780

    (3)

    624

    (3)

    668

    (3)

    gibbicepsMeinken

    192

    (3)

    689

    (2)

    536

    (2)

    351

    (2)

    926

    (2)

    820

    (2)

    760

    (2)

    gosseiKullander

    287

    (2)

    492

    (2)

    814

    (2)

    hippolytaeKullander

    377

    (1)

    533

    (2)

    494

    (1)

    932

    (1)

    857

    (2)

    hoigneiMeinken

    309

    (3)

    817

    (4)

    hongsloiKullander

    354

    (3)

    293

    (3)

    236

    (3)

    616

    (3)

    275

    (3)

    144

    (3)

    928

    (3)

    796

    (3)

    815

    (4)

    inconspicuaKullander

    389

    (2)

    272

    (2)

    167

    (2)

    768

    (2)

    iniridaeKullander

    344

    (3)

    796

    (2)

    linkeiKoslowski

    159(17)

    662

    (7)

    492

    (7)

    342

    (6)

    889(13)

    luelingiKullander

    300

    (2)

    885

    (2)

    macmasteriKullander

    304

    (2)

    509

    (2)

    867

    (2)

    meinkeniKullander

    475

    (1)

    376

    (2)

    404

    (1)

    603

    (1)

    554

    (2)

    459

    (1)

    687

    (1)

    652

    (2)

    609

    (1)

  • TableI.Continued

    Species

    23)C

    26)C

    29)C

    pH45

    pH55

    pH65

    pH45

    pH55

    pH65

    pH45

    pH55

    pH65

    Apistogramma

    mendeziRm

    er

    358

    (2)

    872

    (2)

    nijsseniKullander

    144(14)

    99(12)

    75(13)

    587(20)

    496(24)

    459(21)

    948(12)

    850(18)

    755(16)

    norbertiStaeck

    319

    (2)

    273

    (2)

    157

    (2)

    714

    (2)

    533

    (2)

    311

    (2)

    892

    (3)

    ortmanni(Eigenmann)

    250

    (2)

    488

    (1)

    829

    (2)

    paucisquamisKullander&Staeck

    432

    (2)

    311

    (2)

    672

    (1)

    529

    (1)

    411

    (1)

    763

    (2)

    670

    (2)

    pertensis(Haseman)

    293

    (6)

    764

    (6)

    resticulosaKullander

    505

    (2)

    257

    (2)

    387

    (2)

    903

    (2)

    759

    (2)

    staeckiKoslowski

    278

    (2)

    543

    (2)

    915

    (2)

    steindachneri(Regan)

    411

    (3)

    193

    (3)

    909

    (4)

    770

    (2)

    trifasciata(Eigenmann&Kennedy)

    168(15)

    490(15)

    859(15)

    uaupesiKullander

    349

    (3)

    264

    (3)

    817

    (3)

    588

    (2)

    975

    (3)

    838

    (2)

    Breitbindensp.*

    263

    (5)

    792

    (2)

    685

    (2)

    893

    (5)

    650

    (1)

    Gelbwangensp.*

    311

    (3)

    706

    (2)

    Orangeschwanzsp.*

    343

    (3)

    611

    (1)

    333

    (1)

    672

    (3)

    PuertoNarinosp.*

    266

    (3)

    796

    (3)

    RioBrancosp.*

    378

    (3)

    674

    (3)

    Rotpunktsp.*

    384

    (2)

    259

    (3)

    509

    (3)

    360

    (2)

    849

    (2)

    773

    (1)

    622

    (2)

    Smaragdsp.*

    667

    (2)

    626

    (2)

    762

    (2)

    759

    (1)

    615

    (1)

    756

    (2)

    849

    (2)

    Poecilia

    (Limia)

    melanogasterSeegers

    46(15)

    41(15)

    29(10)

    59(12)

    49(14)

    38(25)

    71(10)

    67(18)

    58(17)

    Pseudocrenilabrus

    m.victoriae(Gnther)

    483(29)

    507(35)

    503(29)

    477(34)

    539(43)

    491(55)

    516(19)

    464(12)

    525(17)

    Figuresinparenthesesindicatenumberofbroods.

    *Undescribedspecies.NamesusedinGerman

    aquarium

    literature.

  • caught in the wild by the subspecies-describer. Poecilia melanogaster used in ourinvestigations were descended from a laboratory-stock which was bred for about 25generations in captivity.All fish were bred in the laboratory at constant water conditions. Temperature, pH,

    and water hardness were measured electronically. Deviation in temperature was less than&02) C, deviation of pH less than &05. Water was purified by filtration and by weeklychanges of 30% of water. If water was changed it was brought to the experimentalconditions in advance. Manipulation of pH was established by humic acid, sodiumbiphosphate and sodium bicarbonate.For the experiments, pairs as well as groups of five males and 25 females were bred in

    150#50#40 cm tanks. No statistical diVerences of sex ratio were found between singlepairs and groups, for instance neither between 15 diVerent pairs of Apistogramma nijsseniKullander nor between four diVerent groups of A. linkei Koslowski. Spawning inartificial caves (46#30 mm, transparent boxes) was observed continually during thespawning period of about 48 h in temperature reversal experiments or at least daily instandard experiments by one of the authors (UR). The spawning period was regulated byfeeding the animals ad libitum with nauplii of brine shrimps (Artemia sp.). The numbersof eggs, larvae or fry were counted regularly. Females and clutches were transferred fromthe spawning tank to rearing tanks after fertilization. Females were removed from theirbrood after the oVspring became free swimming, which was usually after 7 to 10 daysfrom hatching.Fish were bred and raised at 23, 26 and 29) C, a

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