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δ13C and δ15N in Humboldt squid beaks: understanding potential geographic population connectivity and movement
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Bilin Liu1, 2, 3, Xinjun Chen1, 2, 3, 6, *, Weiguo Qian1, 2, 4, Yue Jin1, Jianhua Li1, 5
Acta Oceanologica Sinica | 2019, 38(10) : 53 - 59
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Acta Oceanologica Sinica | 2019, 38(10): 53-59
• Marine Biology •
δ13C and δ15N in Humboldt squid beaks: understanding potential geographic population connectivity and movement
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Bilin Liu1, 2, 3, Xinjun Chen1, 2, 3, 6, *, Weiguo Qian1, 2, 4, Yue Jin1, Jianhua Li1, 5
Affiliations
  • 1 College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China
  • 2 National Engineering Research Center for Oceanic Fisheries, Shanghai 201306, China
  • 3 Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, Shanghai 201306, China
  • 4 Key Laboratory of Oceanic Fisheries Exploration, Ministry of Agriculture, Shanghai 201306, China
  • 5 Scientific Observing and Experimental Station of Oceanic Fishery Resources, Ministry of Agriculture, Shanghai 201306, China
  • 6 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
Published: 2019-10-25 doi: 10.1007/s13131-019-1487-2
Outline
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We quantified the δ13C and δ15N values in the lower beaks of Humboldt squid, Dosidicus gigas, collected from international waters off Costa Rica, Ecuador, Peru and Chile by Chinese squid jigging vessels during 2009, 2010 and 2013. There was a significant difference in the isotopic values among regions with the lowest value off Ecuador and the highest off Chile, which were interpreted as a function of trophic effects as well as baseline values. However, constant trophic level of D. gigas across its geographic range showed that spatial variation in the baseline of primary production is the main driver responsible for the observed geographic isotope variability. Inter-regional difference and intra-regional convergence of isotope values indicated squid off Costa Rica, Ecuador and Chile belong to different geographically segregated populations, which were previously proved by integrated population identifying method. In contrast, the higher variations in δ13C and δ15N values in a given size group suggest the squid off Peru move and forage in different places. Moreover, potential population exchange could be responsible for the overlap of the isotope values between the squid off Peru and off Chile. On the whole, the spatial difference in isotopic values of Humboldt squid beaks improves our understanding of potential geographic population connectivity and movement.

stable isotope  /  Dosidicus gigas  /  beaks  /  geographic variability  /  trophic level  /  the eastern Pacific Ocean
Bilin Liu, Xinjun Chen, Weiguo Qian, Yue Jin, Jianhua Li. δ13C and δ15N in Humboldt squid beaks: understanding potential geographic population connectivity and movement[J]. Acta Oceanologica Sinica, 2019 , 38 (10) : 53 -59 . DOI: 10.1007/s13131-019-1487-2
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1 Introduction
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The Humboldt squid (Dosidicus gigas) widely inhabits coastal and pelagic waters in the eastern Pacific Ocean (Nigmatullin et al., 2001). The squid is considered to be ecologically and economically important on a global scale, owing to its large geographic range, extremely high fecundity, flexible feeding strategies, tolerance of environmental extremes and great fishery potential (Gilly and Markaida, 2007). Distribution of the Humboldt squid is related to not only its principal prey (Nevárez-Martínez et al., 2000) but also top predators (Jaquet et al., 2003), which means it plays an important trophic role in the ecosystem (Rosas-Luis et al., 2008). Dosidicus gigas supports the largest cephalopod fisheries in the eastern Pacific Ocean including the Gulf of California (Nevárez-Martínez et al., 2000), the coastal and oceanic waters of Peru (Taipe et al., 2001; Chen and Zhao, 2006) and Chile (Zúñiga et al., 2008; Liu et al., 2010) and the Costa Rica Dome (Ichii et al., 2002; Chen et al., 2014) as well as in equatorial regions (Chen et al., 2012).
Stable isotope analysis (SIA) of carbon and nitrogen (δ13C and δ15N) has been widely used in the study of habitat use, movement patterns and trophic position of marine organisms including marine mammals (Mendes et al., 2007), sea birds (Jaquemet et al., 2008), fishes (McMahon et al., 2011) and cephalopods (Ruiz-Cooley et al., 2004, 2013). Stable isotopes in cephalopod soft tissues (e.g., mantle and buccal mass) may reveal environmental information prior to capture because of their relatively quick turnover (Stowasser et al., 2006). In contrast, hard tissues (e.g., beaks, gladii and eye lenses) are metabolically inactive structures with new molecules being continuously laid down and with no turnover after synthesis (Xavier et al., 2015). Consequently, δ13C and δ15N within these structures combine the feeding ecology of cephalopods over their lifespan.
