MARINE MAMMAL SCIENCE, 23(1): 15–29 (January 2007)  C 2006 by the Society for Marine Mammalogy No claim to original US government works DOI: 10.1111/j.1748-7692.2006.00083.x PHYSIOLOGICAL AND BEHAVIORAL DEVELOPMENT IN DELPHINID CALVES: IMPLICATIONS FOR CALF SEPARATION AND MORTALITY DUE TO TUNA PURSE-SEINE SETS SHAWN R. NOREN 1 ELIZABETH F. EDWARDS Protected Resources Division, Southwest Fisheries Science Center, National Marine Fisheries Service, 8604 La Jolla Shores Drive, La Jolla, California 92037, U.S.A. E-mail: shawn.noren@noaa.gov ABSTRACT Tuna purse-seiners in the eastern tropical Pacific (ETP) capture yellowfin tuna by chasing and encircling herds of associated dolphins. This fishery has caused mortality in 14 dolphin species (20 stocks) and has led to significant depletions of at least three stocks. Although observed dolphin mortality is currently low, set frequency remains high and dolphin stocks are not recovering at expected rates. Mortality of nursing calves permanently separated from their mothers during fishery operations may be an important factor in the lack of population recovery, based on the recent discovery that calves do not accompany 75%–95% of lactating females killed in the purse-seine nets. We assessed age-specific potential for mother–calf separations and subsequent mortality of calves by reviewing and synthesizing published data on physiological and behavioral development in delphinids from birth through 3 yr postpartum. Results indicate that evasive behavior of mothers, coupled with the developmental state of calves, provides a plausible mechanism for set-related mother–calf separations and subsequent mortality of calves. Potential for set-related separation and subsequent mortality is highest for 0–12-mo-old dolphins and becomes progressively lower with age as immature dolphins approach adult stamina and attain independence. Key words: dolphin, calf, physiology, behavior, ontogeny, ETP, tuna purse-seine fishery, mortality, Stenella attenuata, Stenella longirostris. Tuna purse-seine fisheries in the eastern tropical Pacific Ocean (ETP) capture schools of yellowfin tuna (Thunnus albacares) by locating, chasing, and encircling herds of associated dolphins, primarily spotted (Stenella attenuata), and spinner (Stenella 1 Current address: Institute of Marine Science, University of California at Santa Cruz, 100 Shaffer Road, Santa Cruz, California 95060, U.S.A. 15 16 MARINE MAMMAL SCIENCE, VOL. 23, NO. 1, 2007 longirostris) dolphins (National Research Council 1992). Fishery activities last for an extended period of time, with 20–30 min of chase followed by 40–50 min of net encirclement (Myrick and Perkins 1995). Once the net is closed and the bottom pursed shut, fishermen release the dolphins alive over the submerged end of the “backdown channel” (National Research Council 1992), and the dolphins escape, swimming at high speeds for up to 100 min postrelease (Chivers and Scott 2002). Although mortality of encircled dolphins was historically high (reviewed by Wade 1995), improvements in backdown methods and other fishery procedures have reduced annual observed mortality from several hundred thousand dolphins in the early 1960s (Wade 1995, 2002) to less than 2,000 dolphins per year since the late 1990s (IATTC 2004). Currently, reported fishery-related mortality is less than 0.1% of the estimated 640,000 northeast offshore spotted and 450,000 eastern spinner dolphins in the ETP (Gerrodette and Forcada 2005). Despite reduced observed mortality, the populations are not recovering at growth rates (4% per year) consistent with the level of depletion (Gerrodette and Forcada 2005). Four primary hypotheses have been proposed to explain this lack of recovery: (1) under reporting of direct fishery-related mortality, (2) fishery-related unobserved mortality or suppression of reproduction, (3) decreasing dolphin habitat quality, and (4) erroneous expectations for rate of dolphin population recovery (Gerrodette and Forcada 2005). These hypotheses are not mutually exclusive, so a combination of factors may contribute to the lack of recovery. The present study addresses a component of Hypothesis 2, unobserved calf mortality. Several studies have suggested that unobserved calf mortality could affect recovery of dolphin populations in the ETP (Archer et al. 2001, 2004). Examination of the age composition of dolphins killed in the purse-seine nets demonstrated that fewer 0–1-yr-old eastern spinner (Chivers 2002) and 0–3-yr-old northeast offshore spotted dolphins (Archer and Chivers 2002) were present than expected, as calves did not accompany 75%–95% of the killed lactating females (Archer et al. 2004). These findings imply that dolphin calves become separated from their mothers during tuna purse-seine activities, as is evident in a series of photographs depicting an ETP dolphin calf falling behind its mother during chase (Weihs 2004). Without their mothers, calves have an increased risk of mortality due to starvation and predation. The fishing intensity in the ETP provides ample opportunities for mother–calf separations and subsequent calf mortality to occur. From 1998 to 2000, set frequency on northeast offshore spotted dolphins alone averaged 5,000 sets per year, resulting in 6.8 million dolphins chased per year, and 2 million dolphins captured per year (Archer et al. 2002), with each individual dolphin hypothetically experiencing 10.6 chases and 3.2 captures per year (calculated from Archer et al. 2002). Since that time, total set frequency on all dolphin species has risen from 9,235 to 13,839 from the year 2000 to 2003 (IATTC annual report 2002a, b, 2004). Yet the mechanism(s) by which mother–calf pairs become separated during tuna purse-seine sets remain(s) unknown (Archer et al. 2004). To evaluate the risk for mother–calf separations and subsequent mortality of permanently separated calves, we compiled and synthesized