Marine Biology

, Volume 160, Issue 12, pp 3113–3124 | Cite as

Pregnancy patterns of pantropical spotted dolphins (Stenella attenuata) in the eastern tropical Pacific determined from hormonal analysis of blubber biopsies and correlations with the purse-seine tuna fishery

  • Nicholas M. Kellar
  • Marisa L. Trego
  • Susan J. Chivers
  • Fredrick I. Archer
Original Paper

Abstract

The northeastern offshore population of the pantropical spotted dolphin (Stenella attenuata) in the eastern tropical Pacific remains listed as depleted under the Marine Mammal Protection Act, and recent estimates of abundance show that recovery has been slow. One hypothesis for the slow recovery is that continued chase and encirclement by the tuna fishery negatively affects reproduction. Insufficient life-history sampling in this region over the last two decades makes traditional estimates of reproductive rates impossible. Here, we examine the current reproductive patterns of these dolphins by measuring blubber progesterone (BP) concentrations in biopsy samples to assess pregnancy state. BP was quantified in 212 biopsies from female offshore spotted dolphins sampled between 1998 and 2003 in the northeastern tropical Pacific, and we found that 11.5 % of the biopsied females (mature and immature) were pregnant. The relationship between pregnancy and fishery exposure was analyzed, and we found that pregnant females were exposed to significantly less fishery activity than non-pregnant ones (p = 0.022), suggesting that the fishery may have an inhibitive effect on pregnancy. Spatial analysis indicated that pregnancy was more aggregated than random (p < 0.05) at a scale up to 180-nmi, with the highest proportion pregnant in the mouth of the Gulf of California, an area with relatively low reported fishery activity.

