Integrating life-history and reproductive success data to examine potential relationships with organochlorine compounds for bottlenose dolphins ( Tursiops truncatus) in Sarasota Bay, Florida

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Integrating life-history and reproductive success data to examine potential relationships with organochlorine compounds for bottlenose dolphins ( Tursiops truncatus) in Sarasota Bay, Florida
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  Integrating life-history and reproductive success data to examine potential relationships with organochlorine compounds for  bottlenose dolphins ( Tursiops truncatus ) in Sarasota Bay, Florida Randall S. Wells a, T , Victoria Tornero  b , Asuncion Borrell  b , Alex Aguilar   b ,Teri K. Rowles c , Howard L. Rhinehart  d , Suzanne Hofmann d , Walter M. Jarman e ,Aleta A. Hohn f  , Jay C. Sweeney g a  Chicago Zoological Society, c/o Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236, USA  b  Department of Animal Biology, Faculty of Biology, University of Barcelona, 08071 Barcelona, Spain c  Marine Mammal Health and Stranding Response Program, NOAA Fisheries, 1315 East–West Highway, Silver Spring, MD 20910, USA d  Mote Marine Laboratory, 1600 Ken Thompson Parkway, Sarasota, FL 34236, USA e UN Environmental Programme, P.O. Box 30552, Nairobi, Kenya f   NOAA Fisheries Laboratory, Beaufort, NC 28516, USA g  Dolphin Quest Inc., 4467 Saratoga Ave., San Diego, CA 92107, USA Received 20 August 2004; accepted 12 January 2005Available online 14 March 2005 Abstract Research initiated in 1970 has identified a long-term, year-round resident community of about 140 bottlenose dolphins( Tursiops truncatus ) in Sarasota Bay, Florida, providing unparalleled opportunities to investigate relationships betweenorganochlorine contaminant residues and life-history and reproductive parameters. Many individual dolphins are identifiableand of known age, sex, and maternal lineage ( V 4 generations). Observational monitoring provides data on dolphin spatial andtemporal occurrence, births and fates of calves, and birth-order. Capture–release operations conducted for veterinaryexaminations provide biological data and samples for life-history and contaminant residue measurement. Organochlorineconcentrations in blubber and blood (plasma) can be examined relative to age, sex, lipid content, and birth-order. Reproductivesuccess is evaluated through tracking of individual female lifetime calving success.For the current study, 47 blubber samples collected during June 2000 and 2001 were analyzed for PCB concentrations of 22congeners relative to life-history factors and reproductive success. Prior to sexual maturity, males and females exhibited similar concentrations of about 15–50 ppm. Classical patterns of accumulation with age were identified in males, but not in females.Subsequently, males accumulated higher concentrations of PCBs through their lives ( N 100 ppm), whereas females begin todepurate with their first calf, reaching a balance between contaminant intake and lactational loss ( b 15 ppm). In primiparousfemales, PCB concentrations in blubber and plasma and the rates of first-born calf mortality were both high. First-born calves 0048-9697/$ - see front matter   D  2005 Elsevier B.V. All rights reserved.doi:10.1016/j.scitotenv.2005.01.010 T  Corresponding author. Tel.: +941 388 4441x454; fax: +941 388 4223.  E-mail address:  rwells@mote.org (R.S. Wells).Science of the Total Environment 349 (2005) 106–119www.elsevier.com/locate/scitotenv  had higher concentrations than subsequent calves of similar age ( N 25 vs. b 25 ppm). Maternal burdens were lower early inlactation and increased as calves approached nutritional independence. Empirical data were generally consistent with a published theoretical risk assessment and supported the need for incorporation of threats from indirect anthropogenic impactssuch as environmental pollutants into species management plans. Long-term observational monitoring and periodic biologicalsampling provide a powerful, non-lethal approach to understanding relationships between organochlorine residueconcentrations in tissues and reproductive parameters for coastal dolphins. D  2005 Elsevier B.V. All rights reserved.  