published data on delphinid development. Physical development, particularly development of aerobic and anaerobic capacities, affects swimming capacity and the ability of calves to maintain proximity with their mothers during chase. Behavioral development, particularly the level of nutritional and social independence, affects the ability of permanently separated calves to survive alone. Adoption as a possible strategy to mitigate mortality of permanently separated calves was also examined. NOREN AND EDWARDS: DEVELOPMENT OF DELPHINIDS 17 PHYSIOLOGICAL AND BEHAVIORAL DEVELOPMENT OF DELPHINIDS Although logistical constraints have limited collection of detailed physiological and behavioral data from spotted and spinner dolphins in the ETP, extensive data are available from other dolphin species, which can be considered representative of ETP dolphins because they share morphological, behavioral, and developmental characteristics (Peddemors 1990; Noren et al. 2002; Perrin 2002a, b; Wells and Scott 2002; Noren 2004), associate and interbreed in captivity and in the wild (Herzing and Johnson 1997, Herzing et al. 2003, Psarakos et al. 2003) and are genetically related within the family Delphinidae (Leduc et al. 1999). In this study, we assigned several stages of calf development because physical and behavioral characteristics of dolphins change markedly throughout the first three years of life. These age classes are defined as postpartum time intervals. Detailed age-specific information derived from our literature review appears in Appendix S1. This was the basis for our synthesis below. Neonates (<2 wk) Although neonatal dolphins are considered to be precocial at birth (Dearolf et al. 2000), a prolonged postnatal development period is required to attain mature physiological characteristics that support swimming and diving. Both coastal and pelagic neonatal dolphins have lower aerobic and anaerobic capacities (Dolar et al. 1999; Dearolf et al. 2000; Noren et al. 2001, 2002; Noren 2004) and proportionally smaller muscle mass (Edwards 1993; Lockyer 1995a, b; Dearolf et al. 2000; reviewed by McLellan et al. 2002) than adult conspecifics. For example, comparisons of aerobic and anaerobic indices within bottlenose dolphins indicated that neonatal dolphins have only 72% of the oxygen carrier in the blood (hemoglobin, Hb; Noren et al. 2002), 10% of the oxygen carrier in the muscle (myoglobin, Mb; Noren et al. 2001), and 65% of the muscle acid buffering capacity found in adults (Fig. 1; Noren 2004). In addition, only 17.7% of total body mass is appropriated to locomotor muscle in neonates compared to 25.7% for adults (calculated from Dearolf et al. 2000). At the same time, extreme skeletal and muscular flexibility (Etnier et al. 2003) and floppy dorsal fins and flukes (McBride and Kritzler 1951, Tavolga and Essapian 1957, Cockcroft and Ross 1990) compromise swimming efficiency. In addition, the small body size of neonates (e.g., newborn spotted dolphins are only 45% of adult female body length; Hohn and Hammond 1985) further limits performance because swimming and diving capabilities within cetaceans increase with body size (Fish 1998, Noren and Williams 2000). As a result, neonatal bottlenose dolphins breathe more often than their mothers (3.8 vs. 2.6 breaths per minute; Mann and Smuts 1999), have only 35% of adult aerobic breath-hold diving capacity (Noren et al. 2002), and do not dive for the first week postpartum (Eastcott and Dickinson 1987, Mann and Smuts 1999). Behavioral adaptations mitigate the swimming and diving limitations of neonates. The swimming style of newborn dolphins is qualitatively different from that of older animals. Neonates predominantly swim with their mothers in “echelon position” by flanking their mothers’ dorsal fin region (McBride and Kritzler 1951, Tavolga and Essapian 1957, Au and Perryman 1982, Cockcroft and Ross 1990, Smolker et al. 1993, Gubbins et al. 1999, Mann and Smuts 1999). This positioning theoretically reduces the cost of transport for neonates as they are carried by the pressure wave created by their mothers’ larger body (Weihs 2004), permitting neonates to maintain 18 MARINE MAMMAL SCIENCE, VOL. 23, NO. 1, 2007 Proportion of adult value (%) 100 80 60 40 Weaning Independence 20 Sexual Maturity Adult Body Size 0 0 1 2 3 4 5 6 7 8 9 10 11 12 Age (yr) Figure 1. Physiological and behavioral development of bottlenose dolphins (Tursiops truncatus). The bottlenose dolphin serves as a model to demonstrate that independence in delphinids occurs naturally only after the majority of physiological development is complete. Physiological characteristics are presented as open circles with dash-dot-dot-dash line representing muscle acid buffering capacity, diamonds with short dash line the blood oxygen stores, squares with long dash line the muscle oxygen stores, triangles with dotted line the level of bradycardia, closed circles with solid line the calculated aerobic dive limit, and upside down triangles with dash-dot-dash line the body mass. Figure adapted from Noren 2002. group speed with reduced tailbeat frequency (Norris and Prescott 1961). Similarly, the limited dive capacity of neonates is likely unimportant as they are not required to forage because their mothers provide the sole source of nutrition (Wells 1991, Archer and Robertson 2004). Young Infants (2–10 wk) Physiological capacity and behavioral independence does not improve much during the young infant stage. However, a change in swimming position indicates that young infants are more competent swimmers than neonates. The time spent in echelon position decreases markedly (from 69% to 11% of the time) as infant position (calf positioned underneath mother’s peduncle) and infant traveling alone increase in importance (Mann and Smuts 1999). Yet the limited physiological stamina of young infants remains evident as they immediately resume either echelon