References

  1. Archer FI, Chivers SJ (2002) Age structure of the northeastern spotted dolphin incidental kill by year for 1971–1990 and 1996–2000. NOAA Admin Rep LJ-02-12Google Scholar
  2. Archer F, Gerrodette T, Dizon A, Abella K, Southern S (2001) Unobserved kill of nursing dolphin calves in a tuna purse-seine fishery. Mar Mammal Sci 17:540–554CrossRefGoogle Scholar
  3. Archer F, Gerrodette T, Chivers S, Jackson A (2004a) Annual estimates of the unobserved incidental kill of pantropical spotted dolphin (Stenella attenuata) calves in the tuna purse-seine fishery of the eastern tropical Pacific. Fish Bull 102:233–244Google Scholar
  4. Archer FI, Ballance LT, Barlow J, Chivers SJ, Cramer K, Dizon AE, Donahue M, Edwards EF, Gerrodette T, Kellar NM, Mesnick SL, Perrin WF, Perryman WL, Pitman RL, Reilly SB (2004b) A research plan to investigate fishery effects on reproduction and post-natal mortality. NOAA Admin Rep LJ-04-03Google Scholar
  5. Archer FI, Redfern JV, Gerrodette T, Chivers SJ, Perrin WF (2010) Estimation of relative exposure of dolphins to fishery activity. Mar Ecol Prog Ser 410:245–255. doi:10.3354/meps08641 CrossRefGoogle Scholar
  6. Barlow J (1985) Variability, trends, and biases in reproductive rates of spotted dolphins, Stenella attenuata. Fish Bull 83:657–669Google Scholar
  7. Barlow J, Hohn A (1984) Interpreting spotted dolphin age distributions. NOAA Tech Memo NMFS-SWFSC-48Google Scholar
  8. Benirschke K, Johnson ML, Benirschke RJ (1980) Is ovulation in dolphins, Stenella longirostris and Stenella attenuata, always copulation-induced? Fish Bull 78:507–528Google Scholar
  9. Berube M, Palsboll P (1996) Identification of sex in cetaceans by multiplexing with three ZFX and ZFY specific primers. Mol Ecol 5:283–287. doi:10.1111/j.1365-294X.1996.tb00315.x Google Scholar
  10. Besag J, Clifford P (1989) Generalized Monte-Carlo significance tests. Biometrika 76:633–642CrossRefGoogle Scholar
  11. Bonenfant C, Gaillard JM, Klein F, Loison A (2002) Sex- and age-dependent effects of population density on life history traits of red deer Cervus elaphus in a temperate forest. Ecography 25:446–458. doi:10.1034/j.1600-0587.2002.250407.x CrossRefGoogle Scholar
  12. Bowen WD, Iverson SJ, Boness DJ, Oftedal OT (2001) Foraging effort, food intake and lactation performance depend on maternal mass in a small phocid seal. Funct Ecol 15:325–334. doi:10.1046/j.1365-2435.2001.00530.x CrossRefGoogle Scholar
  13. Bowyer RT (2004) Sexual segregation in ruminants: definitions, hypotheses, and implications for conservation and management. J Mamm 85:1039–1052. doi:10.1644/Bbl-002.1 CrossRefGoogle Scholar
  14. Brook F, Lim EHT, Chua FHC, Mackay B (2004) Assessment of the reproductive cycle of the Indo-Pacific humpback dolphin, Sousa chinensis, using ultrasonography. Aquatech Mamm 30:137–148CrossRefGoogle Scholar
  15. Bustos-Serrano H, Castro-Valdez R (2006) Flux of nutrients in the Gulf of California: geostrophic approach. Mar Chem 99:210–219. doi:10.1016/j.marchem.2005.09.012 CrossRefGoogle Scholar
  16. Chivers SJ, Demaster DP (1994) Evaluation of biological indices for three eastern Pacific dolphin species. J Wildl Manage 58:470–478CrossRefGoogle Scholar
  17. Chivers SJ, Myrick AC Jr (1993) Comparison of age at sexual maturity and other reproductive parameters for two stocks of spotted dolphin, Stenella attenuata. Fish Bull 91:611–618Google Scholar
  18. Ciuti S, Bongi P, Vassale S, Apollonio M (2006) Influence of fawning on the spatial behaviour and habitat selection of female fallow deer (Dama dama) during late pregnancy and early lactation. J Zool 268:97–107. doi:10.1111/j.1469-7998.2005.00003.x CrossRefGoogle Scholar
  19. Collins CA, Garfield N, Mascarenhas AS, Spearman MG, Rago TA (1997) Ocean currents across the entrance to the Gulf of California. J Geophys Res Oceans 102:20927–20936. doi:10.1029/97jc01302 CrossRefGoogle Scholar
