Reproductive Biology and Annual Variation of Reproductive Variables of Black Drum in the Northern Gulf of Mexico

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Reproductive Biology and Annual Variation of Reproductive Variables of Black Drum in the Northern Gulf of Mexico
  Transactions  of  the  merican  Fisheries  Society  122:318-327.  1993   Copyright by the American  Fisheries Society  1993 Reproductive  Biology  and  Annual  Variation  of Reproductive Variables  of  Black  Drum  in the  Northern Gulf  of  Mexico DAVID  L.  NIELAND  AND  CHARLES  A.  WILSON Coastal  Fisheries  Institute Center for Coastal,  Energy,  and  Environmental  Resources Louisiana  State  University,  Baton Rouge. Louisiana 70803-7503,  USA Abstract. —Black  drums  Pogonias  cromis  were  sampled  from  commercial and  recreational  catch- es in the northern  Gulf  of  Mexico  from  July  1987  to  September  1990. Seasonal  onset  of spawning,evidenced by the  presence  of  postovulatory  follicles  in  ovarian tissue  sections  and by  elevated gonadosomatic indices, occurred  in January of  each year  (one  female  with  hydrated  oocytes  was sampled in December 1988). Atretic  oocytes observed  in mid to late  April  indicated  imminent cessation  of  spawning.  Two of  115  females  less  than age 5 had  achieved  sexual  maturity; all  females age 5 and  older  were  mature.  Fifty  percent  maturity of  females  was  attained  at  640-649  mm  fork length  and all  females  larger  than  690 mm were  mature.  Male black  drums entered  the  breedingpopulation  at a  younger  age  (>50 maturity at age 4) and a smaller  size  (50%  maturity at  6JO- 620  mm .  Multiple  oocyte stages  observed  throughout the annual spawning  seasons  verified  group-synchronous  oocyte  development and multiple batch spawning. Estimated  batch  fecundities of 41 females with  hydrated  oocytes  ranged  from  0.51  million  to  2.42  million  ova.  Mean  batch  fecundi- ties  were  1.22  million ova for the  1988  spawning  season,  1.65  million  ova for  1989,  and  1.21 million  ova for  1990.  Batch  fecundity  was  positively  correlated  with  total  weight,  fork  length, eviscerated  body  weight,  and  age.  Spawning  frequencies  estimated  from  the  proportion  of mature females  with  postovulatory  follicles  were  one  spawning  event per 3.0 d in  1988,  one per 4.2 d in 1989,  and one per 3.9 d in  1990.  A  protracted  spawning  season,  generous batch fecundities, and frequent  spawning  provide  black  drums  with  annual  fecundities of 13 million to 67  million  ova.The black drum  Pogonias cromis  is a commonsciaenid of the western Atlantic Ocean ranging from  Massachusetts, USA, south to Argentina (Hoese  and  Moore 1977).  It is one of the  largest sciaenids,  weighing up to 68 kg (Bigelow andSchroeder 1953; Hoese  and  Moore 1977),  and it may  survive  to  50-60  years  of age in  parts  of its range (Murphy and Taylor  1989).  Specimens  from the northern Gulf of Mexico infrequently exceed20 kg or 40 years (Beckman et al. 1990). Blackdrums may reach maximum abundance in the ne- ritic  waters of the northern Gulf of Mexico adja-cent  to the  Mississippi River delta, where  we  haveseen immense schools estimated  by  experienced fishermen  to  consist  of hundreds of tons of  fish. Smaller schools are formed by black drums in-habiting  estuarine  areas.  The  schooling  behavior of  black drums  and the  accessibility  of the  waters they  inhabit contribute  to the  commercial  and  rec-reational importance  of the  species. Among  the  Sciaenidae,  several species, includ- ing  black drum (Fitzhugh et  al.,  in press), exhibitgroup-synchronous maturation  of  oocytes  and multiple,  or  batch, spawning. These  species  in- clude queen  fish  Seriphus  politus  (DeMartini  and Fountain  1981);  black croaker  Cheilotrema sa- turnum  (Goldberg 1981);  white croaker  Genyone- mus  lineatus  (Love et al. 1984); red drum  Sciaen ops  ocellatus  (Fitzhugh et al. 1988); and  spottedseatrout  Cynoscion nebulosus  (Brown-Peterson  et al.  1988).  