or infant position during traveling activity (Tavolga and Essapian 1957, Cockroft and Ross 1990, Gubbins et al. 1999, Mann and Smuts 1999). Furthermore, young infants continue to remain completely dependent on their mothers for nutrition (Wells 1991, Archer and Robertson 2004). Older Infants (2.5–6 mo) The first marked improvements in some physiological and behavioral attributes occur during this period. For example, the oxygen carrying capacity of the blood NOREN AND EDWARDS: DEVELOPMENT OF DELPHINIDS 19 in bottlenose dolphins increases rapidly (Noren et al. 2002). However, overall their physiology remains underdeveloped (Noren et al. 2001, 2002) and body size remains comparatively small, as spotted dolphin older infants are only approximately half the adult female body length (Hohn and Hammond 1985). As a result, older infants continue to have limited breath-hold, diving, and swimming capabilities relative to adults. Furthermore, older infants remain nutritionally dependent on their mothers’ milk (Wells 1991, Archer and Robertson 2004) even though they begin to develop important behavioral skills, such as echolocation (Reiss 1984) and foraging (Wells 1991, Mann 1997, Mann and Smuts 1999, Mann and Sargeant 2003, Archer and Robertson 2004, Mann and Watson-Capps 2005). Young Calves (6–12 mo) Physiology continues maturing, and by this stage the anaerobic capacity of the muscle is similar to that of adults (Noren 2004). This may partially offset aerobic deficiencies (e.g., 12-mo-old bottlenose dolphin Hb and Mb levels are 86% and 57% of adult levels, respectively; Noren et al. 2001, 2002) as breath-hold ability shows a marked improvement by 6 mo of age (Peddemors 1990). Yet aerobic deficiencies combined with small body size continue to limit performance as 12-mo olds have only 60% adult aerobic breath-hold capacity (Noren et al. 2002). The improved physiological status is evident in behavioral changes. By 12 mo postpartum, calves rely less on echelon swimming and spend only 23% of their time in this position (Gubbins et al. 1999). Furthermore, although calves remain dependent on their mothers’ milk (Gurevich 1977, Cockroft and Ross 1990, Wells 1991, Peddemors et al. 1992, Triossi et al. 1998, Miles and Herzing 2003, Archer and Robertson 2004), solid food becomes a regular part of their diet (McBride and Kritzler 1951, Essapian 1953, Tavolga and Essapian 1957, Perrin and Reilly 1984, Cockroft and Ross 1990, Wells 1991, Peddemors et al. 1992, Mann 1997, Triossi et al. 1998, Mann and Smuts 1999, Miles and Herzing 2003, Archer and Robertson 2004). Yearlings (12–24 mo) Additional physiological characteristics reach maturity during this stage. By 24 mo postpartum, the blood and muscle oxygen stores approximate adult levels (Noren et al. 2001, 2002). However, yearlings attempting a dive are still unable to reduce heart rate to levels found for 3.5–5.5-yr olds and adults (Noren et al. 2004). This cardiac deficiency limits yearlings’ ability to conserve oxygen during breath-hold, reducing their dive capacity (Noren et al. 2004). In addition, the comparatively small body size of yearlings (e.g., spotted dolphin yearlings are only 67%–76% of adult female length; Hohn and Hammond 1985) continues to limit swimming and diving performance. Nonetheless, the behavior of yearlings reflects increased physical competency relative to earlier developmental stages. Drafting in echelon position is rare (Mann 1997). In addition, nursing decreases (Gurevich 1977, Cockroft and Ross 1990, Wells 1991, Peddemors et al. 1992, Triossi et al. 1998, Miles and Herzing 2003, Archer et al. 2004) while foraging increases (Miles and Herzing 2003, Archer and Robertson 2004). Some bottlenose (McBride and Kritzler 1951, Essapian 1953, Wells 1991) and spotted (Archer and Robertson 2004) dolphins may cease to rely primarily on milk as early as 1.5 yr postpartum. 20 MARINE MAMMAL SCIENCE, VOL. 23, NO. 1, 2007 Two-year-old Calves (24–36 mo) Dolphins continue to undergo some remaining physiological development during this period. The cardio-respiratory system continues to be refined (Noren et al. 2004) and body size continues to increase (Barlow and Hohn 1984, Hohn and Hammond 1985, Read et al. 1993). Although 2-yr olds are undoubtedly more accomplished swimmers than younger dolphins, the need for further physiological and morphological development likely precludes attainment of adult exercise performance. Even though there are no accounts of swim speeds or dive durations for wild 2-yr-old dolphins, experimental dive durations for 2-yr olds were significantly shorter compared to adults (Noren et al. 2004). Despite improved physical competency, 2-yr olds continue to spend most of their time within a few meters of their mothers (Gurevich 1977, Smolker et al. 1993, Mann 1997, Miles and Herzing 2003) and many still nurse (Cockroft and Ross 1990, Wells 1991, Peddemors et al. 1992, Miles and Herzing 2003). Three-year-old Calves (36–48 mo) Remaining limitations in exercise performance at this age are primarily due to body-size effects, as 3-yr-old spotted dolphins are approximately 84%–86% of adult female body length (Barlow and Hohn 1984). Although actual swimming stamina remains to be quantified, ETP dolphin calves greater than 2-yr-old are seldom observed in drafting formation (Archer et al. 2004), suggesting improved swimming capabilities. Meanwhile, diving capacity remains significantly lower than adult capacity until 4.5 yr postpartum (Noren et al. 2004). The remaining limitations in performance (Noren 2002) and continued social learning (Mann and Sargeant 2003) likely contribute to the persistence of associations between 3-yr olds and their mothers (Wells 1991, Smolker et al. 1993, Herzing and Brunnick 1997, Mann et al. 2000, Miles and Herzing 2003). SYNOPSIS AND IMPLICATIONS Although the difficult logistics of studying pelagic dolphins have precluded detailed observations