Research Article Received: 28 April 2015
Revised: 27 June 2015
Accepted: 29 June 2015
Published online in Wiley Online Library
Rapid Commun. Mass Spectrom. 2015, 29, 1676–1686 (wileyonlinelibrary.com) DOI: 10.1002/rcm.7271
Stable carbon and nitrogen isotope values of dorsal spine age rings indicate temporal variation in the diet of striped marlin (Kajikia audax) in waters around Cabo San Lucas, Mexico Tatiana A. Acosta-Pachón1*, Sofia Ortega-García1 and Brittany Graham2 1
Instituto Politécnico Nacional-CICIMAR, Departamento de pesquerías y biología marina, Avenida IPN s/n. La Paz, B.C.S. 23096, Mexico 2 National Institute of Water and Atmospheric (NIWA) Research Ltd., Wellington 6021, New Zealand Rationale: Billfishes, such as marlin, are top pelagic predators that play an important role in maintaining the stability of marine food webs. Notwithstanding the importance of these species, there remain gaps in our knowledge on their movements, foraging, and trophic status in the early stage of life. METHODS: We measured the δ13C and δ15N values in each annual growth band deposited in the dorsal spine from striped marlin caught off Cabo San Lucas, Mexico, to produce retrospective isotopic profiles that would enable us to detect any significant isotopic changes across development. The samples were analyzed using an elemental analyzer coupled to an isotope ratio mass spectrometer. RESULTS: There was no relationship between the size of striped marlin and the δ15N values. Differences in δ15N mean values across different age classes were not significant and the variation in δ15N values through the marlins’ life cycle was less than 2‰. However, the mean δ15N values between individuals varied by up to 6‰. The δ13C values increased as a function of age, and the mean δ13C values varied significantly between age classes. CONCLUSIONS: Fin spines can be used to construct retrospective isotopic histories for the investigation of trophic dynamics and migratory histories in billfishes, for which population dynamics are often poorly known. Copyright © 2015 John Wiley & Sons, Ltd.
Marine pelagic ecosystems face a number of threats including overfishing, climate change, resource exploitation, and introduced species.[1] Each of these factors can have wideranging effects, from affecting the structure and function of marine food webs to altering resource competition among top predators.[2–4] Top predators can play a key role in maintaining the stability of marine food webs by exerting top-down control on their prey, but these relationships shift as prey abundance varies.[2,3,5] In addition, physical and biogeochemical changes in the environment can affect the spatial and seasonal distribution of species, which can lead to changes in prey availability[6] and, in turn, the recruitment and growth of the top predators.[7] Billfishes are a key component of the pelagic predator guild and the reduction in their abundance due to exploitation by commercial fisheries raises questions about the ecological consequences.[8] In particular, striped marlin (Kajikia audax) represents an important commercial and recreational resource throughout its range in Indo-Pacific tropical and sub-tropical areas. In the Pacific Basin, striped marlin are captured from around 45° N in the North Pacific to 30° S in
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* Correspondence to: T. A. Acosta-Pachón, Instituto Politécnico Nacional-CICIMAR, Departamento de pesquerías y biología marina. Avenida IPN s/n. La Paz, B.C.S. 23096, Mexico. E-mail:
[email protected]
Rapid Commun. Mass Spectrom. 2015, 29, 1676–1686
the eastern South Pacific,[7] with the largest catches taken as bycatch by tuna (Thunnus spp.) longline fisheries (in vessel classes 1–4).[9] Commercial fisheries for tuna and associated species have grown continuously since the 1950s and have removed more than 50 million tons of large pelagic fishes,[10] an estimated 90% of the global commercial catch of billfishes taken by fisheries targeting other species.[11] Data from these fisheries show a 50-year record of impact on open-ocean ecosystems, so the variability in biomass over time and among stocks cannot be entirely attributed to fishing.[10] In the eastern Pacific, K. audax have been caught by commercial and recreational fisheries for many decades off the southwestern coast of the State of Baja California Sur, and the Cabo San Lucas fishing and resort center.[12] The Cabo San Lucas region is the most important sport fishing area on the Pacific coast for large top predators. Striped marlin can be caught almost year-round, with lower catches in summer. This level of activity is consistent with Cabo San Lucas as a core area where striped marlin aggregate and feed.[13,14] Despite the importance of this fishery, there remain gaps in our knowledge on the movements, foraging behavior and trophic status of the striped marlin.[14–17] Understanding key biological characteristics is important to determine the status of striped marlin and it is necessary in order to practise sustainable management.[17] Stomach contents analysis is a standard approach to determine the diet of marine fish.[18] The technique is time and labor intensive but it is limited to presenting only a
Copyright © 2015 John Wiley & Sons, Ltd.