For  such  species,  annual fecundity can- not be  estimated  from  the  standing crop  of vitel- logenic (yolked)  oocytes  because oocyte matura-tion  is a  continuing  process  and  spawning  batches are  produced throughout  the  spawning  season. Thus annual fecundity is a function of the length of  the  spawning  season,  the  number  of ova per spawn (batch fecundity),  and the  interval betweensuccessive spawnings (Hunter  et al.  1985).Various  aspects  of black drum reproduction in the  Gulf  of  Mexico have been summarized  by Pearson  (1929), Simmons  and  Breuer (1962),Fontenot and Rogillio (1970), Jannke  (1971),  Sil-verman  (1979), Cody  et al.  (1985),  and  Fitzhugh et al. (in  press). None  of  these authors used his- tological  techniques  to  describe  reproductive  ac- tivity over several successive spawning  seasons nor did  they discuss annual variation  of  repro-ductive variables. Herein  we  report  the  findingsof  a  39-month study, encompassing three spawn- ing  seasons, of age and length at sexual maturity,annual ovarian cycling, spawning season  and du- ration, annual and batch fecundities, and spawn-ing frequency, as well as year-to-year variation of 318  BLACK DRUM  REPRODUCTION 319 these  properties,  for  black  drums inhabiting  theestuarine and neritic waters of  Louisiana  and  Mis- sissippi. Methods Black  drums  were  sampled  monthly  from  either commercial  landings  or  recreational  tournamentcatches  from  July 1987  to  September  1990  except in  August  1987,  September  1989,  December  1989, and  August  1990.  Twice-monthly sampling  was frequently  employed during  January-April  to aug- ment  sample  sizes.  All black  drums  sampled  were captured  from  the  estuarine  and neritic  waters  ofLouisiana  and  Mississippi  from  Atchafalaya  Bay eastward to Mississippi  Sound,  including  Lakes Borgne  and  Pontchartrain. Fork  length (mm)  and  total  weight  (nearest  0.01 kg)  were  recorded  for  each  fish  sampled. Sagittal otoliths  were  removed  and  processed  for age  anal- ysis  as  described  by  Beckman  et  al.  (1990). Go- nads  were  excised,  placed individually into  num- bered  plastic bags,  and  packed  in ice for  transport to the laboratory. The  remaining  visceral organs were  removed and an  eviscerated  body  weight  to the  nearest  0.01  kg was  recorded. In  the laboratory,  testes  and  ovaries  were  cleaned of  extraneous nongonadal  tissue,  blotted  dry,  and weighed  to the  nearest  0.1 g.  Ovaries  were  fixed in  10 formalin  for at  least  2  weeks.  A  subsample of  fixed  ovarian tissue  (30-50  g) was  dissected  from one randomly  chosen ovarian  region  (three  regionsper  lobe: anterior,  medial, and  posterior).  Eachsubsample was  embedded  in  Paraplast (Sherwood Medical Industries)  and  sectioned  to 3  nm  thick- ness.  Sections  were  mounted  on  microscope  slides, stained  in Gill  hematoxylin,  and  counterstained in  eosin  Y. Oocytes  were  staged  and  counted  by micro-scopic  examination  of the  prepared  sections  at 40 x or  lOOx  magnification.  Four  maturation stages were  recognized in black drum  oocyte  develop- ment:  primary growth,  cortical  alveoli,  vitello- genic,  and  hydrated (Wallace  and Selman  1981). A  minimum  of 200  oocytes  per slide  were  staged in  randomly  chosen  fields.  Cells  with  less  than 50 of  their area  visible  in the  field  were not in-cluded in the  counts  (Fitzhugh et al.  1988;  Brown- Peterson  et al.  1988).  Each  slide was  also  scanned for  the  presence  of  atretic  follicles  and  postovu- latory  follicles.  Designation  of  atretic states  and characteristics  used in  determining  age of  posto- vulatory  follicles  followed  Hunter and Macewicz (1985). Maturation of  oocytes  to  vitellogenesis  during the spawning  season  was used to  identify  mature female  black  drums  (Hunter and  Goldberg  1980; Brown-Peterson et al. 1988;  Murphy  and Taylor 1989). Males  were  classified  mature  if  gentle squeezing  of the  testis  induced  milt  flow  from  the central  lumen  (Pearson  1929;  Brown-Peterson et al.  1988;  Murphy  and  Taylor  1989). Batch  fecundity  was  estimated  gravimetrically with  fresh  ovarian  weights as the  number  of hy- drated oocytes  present in the  ovary  (hydrated oo- cyte  method  of Hunter et al.  1985). When  thisresearch  began,  individual  batch  fecundity  was es-timated as the mean of 12  estimates  (replicate samples  from  each  of six  ovarian  regions).  