of mother–calf evasive behavior during and after tuna purseseine sets, clues to the behavioral responses of chased dolphins can be obtained from comparisons with ecologically similar mammalian systems. Dolphins in the ETP share a number of characteristics with terrestrial herd-forming mammals (specifically, follower-type species of bovids, equids, and cervids) that live in open and relatively featureless habitats (e.g., prairie, savannah, tundra). To deter and evade predators in the absence of spatial refuges, these terrestrial animals aggregate in large herds (Kie 1999, Caro et al. 2004), produce physically precocious offspring that follow the mother within minutes after birth (Lent 1966, Estes and Estes 1979), and react to threat by aggregating and running as a group (stampeding) away from the perceived source of danger (Lent 1966, 1974; Leuthold 1977). Similarly, ETP dolphins live in an open habitat without physical refuges (i.e., pelagic ocean), aggregate in large herds (Perkins and Edwards 1999), produce physically precocious offspring that must swim with their mother immediately after birth (Dearolf et al. 2000), and upon perception of a threat immediately aggregate and swim as a group, elevating routine speeds of 1 m/s to chase and burst speeds of 2–4 m/s and 5–8 m/s, respectively (Au and NOREN AND EDWARDS: DEVELOPMENT OF DELPHINIDS 21 Perryman 1982, Au et al. 1988, Chivers and Scott 2002). The presence of a calf does not deter maternal herd-conforming behavior during the flight response. Terrestrial mothers kept running with their herd while avoiding threats, even after their calves became separated (Lent 1966, Stringham 1974, Ralls et al. 1986). Similarly, photographs of an ETP dolphin school evading a vessel revealed that a mother dolphin did not change her trajectory during chase, despite her calf falling behind (Weihs 2004). Terrestrial mothers attempted to relocate and reunite with their separated calves once the threat abated (Lent 1966, 1974) and, by analogy, ETP dolphin mothers may do the same. However, unlike the stealthy, short duration chases associated with natural predators like sharks and killer whales, tuna purse-seine chases are noisy and long. Assuming a 20-min chase and a 100-min escape response at a swim speed of 3 m/s (Myrick and Perkins 1995, Chivers and Scott 2002), mother–calf dolphin pairs could become separated by 3.6 km during a chase, and by an additional 18 km after escaping. These prolonged durations and expansive distances could interfere with mother–calf reunions compared to reunions following natural predatory events, which typically occur over much shorter durations and distances. The observation that a mother dolphin remained with the herd during threat evasion, regardless of her calf’s position, seems to contradict observations of coastal and captive mother dolphins tending to their threatened, injured, dying, or dead calves (e.g., McBride and Kritzler 1951, Hubbs 1953, Moore 1955, Tavolga and Essapian 1957, Connor and Smolker 1990, Mann and Barnett 1999). However, these circumstances are quite different. Impending generalized threats, such as an approaching shark (Tayler and Saayman 1972, Connor and Heithaus 1996) or tuna purse-seine set (Au and Perryman 1982, Au et al. 1988), present a danger to the entire herd without a specific target, resulting in a concerted evasive reaction by the entire group. In contrast, threatening events targeting a single calf lead to individualized reactions by the mother and perhaps a few other dolphins (e.g. McBride and Kritzler 1951, Hubbs 1953, Moore 1955, Tavolga and Essapian 1957, Connor and Smolker 1990, Mann and Barnett 1999). Ultimately, permanent mother–calf separation prior to calf maturity is detrimental to the progeny because calf independence in coastal and pelagic dolphin species occurs naturally only after the majority of postnatal development is complete (Appendix S1; Fig. 1). The potential for a permanent mother–calf separation during a tuna-purse seine fishery interaction and the subsequent mortality of a calf will be affected by the calf’s physiological development and nutritional/ behavioral dependence, respectively (Fig. 2). Under normal circumstances, 0–12-mo-old dolphins overcome physical limitations during high-speed travel by drafting next to their mothers in echelon position, which is theoretically sustainable during full-body respiratory leaps at speeds up to 2–3 m/s (Weihs 2004). However, the lack of physical coordination in young dolphins (particularly neonates) in combination with limited aerobic and anaerobic muscular capacities (Dolar et al. 1999, Dearolf et al. 2000, Noren et al. 2001, Noren 2004) will make it difficult for 0–12-mo-old dolphins to maintain or reestablish echelon position during the evasive maneuvering required during chase (Au and Perryman 1982), as echelon position is only sustained when mother and calf leave and re-enter the water synchronously with similar speed and splash formation (Weihs 2004). Furthermore, elevated mass-specific metabolic rates (of immature marine mammals reviewed by Donohue et al. 2000) combined with immature physiology will act synergistically to limit breath-hold capacity, requiring immature dolphins to surface to breathe more often than their mothers, which will further disrupt echelon. Although the follower response of immature dolphins is strong (Mann and Smuts 1998), once calves 22 MARINE MAMMAL SCIENCE, VOL. 23, NO. 1, 2007 NOREN AND EDWARDS: DEVELOPMENT OF DELPHINIDS 23 become separated from their mothers-their physiological limitations will preclude them from sustaining adult swim speeds (Edwards 2006). The younger the dolphin and the longer fast swimming persists, the more likely mother–calf separation will occur. In the event of permanent separation, 0–12-mo-old dolphins have an increased risk of predation and will starve without their mothers’ milk (McBride and Kritzler 