Oceanic squids are typical species that sensitive to the environment change. Previous studies on oceanic squids mainly focus on its annually fluctuated abundance under the background of climate change. The changes of individual morphological sizes, including body and beak, have been observed in recent years. In this study, Ommastrephes bartramii, an important cephalopod species in North Pacific Ocean, has been selected to analyze the annual morphological changes of body and beak under different scales of climate events. Geometric morphometrics was used to analyze the shape variations of both upper beak and lower beak. The possible phenotypic plasticity of body and beak was also discussed in different aspects. Body size showed different variations among different climatic years. The size at the maturity stage in 2015 (El Niño year) was much smaller than that in other years for both sexes. The centroid size representing the beak size showed the significant difference between two types of Pacific Decadal Oscillation phases. The shapes of upper and lower beaks showed significant differences between small-scale climatic patterns in which El Niño or La Niña event occurred, displaying different growth patterns.
Pelagic cephalopods, mostly belonging to Ommastrephidae, are a typical marine invertebrate widely distributed in the temperate and subtropical waters around the world (Chen et al., 2008; Jereb & Roper, 2010). Generally, these squids have a short lifetime less than two years (mostly one year) and are characterized by the life cycle of “grow fast, die young” (Pecl et al., 2004). As a result, the highly fluctuated abundance of pelagic squid has been mentioned by some researchers in recent years (Igarashi et al., 2017; Yu et al., 2019a; Alabia et al., 2020). The potential response of pelagic squid to the climate change has also been discussed (Yu et al., 2019a, b).
With the increasing number of extreme climate events, changes of feeding habitat and food composition increasingly influenced squids (Yu et al., 2019a; Portner et al., 2020). Sea surface temperature (SST) is the most frequently discussed index in previous studies (Chen, 2010; Frawley et al., 2019). The abundance of squids (always represented by catch per unit effort (CPUE) in fishery) showed significant annual fluctuations due to small-scale climate events (El Niño/La Niña) (Yu et al., 2018; Ji et al., 2020). Some large-scale climate events (e.g. Pacific Decadal Oscillation, PDO) also significantly affected marine species in some areas (Kim et al., 2018). In addition, the significant increase in SST also strongly changed the distribution pattern (Yu et al., 2019a), body size and life span of oceanic squids (Arkhipkin et al., 2015a; Takahara et al., 2017). However, the interannual variation of squid body size was rarely reported (Argüelles et al., 2008).
Beak, as the main feeding organ of squid, is one of the important hard corrosion resistance structures in cephalopod (Fang et al., 2016a, b). This hard structure is not only taxon-dependent, but also stock- and sex-dependent in some species (Martínez et al., 2002; Bolstad, 2006; Chen et al., 2012). The lower beak morphology or the relationship between its morphometric and mantle length is a standard criterion for the cephalopod taxonomic recognition (Jackson & McKinnon, 1996; Jackson et al., 1997; GroÈger et al., 2000; Lefkaditou and Bekas, 2004; Fang et al., 2015). Due to the strong relationship between the body size and beak shape, beak is a proper material for the detection of squid body change. However, the beak shape is also influenced by the changes in the ambient environment, including the habitat suitability and food availability (e.g. Dosidicus gigas (d’Orbigny, 1835), Hu et al., 2019; Ommastrephes bartramii (Lesueur, 1821), Fang et al., 2020).
Most of previous studies were focused on beak morphometrics with the traditional linear distance method (Fang et al., 2014; Liu et al., 2015). This is a simple method, although relevant measurements may increase the potential risk of bias to some degree (Bookstein, 1998; Adams et al., 2004). Moreover, the lack of geometric information also limits the application of the traditional method. Geometric morphometrics (GM) has been proposed to avoid the limitation (Adams et al., 2013). A large number of variables in GM can ensure that even a small shape difference (e.g. reduced morphological variability or population level) can be detected (Collyer et al., 2015). In addition, the object size is closely related to its shape (Klingenberg, 2016), and shape variation may be influenced by allometry. GM can mathematically separate shape from size and thus elucidate the level of correlation between two traits (Rohlf and Slice, 1990; Mitteroecker et al., 2013).
Ommastrephes bartramii is the most important oceanic squid widely distributed in the North Pacific Ocean (Bower and Ichii, 2005). The environment-induced abundance fluctuation was reported (Chen, 2010; Yu et al., 2017), but the potential change in body size or beak shape is still unknown. In this study, in order to investigate the change patterns of body size and beak shape under different environment conditions, we selected squid samples from different climatic years and statistically compared the interannual body size change and beak shape difference according to GM method for the analysis of beak morphology.