Spatial patterns of stable isotopes in organism tissues reflect variations in baseline values as well as trophic effects. Consequently, geographic variation in δ13C and δ15N in tissues of marine species to some extent represents differences in both habitats and trophic positions. In general, δ13C values reflect the source of primary producers, since they typically only increase by 0.5‰ to 1.5‰ per trophic level (DeNiro and Epstein, 1978). Therefore, the δ13C values in the marine ecosystem are commonly used to discriminate between inshore vs. offshore or pelagic vs. benthic feeding, as well as the lower- vs. higher-latitude plankton (Sherwood and Rose, 2005; Cherel and Hobson, 2007). In contrast, consumers are enriched in 15N by 2‰ to 3.5‰ relative to their food (DeNiro and Epstein, 1981), which provides a possible mechanism to estimate trophic position (Hobson and Welch, 1992).
SIA in cephalopods hard structures is becoming increasingly helpful for countering the paucity of life history data because its inactive metabolism leads to little elemental turnover after formation. Cephalopod bodies contain few hard structures, and the beak is an important one that has been widely used in the application of age determination (Hernández-López et al., 2001), population identification (Martínez et al., 2002) as well as dietary analysis (Xavier et al., 2011). Recently, δ13C and δ15N values in cephalopod beaks have been widely used in the investigation of trophic positions, energy pathways and migrations (Cherel and Hobson, 2005; Hobson and Cherel, 2006; Cherel et al., 2009, 2011).
In this study, we analysed the δ13C and δ15N values in D. gigas beak samples from four geographic regions (Costa Rica, Ecuador, Peru and Chile) in the eastern Pacific Ocean. Our primary aims were to evaluate variability of the stable isotope values across different regions and to identify the potential geographic populations connectivity and movement of such an intra-specific complex species based on the detected spatial difference in isotopes. The yield results will benefit an understanding of the life history of this squid.
2 Materials and methods
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2.1 Squid sampling
A total of 82 squids (17 off Costa Rica, 28 off Ecuador, 20 off Peru and 17 off Chile) with mantle lengths (ML) ranging between 183 mm and 534 mm were collected from 39 stations in the eastern Pacific Ocean, during 2009 to 2013 (Fig. 1). All samples were immediately frozen at sea and dissected in the laboratory after being defrosted. Beaks were extracted, washed and then kept in 75% ethanol until isotopic analysis.
2.2 Stable isotope analysis
Lower beaks were selected for stable isotope analysis. To reduce the interference of possible contaminants, lower beaks were first rinsed in MilliQ water for 5 min and subsequently dried in an oven at 60°C for 48 h prior to isotope analysis. After drying, beaks were homogenized to fine powder with an agate mortar and pestle. Approximately 1–2 mg of samples were weighed into 0.3 mg tin capsules and analyzed using an ISOPRIME 100 isotope ratio mass spectrometer (Isoprime Corporation, Cheadle, UK) and a vario ISOTOPE cube elemental analyzer (Elementar Analysensysteme GmbH, Hanau, Germany) at the Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, at Shanghai Ocean University. The δ13C and δ15N of the samples are expressed in standard notation as the following functions (Fry, 2006):
$\delta {}^{{\rm{13}}}{\rm{C}} = \left({\frac{{({}^{13}{\rm C}/{}^{12}{\rm C})_{\rm{sample}}}}{{({}^{13}{\rm C}/{}^{12}{\rm C})_{\rm{standard}}}} - 1} \right) \times 1\;000,$
$\delta {}^{{\rm{15}}}{\rm{N}} = \left({\frac{{({}^{1{\rm{5}}}{\rm N}/{}^{1{\rm{4}}}{\rm N})_{\rm{sample}}}}{{({}^{1{\rm{5}}}{\rm N}/{}^{1{\rm{4}}}{\rm N})_{\rm{standard}}}} - 1} \right) \times 1\;000,$
where 13C/12C and 15N/14N are the atomic ratios of 13C and 15N in the sample and standards, respectively, and δ is the measure of the ratio of heavy to light isotopes in the sample. The standard reference material for carbon is Vienna Pee Dee Belemnite (V-PDB) and for nitrogen is atmospheric nitrogen (N2). USGS 24 (−16.049‰ V-PDB) was used as the primary standard for 13C, and USGS 26 (53.7‰ N2) was used to quantify 15N. To assess the associated errors within and between runs, repeated analyses of internal laboratory reference standards (Protein (−26.98‰ V-PDB and 5.96‰ N2)) were performed every ten samples. The analytical precision was less than 0.1‰ for both carbon and nitrogen.