1951, Essapian 1953, Wells 1991, Archer and Robertson 2004). Mortality of permanently separated milk-dependent calves could be mitigated by adoption; however, this behavior is unlikely in the ETP. Although there are cases of dolphins providing some degree of alloparental care (Reidman 1982), allonursing and adoption have never been observed in wild dolphin populations, despite intensive long-term studies of several species (Wells 1991, Norris et al. 1994, Herzing 1997, Mann and Smuts 1999, Whitehead and Mann 2000). This is consistent with a review of 82 nondomesticated mammalian species, in which allonursing was infrequent in wild populations and rarely tolerated in animals that gave birth to a single offspring (Packer et al. 1992). Compared with younger age classes, yearlings and 2-yr olds are more accomplished swimmers and less dependent on their mothers. However, incomplete physiological development and smaller body size undoubtedly precludes sustained performance at adult levels, and could result in separation, particularly if set evasion is prolonged. Although yearlings and 2-yr olds have been observed suckling (Gurevich 1977, Cockroft and Ross 1990, Wells 1991, Peddemors et al. 1992, Miles and Herzing 2003), and dolphins may not be weaned until 3 yr postpartum or more (Herzing 1997, Mann et al. 2000, Kogi et al. 2004), separated yearlings and 2-yr-old calves are less likely to starve (Archer and Robertson 2004) due to improved foraging abilities (Miles and Herzing 2003, Archer and Robertson 2004). This is supported by the observation that a dolphin orphaned at 16 mo of age successfully attained sexual maturity in the absence of adoption (Wells 2003). However, the observation that yearlings and 2-yrold calves continue to spend most of their time within a few meters of their mothers (Smolker et al. 1993, Mann 1997, Miles and Herzing 2003) suggests that the mother– calf social bond continues to provide an advantage to calf survival, ensuring that calves learn additional foraging-related behaviors (Mann and Sargeant 2003) and complete all physiological development before becoming completely nutritionally independent (Noren 2002). Thus, the potential for long-term survival of yearlings and 2-yr-old calves permanently separated from their mothers is greater than that for 0–12-mo-old dolphins but is still uncertain. The physiological characteristics of 3-yr-old calves are similar to those of adult conspecifics (Noren et al. 2001, 2002, 2004; Noren 2004) so that the potential for separation will decrease progressively as adult body size and swimming ←−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−−− Figure 2. Potential outcomes for a calf, based upon the calf’s level of physiological and behavioral maturity, after it and its mother have been involved in a fishery interaction. Physiological characteristics that affect diving and swimming performance are presented top down in the order in which they mature during development. Likewise, behavioral advantages gained from maintaining an association with the mother are presented top down in the order in which the calf no longer requires that type of assistance from its mother. Only a calf approaching physiological maturity will be able to consistently maintain proximity or reunite with its mother during a fishery interaction. Similarly, only a calf approaching behavioral maturity will be capable of independent survival if permanently separated from its mother. 24 MARINE MAMMAL SCIENCE, VOL. 23, NO. 1, 2007 performance are attained. Although 3-yr-old calves are likely weaned (Herzing 1997, Mann et al. 2000, Miles and Herzing 2003, Archer and Robertson 2004, Kogi et al. 2004), mother–calf associations are sometimes maintained (Wells 1991, Smolker et al. 1993, Herzing and Brunnick 1997, Miles and Herzing 2003) and nursing may continue for up to 8 yr (Scott et al. 1990, Mann et al. 2000). Regardless, the potential for long-term survival of permanently separated 3-yr-old calves is undoubtedly greater than that for younger age classes. Conclusions In conclusion, the flight response of dolphin mothers coupled with the limited physical stamina of their calves provides a plausible mechanism for mother–calf separations during tuna purse-seine activities. The behavioral development of calves mirrors physiological development, such that calves are naturally independent only after their physiological maturation is primarily complete (Fig. 1). By implication, mother–calf separations prior to the maturation of the calf would be detrimental for immature dolphins (Fig. 2). The risk for separation and subsequent mortality is age dependent and is highest for 0–12-mo-old dolphins, lowering progressively with age as immature dolphins approach adult stamina and gain independence. The high fishing intensity in the ETP provides ample opportunities for mother–calf separations and subsequent calf mortalities, thus the developmental factors discussed here undoubtedly impact survival rates of dolphin calves in the ETP. Given the increasingly frequent and geographically extensive nature of tuna purse-seining in the ETP, these impacts may be of substantial demographic importance to various species and stocks of dolphin. ACKNOWLEDGMENTS This research was conducted under Section 304(a)(1): Stress Studies, of the 1997 International Dolphin Conservation Program Act amendments to the Marine Mammal Protection Act, and subsequent Congressional directives. S. R. Noren was supported through a National Research Council Resident Research Associate Award. Comments from D. A. Pabst, J. Mann, J. L. Dearolf, an anonymous reviewer, and the T. M. Williams laboratory significantly improved the manuscript. LITERATURE CITED ARCHER, F., AND S. J. CHIVERS. 2002. Age structure of the northeastern spotted dolphin incidental kill by year for 1971 to 1990 and 1996 to 2000. National Marine Fisheries Service Science Center Administrative Report LJ-02-12 (unpublished). 