Materials and methods
Sampling and image acquisition
The samples were collected in 2009, 2010, 2015 and 2016 by the Chinese commercial jigging vessels in the main fishing ground for Ommastrephes bartramii (150 °E to 160 °E, 35 °N to 45 °N) (Table 1). Different climate events were observed in the North Pacific Ocean in the above four years. El Niño and La Niña events were all presented by the mean values of SSTA during the sample months. The PDO index is the leading empirical orthogonal function (EOF) of monthly sea surface temperature anomalies (SSTA) over the North Pacific (poleward of 20 °N) after the global average sea surface temperature has been removed (Deser et al., 2010). During a “positive” phase of PDO, the west Pacific becomes cooler and part of the eastern ocean warms; during a “negative” phase of PDO, the opposite pattern occurs (Mantua et al., 1997). In this study, large-scale climate varied from cold (negative) PDO phase in the years of 2009 to 2013 to warm (positive) PDO phase in the years of 2014 to 2016. El Niño (2009 and 2015) and La Niña (2010 and 2016) also happened in the changing climatic years (Fig. 1). Therefore, the squid samples in El Niño and La Niña years from different large-scaled climate events were collected and selected for morphometric analysis (Table 1).
Dorsal mantle length (ML) was measured to the nearest 1 mm after samples were captured and randomly selected on the deck. The squid samples were dissected with scissors to observe the maturity stage according to the method by Lipiński & Underhill (1995). All the upper (UB) and lower beaks (LB) were successfully dissected from the buccal mass of the samples and then stored in 75% ethyl alcohol. Since a beak was a parallel structure, we focused on one side of the beak to analyze and simulate the morphological variation. Each picture of UB and LB was photographed with Nikon D7000 camera in the same lens and a scale (ruler) was placed in each picture to enhance the morphometric standardization (Crespi-abril et al., 2010; Fang et al., 2017, 2018). Landmarks were chosen according to the previous study, including 8 landmarks and 2 semi-landmarks for UB and 10 landmarks and 10 semi-landmarks for LB (Fang et al., 2017, Fig. 2). The combination of landmarks and semi-landmarks was used to describe the beak characteristics and better simulate the shape of beak (Neige and Dommergues, 2002; Gunz and Mitteroecker, 2013).
These series of landmarks were digitized by two different persons to minimize the measurement errors and the first digitized data set was chosen when the error between two measurements was less than 5% (Viscosi and Cardini, 2011). If the error was higher than 5%, a third person would be digitized again until the error between two data sets was less than 5% and then chose the first of them for the analysis (Viscosi and Cardini, 2011). A series of coordinate-based datasets were standardized in size and the landmark configuration was translated and rotated through the generalized least-squares Procrustes analysis (GPA, Rohlf and Slice, 1990). The positions of semi-landmarks were optimized with Procrustes distance criterion to minimize the Procrustes Distance across samples during GPA (Bookstein, 1998). The semi-landmarks slid separately, so that their positions were not influenced by the rest landmarks (Gunz and Mitteroecker, 2013).
An ANOVA test was performed to evaluate the variations of mantle length and size of mature individuals among different years. We performed the Procrustes MANCOVA to investigate the effects of climatic factors (including small-scale and large-scale factors), sex and their interaction on the beak shape variation. Then, to reduce the redundancy of Procrustes shape coordinate, the principal component analysis (PCA) on Procrustes coordinates was performed (Dryden and Mardia, 1998) and the beak shape variation associated with each principal component (PC) was graphically depicted. Multivariate patterns of beak shape variation were visualized with the scores from multivariate regressions of beak shape versus log(Centroid Size). Furthermore, in order to facilitate the climate comparison, the predicted values, which was the regression of shape on size were chosen to compare the allometric trend among factors (Adams and Nistri, 2010). Thus, the plots of the predicted values from multivariate regressions by years (in different climatic patterns) versus log(Centroid Size) were also generated (Adams and Nistri, 2010; Kelly et al., 2013). Thin-plate spline (TPS) deformation grids for the phenotypic mean shapes of O. bartramii at different scales of climatic patterns were also presented to improve the ecological interpretation of allometric changes in beak shape. All the statistical analyses were performed in R 3.5.3 (R Core Team, 2019) with the package ‘‘geomorph’’ (Adams & Otarola-Castillo, 2013).