2.3 Adjustment for δ15N baseline values
To correctly compare the δ15N values among different regions, we adjusted all specimen δ15N values (referred to as baseline-adjusted δ15N values, BA-δ15N) by subtracting phytoplankton δ15N values obtained for each sampling station (Fig. 1) from a global coupled ocean circulation-biogeochemistry-isotope model with a horizontal resolution of 1.8° (latitude)×3.6° (longitude) and 19 vertical levels (Somes et al., 2010; Navarro et al., 2013).
2.4 Statistical analysis
An analysis of variance (ANOVA) and subsequent Tukey’s pairwise comparison tests were conducted to determine the difference in δ13C and δ15N when multiple comparisons between regions were possible. Bayesian ellipses stable isotope analysis was conduct to compare isotopic niche widths among communities (Jackson et al., 2011). All statistical tests were performed using SPSS 15.0, and significance was determined at α=0.05 level.
3 Results
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3.1 Stable isotope values
The δ13C in the lower beaks of squid from Costa Rica, Ecuador, Peru and Chile had a relatively small range from –18.2‰ to –17.7‰ (–17.9‰±0.1‰), –19.2‰ to –18.5‰ (–19.0‰±0.1‰), –17.8‰ to –15.9‰ (–17.0‰±0.6‰) and –17.1‰ to –16.1‰ (–16.6‰±0.3‰), respectively. The δ15N ranges in the lower beaks of squid from waters off these countries were much larger from 5.9‰ to 7.9‰ (6.9‰±0.5‰), 2.9‰ to 4.7‰ (3.6‰±0.5‰), 6.1‰ to 15.4‰ (9.7‰±2.6‰) and 14.2‰ to 17.0‰ (15.5‰±0.8‰), respectively (Table 1).
3.2 Spatial difference in stable isotope values
ANOVA showed a significant spatial difference both in δ13C and δ15N among regions (Table 2; ANOVA, P<0.05 for both δ13C and δ15N), and the squid samples off Chile had the highest, while the samples from Ecuador had the lowest values (Fig. 2). Pairwise analysis showed that there was a significant inter-regional difference in isotope values between regions (Table 1; Tukey HSD, P<0.05). Scatter plots of δ13C and δ15N showed that squid from different regions were separated clearly except for those from Peru which, to some extent, shared considerable overlaps with those in Costa Rica and Chile (Fig. 3).
3.3 Stable isotope values correlating with squid size
There was no clear increase in δ13C and δ15N values was apparent with ascending squid size for a given study area, except for the sample squid for Peru (F1, 6=55.2, P=0.000<0.05 for δ13C and F1, 6=11.7, P=0.014<0.05 for δ15N). The δ13C and δ15N values of squid off Peru varied greatly in a given size group, while the range of isotopes off Costa Rica, Ecuador and Chile for a given size group were small (Fig. 4).
4 Discussion
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The δ13C and δ15N values in different tissues (muscle, gladii, beaks and eye lenses) of D. gigas were reported over its distribution ranges (Table 3). However, the isotope values in beaks were only reported in the Gulf of California (Ruiz-Cooley et al., 2006, 2011) and coastal Peru (Ruiz-Cooley et al., 2011), which are not covered in this study. A comparative experiment shows that muscle isotope values were higher than isotope values for beak by 1‰ for δ13C and 4‰ for δ15N (Ruiz-Cooley et al., 2006). By adding these enrichment factors to beak values, the adjusted isotope values off Chile and Peru in this study are similar to conclusions previously reported for muscle (Hückstädt et al., 2007; Argüelles et al., 2012). Off Costa Rica and Ecuador, the δ15N values were reported in another chitin structure, the gladius, and were slightly higher than those found in the beaks in this study (Ruiz-Cooley et al., 2010).