  20. Coubrough RI (1985) Stress and fertility: a review. Onderstepoort J Vet Res 52:153–156Google Scholar
  21. Cramer KL, Perryman WL, Gerrodette T (2008) Declines in reproductive output in two dolphin populations depleted by the yellowfin tuna purse-seine fishery. Mar Ecol Prog Ser 369:273–285CrossRefGoogle Scholar
  22. Curry BE (1999) Stress in mammals: the potential influence of fishery-induced stress on dolphins in the eastern tropical pacific ocean. NOAA Tech Memo NMFS-SWFSC-260Google Scholar
  23. DeMaster DP, Edwards EF, Wade PJ, Sisson JE (1992) Status of dolphin stocks in the Eastern tropical pacific. In: McCullough DR, Barrett RH (eds) Wildlife 2001: population. Elsevier Press, London, pp 1038–1050CrossRefGoogle Scholar
  24. Dizon AE, Perrin WF, Akin PA (1994) Stocks of dolphins (Stenella spp. and Delphinus delphis) in the Eastern tropical pacific: a phylogeographic classification. NOAA Technical Report NMFS 119Google Scholar
  25. Edwards EF (2006) Duration of unassisted swimming activity for spotted dolphin (Stenella attenuata) calves: implications for mother-calf separation during tuna purse-seine sets. Fish Bull 104:125–135Google Scholar
  26. Ellenberg U, Setiawan AN, Cree A, Houston DM, Seddon PJ (2007) Elevated hormonal stress response and reduced reproductive output in yellow-eyed penguins exposed to unregulated tourism. Gen Comp Endocrinol 152:54–63. doi:10.1016/j.ygcen.2007.02.022 CrossRefGoogle Scholar
  27. Fiedler PC (2002) Environmental change in the eastern tropical Pacific Ocean: review of ENSO and decadal variability. Mar Ecol Prog Ser 244:265–283. doi:10.3354/Meps244265 CrossRefGoogle Scholar
  28. Fiedler PC, Reilly SB (1994) Interannual variability in dolphin habitats in the eastern tropical Pacific. II: effects on abundances estimated from tuna vessel sightings, 1975–1990. Fish Bull 92:451–463Google Scholar
  29. Forney KA, St. Aubin DJ, Chivers SJ (2002) Chase encirclement stress studies on dolphins involved in eastern tropical Pacific ocean purse-seine operation during 2001. NOAA Admin Rep LJ-02-32Google Scholar
  30. French SS, Gonzalez-Suarez M, Young JK, Durham S, Gerber LR (2011) Human disturbance influences reproductive success and growth rate in California sea lions (Zalophus californianus). PLoS ONE 6:e17686. doi:10.1371/journal.pone.0017686 CrossRefGoogle Scholar
  31. Gerrodette T, Forcada J (2005) Non-recovery of two spotted and spinner dolphin populations in the eastern tropical Pacific Ocean. Mar Ecol Prog Ser 291:1–21CrossRefGoogle Scholar
  32. Gosliner ML (1999) The tuna-dolphin controversy. In: John R, Twiss J, Reeves RR (eds) Conservation and management of marine mammals. Smithsonian Institution Press, Washington, pp 120–155Google Scholar
  33. Hadjipie G, Holmes W (1966) Studies on feed intake and feed utilization by sheep: voluntary feed intake of dry pregnant and lactating ewes. J Agr Sci 66:217–223CrossRefGoogle Scholar
  34. Harrington FH, Veitch AM (1992) Calving success of woodland caribou exposed to low-level jet fighter overflights. Arctic 45:213–218Google Scholar
  35. Hecker M, Newsted JL, Murphy MB, Higley EB, Jones PD, Wu R, Giesy JP (2006) Human adrenocarcinoma (H295R) cells for rapid in vitro determination of effects on steroidogenesis: hormone production. Toxicol Appl Pharmacol 217:114–124. doi:10.1016/j.taap.2006.07.007 CrossRefGoogle Scholar
  36. Hennessy DP, Williamson P (1983) The effects of stress and of ACTH administration in hormone profiles, estrus and ovulation in pigs. Theriogenology 20:13–26CrossRefGoogle Scholar
  37. Hohn AA, Chivers SJ, Barlow J (1985) Reproductive maturity and seasonality of male spotted dolphins, Stenella attenuata, in the eastern tropical Pacific. Mar Mammal Sci 1:273–293. doi:10.1111/j.1748-7692.1985.tb00016.x CrossRefGoogle Scholar