18 pp. ARCHER, F. I., AND K. M. ROBERTSON. 2004. Age and length at weaning and development of diet of pantropical spotted dolphins Stenella attenuata from the eastern tropical Pacific. Marine Mammal Science 20:232–245. ARCHER, F., T. GERRODETTE, A. DIZON, K. ABELLA AND S. SOUTHERN. 2001. Unobserved kill of nursing dolphin calves in a tuna purse-seine fishery. Marine Mammal Science 17:540–554. ARCHER, F., T. GERRODETTE AND A. JACKSON. 2002. Preliminary estimates of the annual number of sets, number of dolphins chased, and number of dolphins captured by stock in the tuna purse-seine fishery in the eastern tropical Pacific, 1971–2000. National Marine NOREN AND EDWARDS: DEVELOPMENT OF DELPHINIDS 25 Fisheries Service Science Center Administrative Report LJ-02-10 (unpublished). 27 pp. Available from SWFSC, 8604 La Jolla Shores Drive, La Jolla, CA 92037. ARCHER, F., T. GERRODETTE, S. CHIVERS AND A. Jackson. 2004. Annual estimates of the unobserved incidental kill of pantropical spotted dolphin (Stenella attenuata) calves in the tuna purse-seine fishery in the eastern tropical Pacific. Fishery Bulletin 102:233– 244. AU, D., AND W. PERRYMAN. 1982. Movement and speed of dolphin schools responding to an approaching ship. Fishery Bulletin 80:371–379. AU, D. W., M. D. SCOTT AND W. L. PERRYMAN. 1988. Leap-swim behavior of “porpoising” dolphins. Cetus 8:7–10. BARLOW, J., AND A. HOHN. 1984. Interpreting spotted dolphin age distributions. U.S. Department of Commerce, NOAA Technical Memorandum NOAA-TM-NMFS-SWFC48. 21 pp. CALDWELL, M. C., AND D. K. CALDWELL. 1966. Epimeletic (care-giving) behavior in cetacea. Pages 755–776 in K. S. Norris, ed. Whales, dolphins, and porpoises. University of California Press, Berkeley, CA. CALDWELL, M. C., AND D. K. CALDWELL. 1979. The whistle of the Atlantic bottlenose dolphin (Tursiops truncatus): Ontogeny. Pages 369–401 in H. E. Winn and B. L. Olla, eds. Behavior of marine mammals, Volume 3. Cetaceans. Plenum Press, New York, NY. CARO, T. M., C. GRAHAM, C. STONER AND J. VARGAS. 2004. Adaptive significance of antipredator behavior in artiodactyls. Animal Behavior 67:205–228. CHIVERS, S. J. 2002. Age structure of female eastern spinner dolphins (Stenella longirostris orientalis) incidentally killed in the eastern tropical Pacific tuna purse-seine fishery. National Marine Fisheries Service Science Center Administrative Report LJ-02-11 (unpublished). 11 pp. Available from SWFSC, 8604 La Jolla Shores Drive, La Jolla, CA 92037. CHIVERS, S. J., AND M. D. SCOTT. 2002. Tagging and tracking of Stenella spp. during the 2001 chase encirclement stress studies cruise. National Marine Fisheries Service Science Center Administrative Report LJ-02-33 (unpublished). 33 pp. COCKCROFT, V. G., AND J. B. ROSS. 1990. Observations on the early development of a captive bottlenose dolphin calf. Pages 461–478 in S. J. Leatherwood and R. Reeves, eds. The bottlenose dolphin. Academic Press, San Diego, CA. CONNOR, R. C., AND M. R. HEITHUS. 1996. Approach by great white shark elicits flight response in bottlenose dolphins. Marine Mammal Science 12:602–606. CONNOR, R. C., AND R. A. SMOLKER. 1990. Quantitative description of a rare behavioral event: A bottlenose dolphin’s behavior toward her deceased offspring. Pages 355–360 in S. J. Leatherwood and R. Reeves, eds. The bottlenose dolphin. Academic Press, San Diego, CA. DEAROLF, J. L., W. A. MCCLELLAN, R. M. DILLAMAN, D. FRIERSON AND D. A. PABST. 2000. Precocial development of axial locomotor muscle in bottlenose dolphins (Tursiops truncatus). Journal of Morphology 244:203–215. DOLAR, M. L. L., P. SUAREZ, P. J. PONGANIS AND G. L. KOOYMAN. 1999. Myoglobin in pelagic small cetaceans. Journal of Experimental Biology 202:227–236. DONOHUE, M. J., D. P. COSTA, M. E. GOEBEL AND J. D. BAKER. 2000. The ontogeny of metabolic rate and thermoregulatory capabilities of Northern fur seal, Callorhinus ursinus, pups in air and water. Journal of Experimental Biology 203:1003–1016. EASTCOTT, A., AND T. DICKINSON. 1987. Underwater observations of the suckling and social behavior of a new-born bottle-nosed dolphin (Tursiops truncatus). Aquatic Mammals 13:51–56. EDWARDS, E. F. 1993. Allometry of energetics parameters in spotted dolphins (Stenella attenuata) from the eastern tropical Pacific Ocean. Fishery Bulletin 91:428–439. EDWARDS, E. F. 2006. Duration of unassisted swimming activity for spotted dolphin (Stenella attenuata) calves: Implications for mother–calf separation during tuna purse-seine sets. Fishery Bulletin 104:125–135. ESSAPIAN, F. S. 1953. The birth and growth of a porpoise. Natural History 62:392–399. 26 MARINE MAMMAL SCIENCE, VOL. 23, NO. 1, 2007 ESTES, R. D., AND R. K. ESTES. 1979. The birth and survival of wildebeest calves. Zeitschrift für Tierpsychologie 50:45–95. ETNIER, S. A., J. L. DEAROLF, W. A. MCLELLAN AND D. A. PABST. 2003. Postural role of lateral axial muscles in developing bottlenose dolphins (Tursiops truncatus). Proceedings of the Royal Society of London B 271:909–918. FISH, F. E. 1998. Comparative kinematics and hydrodynamics of odontocete cetaceans: Morphological and ecological correlates with swimming performance. Journal of Theoretical Biology 201:2867–2877. GERRODETTE, T., AND J. FORCADA. 2005. Non-recovery of two spotted and spinner dolphin populations in the eastern tropical Pacific Ocean. Marine Ecology Progress Series 291:1– 21. GUBBINS, C., B. MCCOWAN, S. K. LYNN, S. HOOPER AND D. REISS. 1999. Mother–infant spatial relations in captive bottlenose dolphins, Tursiops truncatus. Marine Mammal Science 15:751–765. GUREVICH, V. S. 1977. Post-natal behavior of an Atlantic bottlenose dolphin calf (Tursiops truncatus, Montagu) born at Sea World. Pages 168–184 in S. Ridgeway and K. Bernischke, eds. Marine Mammal Commission Report MMC-76/07. U. S. Marine Mammal Commission, Washington, DC. HERZING, D. L. 1997. The life history of free-ranging Atlantic spotted dolphins (Stenella frontalis): Age classes, color phases, and female reproduction. Marine Mammal Science 13:576–595. HERZING, D. L., AND B. J. BRUNNICK. 