4.1 Geographic difference in isotopic values
The potential influence of trophic as well as baseline effects might be responsible for the significant spatial difference in the δ15N values of the Humboldt squid among the four sampling regions in this study. A similar significant geographic variation was also detected in the muscle (Ruiz-Cooley and Gerrodette, 2012) of the same species and also in the squid Sthenoteuthis oualaniensis (Takai et al., 2000). Indeed, dietary studies showed D. gigas has a relatively constant trophic level about 4 across its geographic range, although it can feed on a large range of food (Markaida and Sosa-Nishizaki, 2003; Field et al., 2007; Tam et al., 2008). Therefore, spatial variation in the baseline of primary production (4.96‰–5.10‰ in Costa Rica, 1.83‰ in Ecuador, 3.65‰–4.51‰ in Peru and 0.04‰–2.27‰ in Chile) is likely responsible for the observed geographic variability of δ15N values rather than trophic level.
Baseline adjustment is a good approach only able to account for variability in baseline values in the areas of capture. Thus, regional δ15N difference should disappear after baseline adjustment, if D. gigas are resident in each area. To test the hypothesis, we adjusted all specimen δ15N values (referred to as baseline-adjusted δ15N values, BA-δ15N) by subtracting phytoplankton δ15N values obtained for each sampling station from a global coupled ocean circulation-biogeochemistry-isotope model (Somes et al., 2010). However, the BA-δ15N values still show significant inter-regional variation except for between Costa Rica and Ecuador (Fig. 2). Therefore, if any of these squids are recent migrants to the areas where they were captured, a baseline correction would not properly adjust their isotope values. Given that whole beaks integrate feeding over the entire lifespan, any feeding and movements across different isoscapes during their lifespans would create spatial variability in beak isotope values and some degree of spatial baseline bias from areas outside of the capture location is certainly possible (Young et al., 2015).
Unlike δ15N, there was a more restricted range (3.3‰) in the δ13C values with a gradual increase from –19.2‰ (Ecuador) to –15.9‰ (Peru). In the marine ecosystem, the δ13C values commonly reflect sources of primary productivity and vary greatly with latitude and distance to shore (Cherel and Hobson, 2007). Therefore, in the current study, a significant difference in δ13C values may reflect a geographic shift. For example, in this study, Ecuador samples with lower δ13C values (–19.0‰) were taken more offshore than the samples from other regions, and Chile squid from higher latitudes had higher δ13C values (–16.6‰) than those from Peru (–17.0‰) and Costa Rica (–17.9‰), which is consistent with the conclusion revealed in D. gigas muscle by Ruiz-Cooley and Gerrodette (2012). Such geographic differences were also reported in both muscle and beaks of the same species in the Gulf of California (Ruiz-Cooley et al., 2006), and are consistent with the findings reported for the common Japanese squid (Todarodes pacificus) corresponding to two different sampling regions which were also associated with different geographic populations (Ikeda et al., 1998).
4.2 Population connectivity and movement
Although the isotopic values of squid sampled off Peru shared some overlaps with Costa Rica and Chile (Fig. 3), the sampled squid could be clearly grouped by region according to the significantly different δ13C and BA-δ15N values found in the beaks. The intra-regional similarity of BA-δ15N values in the beaks of the squid from Chile, Costa Rica and Ecuador (Fig. 3), indicated that the squid from a given area tend to have a small range of food. While large range of BA-δ15N values indicates squid from Peru occupy a large range of trophic level.
Similar δ13C values for individuals within a given region except for Peru (with range of 0.5‰ for Costa Rica, 0.6‰ for Ecuador and 1.1‰ for Chile) would be consistent with local feeding linked to a common source of primary production. This indicate that individuals from a given region might share similar primary productivity values over their life, or they experience regionally-distinct isotope values at early life but would have spent a sufficient period of time at the location-of-capture to influence the whole beak isotope values. Previous studies successfully identified these squid as spatially segregated populations based on the analysis of geographic heterogeneous isotopic values in gladius (Ruiz-Cooley et al., 2010), and elemental signature in early ontogenetic statolith (Liu et al., 2015a) as well as spatial variation in beak size (Liu et al., 2015b). Consequently, inter-regional differences and intra-regional convergence of δ13C and δ15N values in the beak indicate that the squid from Costa Rica, Ecuador and Chile belong to different geographic populations.
Off Ecuador, there were no overlaps of the isotope values with other regions (Fig. 3) which led us to believe that the squid off Ecuador are an independent population and do not have any exchange with other populations. Yan et al. (2011) reported that the squid off Ecuador have significant genetic differentiation from both the squid off Peru and those from Costa Rica, and this was further proved by Liu (2014) who recommended that the high geographic genetic diversities and significant genetic differentiation were caused by ocean currents and historical factors.