Keywords:  Pollutants; Organochlorines; Monitoring; Conservation; Survivorship; Reproduction; Age at sexual maturation; Parturition;Lactation 1. Introduction More than three decades have passed since theinitial recognition of possible health and reproductiveeffects of persistent organic pollutants on marinemammals, but much of the literature available today isstill limited to chemical residue data, with littleinformation on the toxicok inetics and impacts of thechemicals (see reviews by O’Shea, 1999; O’Hara andO’Shea, 2001; Reijnders and Aguilar, 2002; O’Sheaand Tanabe, 2003). In recent years, high concen-trations of environmental contaminant residues incarcasses recovered during large scale marine mam-mal mortality events (e.g., Geraci, 1989; Aguilar andBorrell, 1994) have led to increasing interest inidentifying the potential contribution of anthropogeniccontaminants to these and other cetacean mortalities(Kuehl and Haebler, 1995). Such events are increas-ingly reported around the world and there is a need to be proactive in understanding and responding tomorbidity and mortality that might result from, or beexacerbated by, organochlorine contaminants (OCs).To this end, efforts are underway to measure andcompare contaminant concentrations in free-ranging populations of bottlenose dolphins ( Tursiops trunca-tus ) at multiple sites in the southeastern United States(Schwacke et al., 2002; Hansen et al., 2004; Wells et al., 2004) and to perform risk assessments usingavailable information on effects of these chemicals onsurrogate mammalian models (Schwacke et al., 2002). These preliminary models would benefit fromimproved information on the dynamics and effectsof OCs on dolphins.Evaluation of individual and population-level risksfrom OCs requires knowledge of modes and varia- bility in accumulation and excretion patterns, espe-cially relative to age, sex, and life-history. Basedlargely on compilations of single sampling events,descriptions of OC residue accumulation and excre-tion have been inferred for several species of smallodontocete cetaceans, beginning with the work byGaskin et al. (1971) with harbor porpoises (  Phocoena phocoena ). Because of the persistent and lipophilic properties of many OCs, they are accumulatedthrough the food chain, into tissues of high lipidcontent (such as blubber), where they can reachconcentrations of concern for health and reproductionin apex predators such as marine mammals (O’Shea,1999). In males, accumulation of some of the more persistent OCs continues through life but, in females,concentrations appear to decline with reproductiveactivity, presumably through transfer across the placenta (Aguilar and Borrell, 1994; Salata et al.,1995) and via lactation (Tanabe et al., 1994). The transfer of OC residues from blubber through thecirculatory system to milk has been described for greyseals (  Halichoerus grypus , Addison and Brodie,1987; Debier et al., 2003a; 2003b), but comparablestudies remain to be completed for dolphins.Data on apparent variations in female OC residueconcentrations relative to reproductive activity were provided by the work of  Cockcroft et al. (1989). They measured concentrations of polychlorinated biphenylcompounds (PCBs) and DDT and its metabolites in bottlenose dolphins killed in shark nets off SouthAfrica. Based on blubber concentrations of OCsrelative to the occurrence of ovarian scars indicativeof sexual maturity in a sample of 14 lactating females,they proposed that females transferred 80% of their  body burden of OCs to calves through lactation. Theycalculated that this redistribution occurred predom-inantly during the first seven weeks of life, with the  R.S. Wells et al. / Science of the Total Environment 349 (2005) 106–119  107  first-born offspring receiving the majority of themother’s body burden. Further delineation of this pattern in the absence of matched samples from thecalves of the sampled females or serial samples fromthe females themselves was not possible.Access to captive bottlenose dolphins providedRidgway and Reddy (1995) with opportunities tomeasure OC concentrations in serially-collected milk samples from living females. The authors notedrelationships between female age and lactation his-tory, along with a decline in OC concentrations in onecase through the course of lactation that supported theconcept of mammary-based transfer and excretion.Several factors confounded interpretation of thesedata, however, including the unusual circumstances of induced lactation and re-lactation, much-delayedonset of female reproduction as compared to the wild,and