Body size variation in different years
Mantle length showed the different changing trends among different climatic years (Fig. 3). As for females, mean ML was the largest (295.3 mm) in 2016 and the smallest (249.2 mm) in 2010. The female samples in 2009, 2010 and 2015 with the ML of 240–320 mm accounted for approximately 80% of total female samples (Fig. 3A). In 2016, the ML range of the majority of female samples was 280–360 mm (Fig. 3A). The ML of female samples with the highest proportion was 280 mm in 2009 and 2015 (more than 40%), 240 mm in 2010 (nearly 50%) and 320 mm in 2016 (nearly 35%) (Fig. 3A). Similarly, for males, mean ML was the largest (260.2 mm) in 2016 and the smallest (243.6 mm) in 2010. The ML range of the majority of male samples was 240–320 mm in all the selected years and accounted for more than 90% of the total male samples in all the investigated years except 2015 (81.25%) (Fig. 3A). The ML of male samples with the highest proportion was 280 mm in 2009, 2015 and 2016 (more than 40%) and 240 mm in 2010 (nearly 50%) (Fig. 3A). Significant differences were found between different years for both males and females (ANOVA, ♀:F = 35.23, P = 0.0001; ♂: F = 41.87, P = 0.0001).
The body size at the maturity stage of female squid samples in 2009 and 2010 were large than that in other two years (Fig. 3B). The individuals in 2015 were the smallest with the mean size less than 300 mm at the maturity stage. In all the male samples, the mean size was still the largest in 2009 and the smallest (292.2 mm) in 2015 and the mean sizes in 2010 and 2016 were close to 300 mm (Fig. 3B). The ML of both males and females at the maturity stage showed significant differences among different years (ANOVA, ♀:F = 26.91, P < 0.0001; ♂: F = 23.17, P < 0.0001).
Beak size variation in different years
The centroid size (CS) representing the beak size was calculated by GPA. The result showed that the squid beak size in cold PDO pattern (2009 and 2010) was significantly different from that of warm PDO pattern (2015 and 2016) for UB (ANOVA, F = 14.881, P = 0.0005), but the difference in LB was not significant (ANOVA, F = 0.643, P = 0.0980). The beak size in El Niño years (2009 and 2015) was in the similar small range, but more outliers (below lower quartile) were observed in warm PDO pattern (Fig. 4). The wider quartile of the beak size was depicted in cold PDO pattern with a lower median value in La Niña years (2010 and 2016) for both UB and LB (Fig. 4).
Interannual shape variation of upper beak
Sex and climatic pattern represent the covariates for the analysis of beak shape differences. As for the UB shape, sexual dimorphism was not observed based on the results of MANCOVA (Table 2). However, the UB shape difference in small climatic patterns (El Niño and La Niña events) was detected (Table 2) most probably due to the larger width of the hood observed in thin-plate spline grid configurations (Fig. S1). Allometric trends of UB growth significantly differed between small climatic patterns (Table 2). Large climatic patterns (cold PDO and warm PDO) also showed an interactive effect on small climatic pattern for UB shape (Table 2).
The first four components (PC1, PC2, PC3 and PC4) explained 53.6% of total variation in UB shape (Fig. 5A and B). UB shape significantly increased with the increase in body size in cold PDO pattern (Fig. 6A, left panel), but the change trend of UB shape with the increase in body size was not significant in warm PDO pattern (Fig. 6A, right panel). Predicted values showed negative trends in all the sampling years (Fig. 6B). However, the predict values of the individuals were negative/positive in cold/warm PDO pattern, respectively (Fig. 6B).
Interannual shape variation of lower beak
The Procrustes MANOVA with sex and climatic pattern as covariates revealed that LB shape had no significant difference between sex, but the difference in LB shape between small-scale climatic pattern (El Niño and La Niña event) and large-scale climatic pattern (cold PDO and warm PDO) was significant (Table 3). The configuration result of thin-plate spline grids indicated that the lateral wall shape and width of the wing were the characteristics for distinguish the LB shapes under small-scale climatic pattern and large-scale climatic pattern, respectively (Fig. S2). Allometric growth of LB shape existed among small-scale climatic patterns as well as large-scale climatic patterns (Table 3). Large-scale climatic patterns also had an interactive effect on small-scale climatic patterns for LB shape (Table 3).