Elemental signature analyses have shown that D. gigas off Costa Rica is a specific population having a narrow movement (Liu et al., 2015a) which is in agreement with our view in this study. This conclusion was also presented by Ruiz-Cooley et al. (2010), because the squid spawn off the Costa Rica Dome and nursery and feed in the vicinity (Chen et al., 2013; Liu et al., 2015a).
Off Peru, a higher variation in δ13C and BA-δ15N values within a given size group (Fig. 4) indicated that intra-regional differences in isotope values from the same size group was more likely caused by baseline shifts than squid size. Thus, larger δ13C and BA-δ15N ranges indicate that these squid consequently move and feed in different places and subsequently display distinct isotopic values as they grow. Therefore, we hypothesize that the squid off Peru might move and forage in different places with distinct isotopic values as they grow, where squid movement is strongly influenced by the Humboldt Current (Anderson and Rodhouse, 2001). This multivariate inter-individual migration pattern can also been seen in the offshore waters of Northern Peru (Lorrain et al., 2011).
Scatter plots of δ13C and BA-δ15N values (Fig. 3) seem to indicate some of these origins were from Chile and Costa Rica. However, natural tags and molecular methods proved that D. gigas from the southern and northern hemispheres should have different natal origins (Sandoval-Castellanos et al., 2007, 2010; Staaf et al., 2010). Molecular methods analysis showed significant genetic differentiation between the squid off Costa Rica and off Peru (Yan et al., 2011). Therefore, the overlap of the isotope values between the squid off Peru and off Costa Rica was not a result of population exchange but experience of the same baseline isotopic history. Although variation in beak size and statolith elemental signature implies that D. gigas off Peru and Chile were interpreted as different geographic populations (Liu et al., 2015b), considerable overlaps indicated that they should, to a certain extent, have experienced population exchange. This was genetically verified by Sandoval-Castellanos et al. (2007) and Ibáñez et al. (2011), who suggested that Peru currents and its countercurrents were responsible for the population interchange. Thus, the exchange is likely to be responsible for the overlap of the isotope values between the squid off Peru and off Chile in this study.
Acknowledgements
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Special thanks to the anonymous reviewers for helpful comments on the manuscript. We thank Chunxia Gao for the measurement of isotope values and Christopher J. Somes for sharing baseline isotope data. We thank Pauline H. Lovell for editing the English text of a draft of this manuscript.
Funding
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  • The Shanghai Pujiang Program under contract No. 18PJ1404100; the Program for Professor of Special Appointment (Eastern Scholar) at Shanghai Institutions of Higher Learning under contract No. 0810000243; the National Natural Science Foundation of China under contract Nos 41306127 and 41276156.
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Year 2019 volume 38 Issue 10
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doi: 10.1007/s13131-019-1487-2
  • Receive Date：2018-05-23
  • Online Date：2026-04-01
  • Published：2019-10-25
Article Data
Affiliations
History
  • Received：2018-05-23
  • Accepted：2019-02-19
Funding
The Shanghai Pujiang Program under contract No. 18PJ1404100; the Program for Professor of Special Appointment (Eastern Scholar) at Shanghai Institutions of Higher Learning under contract No. 0810000243; the National Natural Science Foundation of China under contract Nos 41306127 and 41276156.
Affiliations
    1 College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China
    2 National Engineering Research Center for Oceanic Fisheries, Shanghai 201306, China
    3 Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, Shanghai 201306, China
    4 Key Laboratory of Oceanic Fisheries Exploration, Ministry of Agriculture, Shanghai 201306, China
    5 Scientific Observing and Experimental Station of Oceanic Fishery Resources, Ministry of Agriculture, Shanghai 201306, China
    6 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China

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表12种不同金属材料的力学参数
科
Family		 属数
Number of
genus		 种数
Number of
species		 占总种数比例
Percentage of
total species (%)		 属
Genus		 种数
Number of
species		 占总种数比例
Percentage of total
species (%)
鹅膏菌科Amanitaceae 2 11 5.26 鹅膏菌属 Amanita 10 4.78
小菇科 Mycenaceae 2 12 5.74 丝盖伞属 Inocybe 5 2.39
多孔菌科 Polyporaceae 8 14 6.70 蜡蘑属 Laccaria 5 2.39
红菇科 Russulaceae 3 23 11.00 小皮伞属 Marasmius 6 2.87
小菇属 Mycena 11 5.26
光柄菇属 Pluteus 5 2.39
红菇属 Russula 17 8.13
栓菌属 Trametes 5 2.39
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