inconsistent results across females. Subsequent work examined OC concentrations in maternal blub- ber prior to parturition relative to calf survivorship(Reddy et al., 2001). Sum PCB concentrations for mothers with calves surviving less than 12 days wereabout 2.5 times those in mothers with surviving calvesand many of the lost calves of mothers with highconcentrations were first-borns.For the purposes of small-cetacean risk assess-ments, empirical evidence of rates of OC accumu-lation in blubber and depuration from living membersof a wild population, in combination with details of sex, age, and reproductive history, would significantlyadvance our understanding of the dynamics of OCmobilization. Repeated measures over time of levelsof OCs for individuals can be very helpful for defining accumulation patterns. Based on the findingsof  Cockcroft et al. (1989) and others, knowledge of  parity is important for identifying the mother’s OClegacy relative to subsequent environmental contribu-tions to calf concentrations. For males, single sam- plings of blubber matched with information on ageand birth-order are sufficient for defining patterns. For females, OC concentration data must be examined inthe context of their reproductive cycle and thetemporal proximity of tissue sampling to lactation.A variety of measures would help to determine theimpact of mother’s OC body burden on her repro-ductive success. Serial sampling of the mother beforeand after lactational transfer to the calf, or of the calf  prior to weaning, would provide a measure of the rateof OC exposure and measures of subsequent calf survivorship could be used in weight of evidenceevaluations. To date, there have been few opportu-nities to obtain this level of information in the wild.In one of the most detailed studies of its kind,Ylitalo et al. (2001) analyzed biopsy dart samples of  blubber from more than 70 free-ranging killer whales( Orcinus orca ) known from years of observationaland genetic studies in Alaska. These authors foundthat reproductive females contained lower levels of OCs than immature whales or mature males of thesame age class and that first-recruited whales con-tained much higher levels than non-first-recruitedwhales, providing additional support for the proposed patterns of accumulation and depuration. However,the lack of serial samples from individuals, incom- plete data on ages, reproductive histories, lactationalstatus, and birth-orders, and the use of remote biopsysampling techniques that may not fully sample blubber through its entire thickness (O’Hara andO’Shea, 2001) limited the interpretation of results.Another promising field site for obtaining empiri-cal information on small cetacean patterns of OCaccumulation, excretion, and potential effects onreproductive success exists for bottlenose dolphinsalong the central west coast of Florida. Research onthe year-round resident Sarasota Bay dolphin com-munity has been ongoing since 1970 and about 140identifiable individuals, mostly of known sex, age,and genetic relationships (Duffield and Wells, 1991,2002), are currently under study (Irvine and Wells,1972; Irvine et al., 1981; Scott et al., 1990a; Wells,1991, 2003). The resident community is composed of at least four generations and includes about one thirdof the dolphins first identified in the early 1970s.Using tagging, tracking, and photographic identifica-tion techniques (Scott et al., 1990b) it has been  possible to define individual home ranges, monitor female reproductive histories including documenting birth-order, measure female reproductive success, anddetermine population-level trends in abundance,losses, and other vital rates (Wells and Scott, 1990). In addition, capture and release operations have beenconducted in which dolphins have been examined for health and reproductive status (Wells et al., 2004) and full-depth blubber samples and other tissues have been collected for analyses of OC residues. Incombination, these features of the Sarasota Bay  R.S. Wells et al. / Science of the Total Environment 349 (2005) 106–119 108  dolphin research program provided a unique oppor-tunity to relate accurate measures of concentrations of OCs to precise measures of life-history parametersand reproductive success, leading to a more refinedunderstanding of the processes of OC accumulationand excretion and their potential effects.Ultimately, our desire to understand the processesof accumulation and depuration is based on a need toevaluate the risks from OCs to individuals and assessthe expected impacts of documented exposures, asthis relates to the conservation of dolphin populations.A probabilistic risk assessment of reproductive effectsof PCBs has been performed by Schwacke et al.