1997. Coefficients of association of reproductively active female Atlantic spotted dolphins, Stenella frontalis. Aquatic Mammals 23:155– 162. HERZING, D. L., AND C. M. JOHNSON. 1997. Interspecific interactions between Atlantic spotted dolphins, Stenella frontalis, and bottlenose dolphins, Tursiops truncatus, in the Bahamas. Aquatic Mammals 23:85–99. HERZING, D. L., K. MOEWE AND B. J. BRUNNICK. 2003. Interspecies interactions between Atlantic spotted dolphins, Stenella frontalis, and bottlenose dolphins, Tursiops truncatus, on Great Bahama Bank, Bahamas. Aquatic Mammals 29:335–341. HOHN, A. A., AND P. S. HAMMOND. 1985. Early postnatal growth of the spotted dolphin, Stenella attenuata, from the offshore eastern tropical Pacific. Fishery Bulletin 83:553– 566. HUBBS, C. 1953. Dolphin protecting dead young. Journal of Mammalogy 34:498. IATTC (InterAmerican Tropical Tuna Commission). 2002a. Annual report of the InterAmerican Tropical Tuna Commission 2000, La Jolla, CA. 176 pp. IATTC. 2002b. Annual report of the Inter-American Tropical Tuna Commission 2001, La Jolla, CA. 156 pp. IATTC. 2004. Annual report of the Inter-American Tropical Tuna Commission 2003, La Jolla, CA. 103 pp. KIE, J. 1999. Optimal foraging and risk of predation. Journal of Mammalogy 80:1114–1129. KOGI, K., T. HISHII, A. IMAMURA, T. IWATANI AND K. M. DUDZINSKI. 2004. Demographic parameters of Indo-Pacific bottlenose dolphins (Tursiops aduncus) around Mikura, Japan. Marine Mammal Science 20:510–526. LEDUC, R. G., W. F. PERRIN AND A. E. DIZON. 1999. Phylogenetic relationships among the Delphinid cetaceans based on full cytochrome B sequences. Marine Mammal Science 15:619–648. LENT, P. C. 1966. Calving and related social behavior in the barren-ground Caribou. Zeitschrift für Tierpsychologie 23:702–756. LENT, P. C. 1974. The behavior of ungulates and its relation to management. IUCN (International Union for the Conservation of Nature and Natural Resources) Publications. New Series 24:14–55. LEUTHOLD, W. 1977. African ungulates: A comparative review of their ethology and behavioral ecology. Springer-Verlag, New York, NY. NOREN AND EDWARDS: DEVELOPMENT OF DELPHINIDS 27 LOCKYER, C. 1995a. Aspects of the biology of the harbour porpoise, Phocoena phocoena, in British waters. Pages 443–457 in A. S. Blix, L. Wallace and O. Ulltang. eds. Whales, seals, fish and man. Elsevier, Amsterdam, The Netherlands. LOCKYER, C. 1995b. Aspects of morphology, body fat condition and biology of the harbour porpoise, Phocoena phocoena, in British waters. Report of the International Whaling Commission (Special Issue 15):199–209. MANN, J. 1997. Individual differences in bottlenose dolphin infants. Family Systems 4: 35–49. MANN, J., AND H. BARNETT. 1999. Lethal tiger shark (Galeocerdo cuvier) attack on bottlenose dolphin (Tursiops sp.) calf: Defense and reactions by the mother. Marine Mammal Science 15:568–573. MANN, J., AND B. SARGEANT. 2003. Like mother, like calf: The ontogeny of foraging traditions in wild Indian Ocean bottlenose dolphins (Tursiops sp.). Pages 236–266 in D. M. Fragaszy and S. Perry, eds. The biology of traditions. Cambridge University Press, Cambridge, U.K. MANN, J., AND B. B. SMUTS. 1998. Natal attraction: Allomaternal care and mother–infant separations in wild bottlenose dolphins. Animal Behavior 55:1097–1113. MANN, J., AND B. SMUTS. 1999. Behavioral development in wild bottlenose dolphin newborns (Tursiops sp.). Behavior 136:529–566. MANN, J., AND J. J. WATSON-CAPPS. 2005. Surviving at sea: Ecological and behavioral predictors of calf mortality in Indian Ocean bottlenose dolphins (Tursiops sp.). Animal Behavior 69:899–909. MANN, J., R. C. CONNOR, L. M. BARRE AND M. R. HEITHUS. 2000. Female reproductive success in bottlenose dolphins (Tursiops sp.): Life history, habitat, provisioning, and group-size effects. Behavioral Ecology 11:210–219. MCBRIDE, A. F., AND H. KRITZLER. 1951. Observations on pregnancy, parturition, and postnatal behavior in the bottlenose dolphin. Journal of Mammology 32:251–266. MCLELLAN, W. A., H. N. KOOPMAN, S. A. ROMMEL, A. J. READ, C. W. POTTER, J. R. NICOLAS, A. J. WESTGATE AND D. A. PABST. 2002. Ontogenetic allometry and body composition of harbour porpoises (Phocoena phocoena, L.) from the western North Atlantic. Journal of Zoology London 257:457–471. MILES, J. A., AND D. L. HERZING. 2003. Underwater analysis of the behavioral development of Atlantic spotted dolphin (Stenella attenuata) calves (birth to 4 years of age). Aquatic Mammals 29:363–377. MOORE, J. 1955. Bottle-nosed dolphins support remains of young. Journal of Mammalogy 36:466–467. MYRICK, A. C., AND P. C. PERKINS. 1995. Adrenocortical color darkness as indicators of continuous pre-mortem stress in chased and purse-seined male dolphins. Pathophysiology 2:191–204. NATIONAL RESEARCH COUNCIL. 1992. Dolphins and the tuna industry/Committee on reducing porpoise mortality from tuna fishing. National Academy Press, Washington, DC. NOREN, S. R. 2002. The ontogeny of diving in bottlenose dolphins (Tursiops truncatus). Doctoral dissertation. University of California, Santa Cruz, CA. 132 pp. NOREN, S. R. 2004. Buffering capacity of the locomotor muscle in cetaceans: Correlates with postpartum development, dive duration, and swim performance. Marine Mammal Science 20: 808–822. NOREN, S. R., AND T. M. WILLIAMS. 2000. Body size and skeletal muscle myoglobin of cetaceans: Adaptations for maximizing dive duration. Comparative Biochemistry and Physiology 126A:181–191. NOREN, S. R., T. M. WILLIAMS, D. A. PABST, W. A. MCCLELLAN AND J. L. DEAROLF. 2001. Development of diving in marine endotherms: Preparing the skeletal muscles of dolphins, penguins, and seals for activity during submergence. Journal of Comparative Physiology B 171:127–134. 