  38. Jonsson KI, Tuomi J, Jaremo J (1995) On the consequences of pre- and post- breeding costs in the evolution of reproductive effort tactics. Ecoscience 2:311–320Google Scholar
  39. Joseph J (1994) The tuna dolphin controversy in the eastern Pacific ocean: biological, economic, and political aspects. Ocean Devel Inter Law 25:1–30CrossRefGoogle Scholar
  40. Kasuya T (1972) Growth and reproduction of Stenella Coeruleoalba based on the age determination by means of dentinal growth layers. Sci Rep Whales Res Inst Tokyo 24:57–79Google Scholar
  41. Kasuya T (1976) Reconsideration of life history parameters of the spotted and striped dolphins based on cemental layers. Sci Rep Whales Res Inst Tokyo 28:73–106Google Scholar
  42. Kasuya T, Ogi H (1987) Distribution of mother-calf Dall’s porpoise pairs as an indication of calving grounds and stock identity. Sci Rep Whales Res Inst Tokyo 38:125–140Google Scholar
  43. Kellar NM, Trego ML, Marks CI, Dizon AE (2006) Determining pregnancy from blubber in three species of delphinids. Mar Mammal Sci 22:1–16CrossRefGoogle Scholar
  44. Labisky RF, Fritzen DE (1998) Spatial mobility of breeding female white-tailed deer in a low-density population. J Wildl Manage 62:1329–1334. doi:10.2307/3801998 CrossRefGoogle Scholar
  45. Manly BFJ (1991) Randomization and Monte Carlo methods in biology. Chapman and Hall, LondonCrossRefGoogle Scholar
  46. Mansour AAH, McKay DW, Lien J, Orr JC, Banoub JH, Oien N, Stenson G (2002) Determination of pregnancy status from blubber samples in minke whales (Balaenoptera acutorostrata). Mar Mammal Sci 18:112–120. doi:10.1111/j.1748-7692.2002.tb01022.x CrossRefGoogle Scholar
  47. McNeilly AS (2001) Lactational control of reproduction. Reprod Fertil Dev 13:583–590CrossRefGoogle Scholar
  48. Millar JS (1975) Tactics of energy partitioning in breeding Peromyscus. Canad J Zool 53:967–976CrossRefGoogle Scholar
  49. Millar JS (1977) Adaptive features of mammalian reproduction. Evolution 31:370–386. doi:10.2307/2407759 CrossRefGoogle Scholar
  50. Millspaugh JJ, Brundige GC, Gitzen RA, Raedeke KJ (2004) Herd organization of cow elk in Custer State Park, South Dakota. Wildlife Soc B 32:506–514. doi:10.2193/0091-7648(2004)32[506:Hoocei]2.0.Co;2CrossRefGoogle Scholar
  51. Moberg GP (1976) Effects of environment and management stress on reproduction in dairy cow. J Dairy Sci 59:1618–1624. doi:10.3168/jds.S0022-0302(76)84414-1 CrossRefGoogle Scholar
  52. Moberg GP (1991) How behavioral stress disrupts the endocrine control of reproduction in domestic animals. J Dairy Sci 74:304–311CrossRefGoogle Scholar
  53. Myrick AC, Hohn AA, Barlow J, Sloan PA (1986) Reproductive biology of female spotted dolphins, Stenella attenuata, from the eastern tropical Pacific. Fish Bull 84:247–259Google Scholar
  54. Noren SR, Edwards EF (2007) Physiological and behavioral development in delphinid calves: implications for calf separation and mortality due to tuna purse-seine sets. Mar Mammal Sci 23:15–29. doi:10.1111/j.1748-7692.2006.00083.x CrossRefGoogle Scholar
  55. Palsbøll PJ, Larsen F, Hansen ES (1991) Sampling of skin biopsies from free-ranging large cetaceans in west Greenland: development of new biopsy tips and bolt designs. Rpt of Internat Whaling Comm. Special Issue 13:71–89 Google Scholar
  56. Perkins PC, Edwards EF (1999) Capture rate as a function of school size in pantropical spotted dolphins, Stenella attenuata, in the eastern tropical Pacific Ocean. Fish Bull 97:542–554Google Scholar
  57. Perrin WF (1969) Using porpoise to catch tuna. World Fish 18:42–45Google Scholar
  58. Perrin WF, Hohn AA (1995) Pantropical spotted dolphin Stenella attenuata. Handb Mar Mamm 5:71–97Google Scholar
  59. Perrin WF, Coe JM, Zweifel JR (1976) Growth and reproduction of the spotted porpoise, Stenella attenuata, in the offshore eastern tropical Pacific. Fish Bull 74:229–269Google Scholar