Stable isotopes profiles in striped marlin dorsal spine
Rapid Commun. Mass Spectrom. 2015, 29, 1676–1686
on the diet over the lifetime of an individual,[44–46] reflecting and retaining the isotope value for the time period during which the growth band was formed.[44] Striped marlin dorsal fin spines are calcified structures of cortical bone that are used for their age determination because the growth bands form annually.[47–51] A complete band consists of a wide, opaque zone that reflects faster growth, followed by a narrow, translucent zone that reflects slower growth.[47] This suggests that fin spines may retain information about the trophic history of the billfish in a similar manner to vertebrae in sharks.[41,42] Thus, sampling the isotope values along the fin spines could be a powerful approach to investigating the feeding ecology and movement over the lifetime of the pelagic predators. In this study, we used stable isotope analysis to determine potential changes in the trophic status and movements of striped marlin caught in Los Cabos area. We determined the δ13C and δ15N values of the age bands in the dorsal fin spine to infer shifts in the diet and movement of striped marlin, and the differences between the δ13C and δ15N values of dorsal spine (solid cortical bone) and muscle tissues. The mean δ15N and δ13C values of muscle were then compared with those of the last growth band of the dorsal spine to provide a context for comparing our results with those from other diet stable isotope studies. To our knowledge, this is the first stable isotope study conducted on billfish dorsal fin spines.
EXPERIMENTAL Field collections Dorsal spines were collected from 15 striped marlin caught by recreational fishers off the coast of Los Cabos (~23° N, ~110° W; Fig. 1) in March through October 2012 (Table 1). The length of each striped marlin was measured (lower jaw fork length, in cm), the sex was identified, and the date of capture recorded. The extracted fourth dorsal fin spine, including the condyle, was used because this spine is most commonly used for determining age.[46,51–53] Preparation of samples Each complete dorsal fin and the adjacent dorsal muscle tissue were placed in labeled plastic bags and frozen at –20 °C until the fourth spine was removed in the laboratory. To ensure that the correct spine of the fin was collected, the first section of the dorsal fin was collected in the field and the spines were separated in the laboratory. The first four spines of the dorsal fin are solid cortical bone; the more caudal elements appear as rays that branch distally.[54] Excess material surrounding the condyle of the fourth dorsal fin spine (D4) was removed with caution to avoid scraping the margin of the spine. The spines were oven-dried 50 °C for 24 h. Prior to sectioning the D4, the maximum width of the condyle (CW) was measured (±0.1 mm) with a manual caliper and marks were made at ¼ CW to indicate the location where sections were to be removed. Transversal sections of ~0.6 mm thickness were cut using a low-speed lapidary saw. The first spine subsection was used for
Copyright © 2015 John Wiley & Sons, Ltd.
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snapshot of recently ingested food, and it may also be biased by differential digestion rates of the prey.[19–22] A complementary technique to stomach content analysis is stable isotope analysis (SIA), which can yield information on the diet, movements, and trophic relationships in marine food webs. Depending on the type of tissue analyzed, SIA can cover a variety of timescales.[23] The stable isotope composition of carbon (13C/12C) and nitrogen (15N/14N) in a tissue or organ reflects an integration of diet related to the turnover rate of that tissue, which can be used as a tracer of foraging variation based on seasonal variations in diet.[23–28] The carbon isotope ratios (δ13C values) of animals are commonly used to determine the source of primary production fueling the local food web,[23,29] because the δ13C value is conserved from phytoplankton to resident predators, with enrichment in 13C of 0.5), or between their δ13C values in D4 (t = 1.95; p >0.1) or muscle (t = 0.73; p >0.1). Based on dorsal spine annual rings, four age groups were created for the striped marlin (Table 2). The most common group collected in 2012 was age 6 (n = 8) and the oldest individual was age 8 (Table 2). The assessment of age in billfish can be affected by the presence of a vascular zone in the dorsal spine.[52] In this study, a vascular zone was present, but it was not very extensive; therefore, the age estimates were accurate. Although the range in age was 4 to 8 years (Table 1), sampling the growth rings in the D4 provided information from early life stages. In addition, the general C/N average ratio (±SD) for D4 was 3.7 (±0.55) and for muscle 3.1 (±0.53). The C/N average ratio for each age growth ring was determined. Age 6 had the highest ratios and age 2 had the lowest ratios (Table 3). However, the C/N ratios of the growth bands showed little variation. Relationship between isotopic values and size There was no linear relationship between the δ15N values of muscle and the D4 spine as a function of length (R2N-m = 0.09, p