28 MARINE MAMMAL SCIENCE, VOL. 23, NO. 1, 2007 NOREN, S. R., G. L. LACAVE, R. S. WELLS AND T. M. WILLIAMS. 2002. The development of blood oxygen stores in bottlenose dolphins (Tursiops truncatus): Implications for diving capacity. Journal of the Zoological Society of London 258:105–113. NOREN, S. R., V. CUCCURULO AND T. M. WILLIAMS. 2004. The development of diving bradycardia in bottlenose dolphins (Tursiops truncatus). Journal of Comparative Physiology B 174:139–147. NORRIS, K. S., AND J. H. PRESCOTT. 1961. Observations on Pacific cetaceans of Californian and Mexican Waters. University of California Publications in Zoology 63:291–402. NORRIS, K. S., B. WÜRSIG, R. S. WELLS AND M. WÜRSIG. 1994. The Hawaiian spinner dolphin. University of California Press, Berkeley, CA. PACKER, C., S. LEWIS AND A. PUSEY. 1992. A comparative analysis of non-offspring nursing. Animal Behavior 43:265–274. PEDDEMORS, V. M. 1990. Respiratory development in a captive-born bottlenose dolphin. South African Journal of Zoology 5:178–184. PEDDEMORS, V. M., A. W. FOTHERGILL AND V. G. COCKCROFT. 1992. Feeding and growth in a captive-born bottlenose dolphin, Tursiops truncatus. South African Journal of Zoology 37:74–80. PERKINS, P. C., AND E. F. EDWARDS. 1999. Capture rate as a function of school size in pantropical spotted dolphins, Stenella attenuata, in the eastern tropical Pacific Ocean. Fishery Bulletin 97:542–554. PERRIN, W. F. 2002a. Atlantic spotted dolphin (Stenella frontalis). Pages 47–49 in W. F. Perrin, B. Würsig and J. Thewissen, eds. Encyclopedia of marine mammals. Academic Press, San Diego, CA. PERRIN, W. F. 2002b. Pantropical spotted dolphin (Stenella attenuata). Pages 865–867 in W. F. Perrin, B. Würsig and J. Thewissen, eds. Encyclopedia of marine mammals. Academic Press, San Diego, CA. PERRIN, W. F., AND S. B. REILLY. 1984. Reproductive parameters of dolphins and small whales of the family Delphinidae. Report of the International Whaling Commission (Special Issue 6):97–133. PSARAKOS, S., D. L. HERZING AND K. MARTEN. 2003. Mixed species associations between Pantropical spotted dolphins (Stenella attenuata) and Hawaiian spinner dolphins (Stenella longirostris) off Oahu, Hawaii. Aquatic Mammals 29:390–395. RALLS, K., K. KRANZ AND B. LUNDRIGAN. 1986. Mother–young relationships in captive ungulates: Variability and clustering. Animal Behavior 34:134–145. READ, A. J., R. S. WELLS, A. A. HOHN AND M. D. SCOTT. 1993. Patterns of growth in wild bottlenose dolphins, Tursiops truncatus. Journal of Zoology London 231:107–123. REID, K., J. MANN, J. R. WEINER AND N. HECKER. 1995. Infant development in two aquarium bottlenose dolphins. Zoo Biology 14:135–147. REIDMAN, M. L. 1982. The evolution of alloparental care and adoption in mammals and birds. The Quarterly Review of Biology 57:405–435. REISS, D. 1984. Observations on the development of echolocation in young bottlenose dolphins. Pages 121–127 in P. Nachtigall and P. Moore, eds. Animal sonar. Plenum Press, New York, NY. SCOTT, M. D., R. S. WELLS AND A. B. IRVINE. 1990. A long-term study of bottlenose dolphins on the west coast of Florida. Pages 235–244 in S. J. Leatherwood and R. Reeves, eds. The bottlenose dolphin. Academic Press, San Diego, CA. SMOLDERS, J. 1988. Adoption behavior in the bottlenose dolphin. Aquatic Mammals 14:78– 81. SMOLKER, R. A., J. MANN AND B. B. SMUTS. 1993. Use of signature whistles during separations and reunions by wild bottlenose dolphin mothers and infants. Behavioral Ecology and Sociobiology 33:393–402. STRINGHAM, S. 1974. Mother–infant relationships in moose. Nature Canada 101:325-369. TAVOLGA, M. C., AND F. S. ESSAPIAN. 1957. The behavior of the bottle-nosed dolphin (Tursiops truncatus): Mating, pregnancy, parturition and mother–infant behavior. Zoologica 42:11–31. NOREN AND EDWARDS: DEVELOPMENT OF DELPHINIDS 29 TAYLER, C. K., AND G. S. SAAYMAN. 1972. Social organization and behavior of dolphins and baboons. Annals of the Cape Provincial Museum of Natural History 9:11–49. THURMAN, G. D., AND M. C. WILLIAMS. 1986. Neonatal mortality in two Indian Ocean bottlenose dolphins bred in captivity. Aquatic Mammals 12:83–86. TRIOSSI, F., D. S. PACE, M. L. TERRANOVA AND P. RENZI. 1998. The development of suckling behavior in two captive-born calves of bottlenose dolphins (Tursiops truncatus). Aquatic Mammals 24:75–83. WADE, P. R. 1995. Abundance and population dynamics of two eastern Pacific dolphins, Stenella attenuata and Stenella longirostris. Ph.D. dissertation. University of California, San Diego, CA. 255 pp. WADE, P. R. 2002. Assessment of the population dynamics of the northeastern offshore spotted and eastern spinner dolphin populations through 2002. National Marine Fisheries Service Science Center Administrative Report LJ-02-13. 55 pp. Available from Southwest Fisheries Science Center, 8604 La Jolla Shores Drive, La Jolla, CA 92037. WEIHS, D. 2004. The hydrodynamics of dolphin drafting. Journal of Biology 3:1–23. WELLS, R. S. 1991. Bringing up baby. Natural History (August): 56–62. WELLS, R. S. 2003. Dolphin social complexity: Lessons from long-term study and life history. Pages 32–56 in F. B. M. de Waal and P. L. Tyack, eds. Animal social complexity: Intelligence, culture, and individualized societies. Harvard University Press, Cambridge, MA. WELLS, R. S., AND M. D. SCOTT. 2002. Bottlenose dolphins. Pages 122–128 in W. F. Perrin, B. Würsig and J. Thewissen, eds. Encyclopedia of marine mammals. Academic Press, San Diego, CA. WHITEHEAD, H., AND J. MANN. 2000. Female reproductive strategies of cetaceans: Life histories and calf care. Pages 219–246 in J. Mann, R. C. Connor, P. Tyack and H. Whitehead, eds. Cetacean societies: Field studies of dolphins and whales. University of Chicago Press, Chicago, IL. Received: 12 September 2005 Accepted: 11 May 2006 SUPPLEMENTARY MATERIAL The following supplementary material is available for this article online: Supplementary Appendix S1