Appli- cation  of analysis of  variance  (ANOVA)  and Dun- can's  multiple-range  test  to  data  from  six  females revealed  no  statistical  differences  in  estimates  be- tween  ovarian lobes,  among  ovarian  regions, or between  replicate samples.  Thereafter batch  fe- cundity  estimates  were  based  on  three  observa- tions  per  individual.  Batch fecundities were  esti- mated  for  41 female  black  drums. Spawning  frequency  was  estimated  with  the postovulatory  follicle  method  (Hunter and  Gold- berg 1980; Hunter and Macewicz 1985;  Hunter  et al.  1986)  after  examination  of 347  ovaries  col- lected during the  spawning  seasons.  All  observed postovulatory  follicles  were  presumed to be less than  24 h  old.  We have yet to document the de-generation of  black  drum  postovulatory  follicles over  time in  captive,  artificially  spawned  speci- mens,  but we  have  done  so  with  red  drum  (un- published  data).  None  of the  postovulatory  folli- cles  seen in  wild  black drums  approached  the degenerative  state  of red  drum  postovulatory  fol- licles 24 h  after  spawning.  Furthermore,  no black drum  postovulatory  follicles  had  assumed  the as- pect of age  1  day postovulatory  follicles  of northern  anchovy  Engraulis  mordax  described  and depicted  by  Hunter  et al. (1985).  Females  with ovaries  exhibiting  atretic  states  2  (alpha  atresia ofat least  half  the vitellogenic  oocytes)  and 3 (no vitellogenic  oocytes  present; beta atresia  present) were not  included  in  calculations  of spawning  fre- quency;  both states indicate  that the probability of  future  spawning  is  zero  (Hunter and Macewicz1985)  and  that  these  females had  effectively  left the  spawning  population. Relative  reproductive preparedness  of  mature black  drum was  assessed  with  gonadosomatic  in- dices  (GSI)  calculated  as GSI = (gonad  weight/ eviscerated  body  weight)  x  100.  Individual an- nual  fecundity  (AF) was  estimated  as AF =  320 NIELAND  AND WILSON (spawning  season  [100 d]/spawning interval  [d]) x  batch  fecundity. The  Statistical  Analysis  System  (SAS  Institute 1985)  was  used  for maximum-likelihood  analysis (PROBIT) to generate 50 maturity  schedules; for  ANOVA  and  Duncan's  multiple-range  tests  asnoted  above and to compare seasonal means of total  weight,  fork  length,  eviscerated  body  weight,age, and  batch  fecundity; for  linear  regression (GLM)  to predict  seasonal  and  overall  relation- ships  between  total  weight,  fork  length,  eviscer- ated  body  weight,  and age and  batch  fecundity; and for  analysis  of  covariance  (ANCOVA)  to compare  regressions  of  seasonal  relationships  be- tween  total  weight,  fork  length,  eviscerated  body weight,  and age and  batch  fecundity.  Significance level  for  statistical  analyses  was  0.05  unless  indi-cated otherwise. Results Over  the  duration  of the  study,  2,068  black drums (1,004  males,  1,064  females)  were  sampled from  commercial  and  recreational catches  in the northern  Gulf of  Mexico. Seasonally Male  and  female  gonadosomatic indices  and ovarian  histology  indicate  black  drums  in thenorthern  Gulf  of  Mexico  spawn  over  a  protracted period  of approximately 100 d  from  January to April. Monthly  mean gonadosomatic indices  for both  sexes  showed  a consistent  annual  cycle  (Fig- ure  1).  Minimum  mean  GSIs  of  mature  black drums  occurred  from  June  to  September  and av-eraged  0.23  for  males  and  1.05  for  females  during these  months.  Both  sexes exhibited  slight  increas- es in  GSI above  summer levels  in  October  and November and  more  abrupt  increases  in  Decem- ber and January.  Annual  GSI maxima were achieved in February and  March  of  each sampling year  and  were  followed  by  rapid declines  to  near minimum  levels  in  May. Black  drum ovaries  also exhibited a  consistent annual  cycle  of  oogenesis  and  recrudescence  (Fig- ure  2).  