(2002) for Sarasota Bay and several other bottlenosedolphin populations in the southeastern United States.This analysis found a high likelihood that reproduc-tive success, especially of primiparous females, is being severely impaired by chronic exposure to PCBs.Previous observational studies have documenteddisproportionately high mortality rates for first-borncalves in Sarasot a Bay (Wells, 2003), consistent with the model of  Schwacke et al. (2002) and the suggestion of  Cockcroft et al. (1989). By integrating empirical data on life-history parameters such as sex,absolute age and age relative to maternal dependenceand maturity, birth order, and female reproductivehistories, reproductive success in terms of calf survival, and OC concentrations from the SarasotaBay dolphin community we have been able to providea test of aspects of the model as a step towardrefinement. 2. Methods 2.1. Study area and field sampling  Dolphins sampled for this project resided in andaround Sarasota Bay, Florida (27 8  N, 82 8  W). SarasotaBay and associated waters extend for about 30 kmalong the central west coast of Florida, south of Tampa Bay. Sarasota and associated shallow bays(generally 1–4 m deep) are separated from the Gulf of Mexico by a series of narrow barrier islands and theycommunicate with the Gulf through narrow passes upto 10 m deep. The shallow, sheltered bay watersfacilitated capturing small groups of selected dolphinswith a 500 m long  4 m deep seine net for sampling,measurements, and marking (Wells et al., 2004).Efforts were made to obtain a representative cross-section of the local dolphin population, thoughdolphins less than 2 years old or more than 45 yearsold were avoided for animal safety reasons. Individualdolphins were placed in a sling and lifted aboard aveterinary examination vessel. The animals wereweighed, measured, and given a veterinary examina-tion. Blood samples were drawn from the fluke intoevacuated tubes via butterfly catheter.Sampling for contaminant residues involved spe-cially prepared tools. Plasma and whole bloodsamples for contaminant residue analyses were trans-ferred from the collection tubes via acid washed glass pipettes into Teflon vials and then placed in liquidnitrogen until they could be transferred to a   80  8 Cfreezer at the laboratory. Wedge-shaped, full-thickness blubber samples were obtained by a veterinarian froma site below the caudal insertion of the dorsal fin.Prior to biopsy, blubber thickness was determinedultrasonically, the site was rinsed with water andlidocaine hydrochloride was administered for localanesthesia. Surgical instruments, foil, and samplereceptacles that had been hexane and acid washedand autoclaved were used to obtain and handle blubber wedges of up to approximately 5  2.5  2cm deep. Blubber samples were cut into subsamplesfor various studies, then placed in Teflon vials andstored in liquid nitrogen until they could be trans-ferred to a   80  8 C freezer at the laboratory. Milk samples were obtained via a specially designedsuction device consisting of the barrel of a 12 ccsyringe attached via plastic tubing to a 60 cc syringe.Samples were transferred into Teflon vials and storedin liquid nitrogen until they could be transferred to a  80  8 C freezer at the laboratory. Blanks of lidocaineadministration and blood and milk sampling gear wereretained for evaluation of their possible contributionsto measured residue concentrations.Upon completion of sampling, dolphins weremarked with freezebrands or tagged as appropriate(Scott et al., 1990b), photographed, involved in a variety of other physiological or acoustic experiments,and released. The total time from capture to releasewas typically about 1–3 h, depending on the number of procedures performed and the number of animalscaptured concurrently. There were no adverse impactson the animals from the handling and sampling; most   R.S. Wells et al. / Science of the Total Environment 349 (2005) 106–119  109  of the dolphins sampled were experienced with thecapture–release process. 