  60. Perrin WF, Miller RB, Sloan PA (1977) Reproductive parameters of the offshore spotted dolphin, a geographic form of Stenella attenuata, in the eastern tropical Pacific, 1973–75. Fish Bull 75:629–633Google Scholar
  61. Perrin WF, Chivers SJ, Archer FI (2003) Fetal mortality in dolphins exploited by the tuna fishery abstracts of the 15th Biennial conference on the biology of marine mammals. The Society of Marine Mammalogy, Greensboro, NCGoogle Scholar
  62. Reilly SB, Donahue MA, Gerrodette T, Forney K, Wade P, Ballance L, Forcada J, Fiedler P, Dizon A, Perryman WF, Archer FA, Edwards EF (2005) Report of the scientific research program under the international dolphin conservation program act. NOAA Tech Memo NMFS-SWFSC-372Google Scholar
  63. Reynolds DS, Kunz TH (2000) Changes in body composition during reproduction and postnatal growth in the little brown bat, Myotis lucifugus (Chiroptera: Vespertilionidae). Ecoscience 7:10–17Google Scholar
  64. Ripley BD (1977) Modeling spatial patterns. J Roy Stat Soc Ser B 39:172–212Google Scholar
  65. Robeck TR, Atkinson SKC, Brook FM (2001) Reproduction. In: Dierauf LA, Gulland FMD (eds) Marine mammal medicine. CRC Press LLC, Boca Raton, pp 193–236CrossRefGoogle Scholar
  66. Scott MD, Chivers SJ (2009) Movements and diving behavior of pelagic spotted dolphins. Mar Mammal Sci 25:137–160. doi:10.1111/j.1748-7692.2008.00241.x CrossRefGoogle Scholar
  67. Scott MD, Wells RS, Irvine AB, Mate BR (1990) Tagging and marking studies of small cetaceans. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphin. Academic Press, San Diego, pp 489–514Google Scholar
  68. Seagle SW, McNaughton SJ (1992) Spatial variation in forage nutrient concentrations and the distribution of Serengeti grazing ungulates. Landsc Ecol 7:229–241CrossRefGoogle Scholar
  69. Smith TD (1983) Changes in size of three dolphin (Stenella spp.) populations in the eastern tropical Pacific. Fish Bull 81:1–13Google Scholar
  70. Trego ML, Kellar NM, Danil K (2013) Validation of blubber progesterone concentrations for pregnancy determination in three dolphin species and a porpoise. PLoS One. In pressGoogle Scholar
  71. Wade P (1994) Revised estimates of incidental kill of dolphins (Delphinidae) by the purse-seine tuna fishery in the eastern tropical Pacific, 1959–1972. Fish Bull 93:345–354Google Scholar
  72. Wade PR, Reilly SB, Gerrodette T (2002) Assessment of the population dynamics of the northeastern offshore spotted and the eastern spinner dolphin populations through 2002. NOAA Admin Rep LJ-02-13Google Scholar
  73. Wade PR, Watters GM, Gerrodette T, Reilly SB (2007) Depletion of spotted and spinner dolphins in the eastern tropical Pacific: modeling hypotheses for their lack of recovery. Mar Ecol Prog Ser 343:1–14. doi:10.3354/Meps07069 CrossRefGoogle Scholar
  74. Wilson SJ, Kirby CJ, Koenigsfeld AT, Keisler DH, Lucy MC (1998a) Effects of controlled heat stress on ovarian function of dairy cattle. 2. Heifers. J Dairy Sci 81:2132–2138. doi:10.3168/jds.S0022-0302(98)75789-3 CrossRefGoogle Scholar
  75. Wilson SJ, Marion RS, Spain JN, Spiers DE, Keisler DH, Lucy MC (1998b) Effects of controlled heat stress on ovarian function of dairy cattle. 1. Lactating cows. J Dairy Sci 81:2124–2131. doi:10.3168/jds.S0022-0302(98)75788-1 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2013

Authors and Affiliations

  • Nicholas M. Kellar
    • 1
  • Marisa L. Trego
    • 1
    • 2
  • Susan J. Chivers
    • 1
  • Fredrick I. Archer
    • 1
  1. 1.Protected Resources Division, Southwest Fisheries Science CenterNational Marine Fisheries Service, National Oceanic and Atmospheric AdministrationLa JollaUSA
  2. 2.Ocean Associates, Inc.ArlingtonUSA

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