Primary  growth  oocytes  were  essentially ubiquitous  in  ovaries  of  immature  females  in all months and made up more  than  93 of the  oocyte populations  in  mature  females  from  May to Oc- tober. Maturation of primary  growth  oocytes  to the  cortical  alveoli stage began as  early  as Au- gust. Following  an  interval  of 1-3 months, vitel- logenic  oocytes  became  evident  in  November samples.  Maximum  proportions  of vitellogenic oocytes,  which  coincided  with  minimum  propor-tions  of  primary  growth  oocytes,  were  observed in  February and  March  of each year. Hydrated oocytes, transitory structures that immediately precede ovulation,  were  found  sporadically  from January  through April.Spawning,  definitively  evidenced  by  postovu- latory  follicles  in  histological  sections,  was  first detected  on  12  January  1988,  10 January  1989, and  19  January 1990.  Although  no  postovulatory follicles  were  observed  in  December samples,  hy- drated oocytes  in the  ovary  of a  female  collected 13  December  1988  indicated  the  probability  of earlier  spawning.  Proportional reductions of vi- tellogenic  oocytes  and concomitant  increases  of primary growth  oocytes  implied  cessation  ofspawning in  April  (Figure  2).  Furthermore, atresia of vitellogenic  oocytes  was  first  seen  in  April  of each  year and its  appearance coincided  with  a de- crease  in the  incidence  of  postovulatory  follicles. Ovaries  sampled  on 5  April 1988  exhibited  lim- ited  atresia  and 64 (14  of 22) of the  ovarian samples  included  postovulatory  follicles. On  19 April  1988,  advanced  atresia (atretic  states  2 and 3)  was  observed  in the  majority  of  ovaries  sam- pled and  only  4 of 23  exhibited postovulatory  fol- licles. Among  22  ovaries  collected  on 27  April 1988,  postovulatory  follicles were  lacking and all vitellogenic  oocytes  were  atretic.  Similar  patterns were  noted  during April  1989  and  April  1990. Age and  Length  at Maturity Few female black  drums  in the  northern  Gulf of  Mexico  mature  before  age 5  (Table  1).  Amongthe  combined  115  females  of  ages  2, 3, and 4  sam- pled  during  the spawning  seasons,  only  one  age-3 female  (630  mm,  4.40  kg  total  weight) and one age-4  female  (630  mm,  4.20  kg)  exhibited vitel-logenesis indicative  of  sexual  maturity.  All fe- males age 5 and  older  showed  varying  degrees  ofvitellogenesis  and  were  considered  to  have achieved  sexual  maturity. Minimum  female  lengthat maturity was 628 mm  (age  5). Maximum-like- lihood estimates  (PROBIT analysis,  Murphy  andTaylor 1989)  of 10-mm  fork  length  incrementsindicated  50%  female  maturity was reached at  640- 649 mm. All  females  larger  than  690 mm  were mature.Male black  drums  from  the  northern  Gulf  enter the  spawning  population  at somewhat  younger  age and at  slightly  smaller  size  than  females  (Table  1). Seven percent of age-3  males,  55 of age-4 males,and all  males  of age 5 and  older  were  mature. Minimum male  length  at maturity was 552 mm (age 3).  Fifty  percent  maturity  of  males  was at-  BLACK DRUM  REPRODUCTION 321 JASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJAS 1987  |  1988  |  1989  |  1990  onth Year FIGURE  I.—Monthly  mean gonadosomatic  indices  (GSI) for  mature  female  (asterisks)  and male  (squares) black drums  from  the northern Gulf of Mexico.  Monthly  sample  sizes  were  5-84  males and  2-68  females  (male  sample sizes  were  less  than  10 in  October  1987,  August  and  November 1988,  May 1989, and  February  and  July  1990; female  sample sizes  were  less  than 10 in  December  1987  and  February  and  August  1990). JASONDJFMAMJJASONDJFMAMJJASONDJFMAMJJAS1987  |  1988  |  1989  |  1990  onth Year FIGURE  2.—Monthly  percent occurrence  of primary growth  (asterisks),  cortical  alveoli  (large  squares),  vitellogenic (crosses),  and  hydrated  (small  squares)  oocyte  stages  in  ovarian tissue  of black  drums  from  the  nonhern  Gulf ofMexico. Monthly  sample  sizes  ranged  from  2 to 67  (sample  sizes  were  less  than 10 in  October  1987 and February and  August  1990).  322 NIELAND  AND  WILSON TABLE  1 .