2.2. Life-history and reproductive success data Information on the sex, age, maturity, and repro-ductive histories of the sampled dolphins wasobtained through long-term observation and monitor-ing, and through hands-on examinations and samplingwhen necessary. Sex was confirmed through direct examination of the genital region of the dolphinsduring capture–release. The ages of most of thesampled dolphins were known from observationssince birth to identifiable mothers. Ages of otherswere determined from examination of growth layer groups in a tooth extracted under local anesthesia(Hohn et al., 1989). Sexual maturity was evaluated through measurements of reproductive hormone con-centrations, through ultrasonic examination of repro-ductive organs, and through observations of presumedfirst births (Wells, 2003). Births to well-known, identifiable females were documented through regu-lar, systematic photographic identification surveysthrough the dolphins’ home range, and relat ionshipswere confirmed through genetic analyses (Duffieldand Wells, 1991, 2002). Efforts were made to capture,mark, sample, and release 2- and 3-year-old calves if they lacked naturally-distinctive markings, in order tofacilitate monitoring of calves of known maternallineages and birth-order. Birth-order data were con-sidered to be relative data within a maternal lineagerather than absolute values because it was possible for calves to be born and lost before observers hadopportunities to detect them, thereby potentially biasing parity values downward. Birth-order wasassigned only when evidence suggested that monitor-ing of the mother began prior to her first parturition.Survivorship and reproductive success data wereobtained through photographic identification surveysthat documented presence and absence of individualsfrom the resident population, and through recovery of carcasses by the Mote Marine Laboratory StrandingInvestigations Program (Wells and Scott, 1990). 2.3. Contaminant residue sample analyses The analyses that follow result from OC analysesof blubber samples collected during June 2000 and2001 as part of a project to evaluate biomar kers of OCs and their effects (Reijnders et al., 1999) and of   blood samples collected during 1988–1999. Blubber samples were analyzed at the University of Barcelonaand plasma samples were analyzed at the Universityof California, Santa Cruz and the University of Utah. 2.3.1. Organochlorine analyses of blubber  Samples weighing 0.2–1.0 g were ground withanhydrous sodium sulphate and extracted with  n -hexane (residue-free quality) in a Soxhlet apparatusfor 5 h. The resulting solution was concentrated to 10ml. A portion of this extract (2 ml) was used todetermine the quantity of extractable fat per gram of  blubber. A further quantity was mixed with sulphuricacid for the clean up, following the proceduresdescribed by Murphy (1972), and the resulting extract  was concentrated to 1.0 ml and centrifuged for 5 min.Chromatographic analysis was carried out on aHewlett-Packard 5890-II gas chromatograph equippedwith an electron capture detector (ECD) at 350  8 C. Afused silica capillary column (length 60 m, 0.25 mmID) coated with SPB-1 was used as the stationary phase (0.25  A m film thickness). The splitless techni-que was used to inject 1  A l of the purified extract. Purenitrogen gas at a flow rate of 1 ml/min was used as acarrier. Temperature was programmed as follows:injection at 40  8 C for 1 min and increased to 170  8 Cat a rate of 25  8 C/min; 1 min constant to 250  8 C at arate of 2  8 C/min and then to 280  8 C, at 5  8 C/min.Heptachlor and congener 199 were used as internalstandards. 2.3.2. Organochlorine analyses of blood  Plasma samples were thawed and gently vortexed.Aliquots of 3 ml were placed into 10 ml culture tubesand the weights were recorded. The samples werethen spiked with PCB 103, PCB 207 [F1 surrogates],and pentachloro-nitrobenzene (PCNB) [F2 surrogate]to facilitate internal standard quantitation. To denatureserum proteins, an equal volume of formic acid wasadded to each sample and the mixture was vortexed.Varian Mega Bond Elut  R 1 g, 6 cc C18 columns were prepared on a vacuum manifold by rinsing twice with6 ml of methanol and twice with 6 ml of Optimawater. The rinses were eluted by applying vacuum at 3–5 psi and the final rinse was not completely eluted.The serum/formic acid mixtures were loaded onto the  R.S. Wells et al. / Science of the Total Environment 349 (2005) 106–119 110
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