—Numbers  sampled  and  percent  maturity  (in parentheses)  of  female  and  male black  drums  in specified age-classes  and  sizes-classes.  Specimens  were  collected from  the  northern  Gulf  of  Mexico  during  December  1987- April  1988,  December  1988-April  1989, and  December 1989-April  1990.  Total  sample sizes  were 592  females and  541  males. Class Age (years) 1 2 3 4>5 Fork  length  (mm) 400-449 450-499 500-549 550-599 600-649650-699 >700 Female 0 3(0) 94(1) 18(6) 477(100) 2(0) 5(0)35(0) 43(0) 25(16) 46  (85) 436(100) Male 00 41(7) 1  1  (55) 489(100) 00 14(0) 20(15)19(37) 51  (100) 437(100) tained at  610-619  mm (PROBIT) and all  males larger  than  640 mm were mature. Batch  Fecundity Microscopic  examination of  preserved  ovarian tissue  from  prespawning  females  revealed  two  dis- tinct  classes  of  oocytes  typical of  group-synchro- nous  oocyte  development  and of a  multiple-  or batch-spawning  species  (Wallace  and Selman  1981; Hunter et al.  1985).  The  bulk  of each  ovarian  sam- ple  consisted  of small  (<0.5-mm-diameter),  var- iously  sized,  opaque  oocytes  (primary growth,  cor- tical alveoli, and  vitellogenic  stages).  Hydratedoocytes  were  less numerous in the  samples  and were  characterized  by  their  larger  size  (1  mm di- ameter) and  translucency. Batch  fecundity  estimates  for 41 females  (11  in1988,  18  in  1989,  and  12  in  1990) displaying  overtmacroscopic and microscopic  oocyte  hydration throughout  the  diameter  and  length  of the  ovarianlobes  ranged  from  0.51 million to 2.42 million ova per  batch,  averaging  1.41  million  ova.  Annual mean batch  fecundity  estimates  were  1.22  million ova in  1988, 1.65 million  ova in  1989,  and  1.21 million ova in 1990  (Table  2). Analysis of  vari- ance  of  annual  mean  ages,  total  weights,  eviscer-ated  weights,  fork  lengths,  and  batch  fecundities revealed  differences  only  among the  last:  batch fecundity was  significantly  greater  in  1989 than  in 1988  or 1990. The  lack  of  variation  among  sea- sonal  means  of the other  variables demonstrates that statistically  similar  populations  were  sampled during each  season. Black  drum  batch  fecundity  increased  with in- creasing age and  size;  no  evidence  of  reproductive senescence  in older individuals was  observed.  Re- gression  analysis of all 41 black  drums  yieldedsignificant  positive correlations  P <  0.0001)  of batch  fecundity  with  total  weight  (TW),  fork  length (FL),  eviscerated  body  weight (BW),  and  age.  Al- though  their low r 2  values limit  the  value  of  theserelationships  as  predictors,  black drum  batch  fe- cundity  (BF)  was  best estimated  with  the  following equations: BF  =  128,684-TW  +  257,588; (r 2  = 0.46); BF  =  4,356  -FL  -  2,064,773;  (r 2  =  0.39); BF  =  141,868-BW  + 354,922;  (r 2  = 0.42); BF  =  49,249-age  +  530,052;  (r 2  =  0.42). Total  weight  and  eviscerated  body  weight  pro- vided  significant  correlations  with  batch  fecundityin  each of the  three  spawning  seasons.  However, relationships between  total  weight,  which  includes the  weight  of the  hydrated ovary,  and  batch  fe-cundity may  reflect  autocorrelations  between  ova- ry  weight  and  batch  fecundity.  Eviscerated body weight  is thus the  better predictor  of  batch  fecun- dity  within  seasons  (Figure  3). TABLE  2.—Means  and  ranges  (in  parentheses)  for  age,  total  weight,  eviscerated  body  weight,  fork  length, andbatch  fecundity  for  female  black  drums sampled  during  the  1988, 1989,  and  1990 spawning  seasons. Season 1988 1989 1990 N 11 18 12 Age (years) 17.6 (7-35) 18.6(10-25) 16.7 (11-26) Total  weight(kg) 8.73 (4.02-15.87) 9.39 (6.01-13.26)8.40 (5.00-14.50) Eviscerated body  weight (kg)7.21 (3.32-13.15) 7.73 (4.71-11.42) 7.11 (4.32-12.68) Fork length(mm) 782 (641-965) 811 (704-889) 789 (673-961) Batch fecundity (millions)1.22 (0.55-2.02) 1.65* (0.72-3.39) 1.21 (0.51-1.82) a  Significantly  different  from  other  annual  batch  fecundities  (analysis of variance and  Duncan's  multiple-range  test;  P <  0.05).
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