The first four components (PC1, PC2, PC3 and PC4) explained 55.3% of total variation in LB shape (Fig. 7A and B). The LB shape varied with the increase in body size under both PDO patterns (Fig. 8A). Predicted values showed positive trends in all the sampling years (Fig. 8B). Most of the individuals’ predicted values in cold PDO pattern were negative (Fig. 8B, left panel) and some of the predicted values in warm PDO pattern (most individuals in 2016 and half of individuals in 2015) were positive (Fig. 8B, right panel).
Body size differences
As a typical phenotypic plasticity species, squids always tend to change their morphology to adapt the changing environment (Arkhipkin et al., 2015a; Jones et al., 2019). In the selected years of this study, the high proportion of small ML groups (< 240 mm) of O. bartramii occurred in 2010 (more than 50% of small groups, Fig. 3) and 2015 (nearly 40% of small groups) and no male sample > 360 mm (Fig. 3). In El-Niño/La Niña years, the small body size could be a consequence of extreme high/low environmental temperatures for other oceanic squids (D. gigas, Keyl et al., 2011), as observed in this study. A higher ambient temperature led to the shrinkage of squid body size, as reported in other species (D. gigas: Arkhipkin et al., 2015a; Todarodes pacificus (Steenstrup, 1880): Takahara et al., 2017). The annual body size variation of D. gigas, which is a sibling species with O. bartramii and has similar biological features (Arkhipkin et al., 2015b), had been discussed in previous studies (Argüelles et al., 2008; Keyl et al., 2008, 2011; Arkhipkin et al., 2015a). Environmental conditions and food availability are the two main causes for this interannual change (Keyl et al., 2008, 2011). Unfavorable temperature might restrain the metabolism of squids, so this phenomenon might also promote body size miniaturization, just like the size at the maturity stage in 2015 in this study (Fig. 3B).
The annual difference in body size of female samples was much bigger than that of male samples (Fig. 3). Body size of females tended to be more plastic than that of males (Fig. 3). Most of previous studies also discussed the variation of female body size in other squid species (e.g. D. gigas, Argüelles et al., 2008; Keyl et al., 2008, 2011; Arkhipkin et al., 2015a). In general, female squids grow faster than males due to their high-rate feeding, thus leading to the faster metabolism and gonadal growth (Markaida et al., 2004; Fang et al., 2016b). This was shown for O. bartramii (Fang et al., 2016b) and D. gigas (Markaida et al., 2004), but also in other oegopsid species, such as Illex illecebrosus (Lesueur, 1821) and Illex argentinus (Castellanos, 1960) (O’Dor 1998). This is a kind of survival strategy to maintain the population in a certain scale (O’Dor 1998).
GM-based beak shape variation among different years
Geometric morphometrics (GM) is a useful method to examine the squid beak shape variation at the stock level (Fang et al., 2017) or in different years (this study), but such variations are too small to be detected. The unusual small centroid size outliers in 2015 (Fig. 4), which were coincident with the ML distribution (Fig. 4), indicated that these small beak shapes were closely related to the slower growth in the beak.
Different scales of climatological and environmental variability, including ENSO events (Chen et al., 2008) and different PDO phases (Yu et al., 2017), may result in large uncertainties of feeding behaviors (Villanueva et al, 2017). This variation of feeding habits, including prey item, may also act as one of the main factors influencing the squid growth, as well as the beak growth. The results of statistical analyses in this study suggested that the beak shape of winter-spring cohort of O. bartramii presented the varied morphology for both UB and LB under different climatological conditions (Tables 2 and 3). The change of feeding habits (i.e. prey type) for squid might be one of the reasons for the variation of beak shape, as reported in other cephalopod species (Matias et al., 2019). The annual beak shape variation was difficult to be identified only from the reconstructed TPS grids (Figs. S1 and S2) because this annual environmental change might not substantially affect the beak shape. However, GM-based statistical analysis results indicated that the annual difference was significant.
Relationship between oceanic squid morphological variation and climate change
In the last several decades, climate change events frequently occurred and induced the landing variation of squids (Igarashi et al., 2017). Actually, the landing fluctuation and the morphological change had been discussed for other squid species in previous studies (Argüelles et al., 2008; Keyl et al., 2008, 2011). The body size change of O. bartramii in El Niño year was similar to that of other Ommastrephidae species, thus it is important to understand the beak morphological variation, which is closely related to the feeding behavior (Hu et al., 2019). Beak shape variation was consistent with the mantle length change in this study, so it is reasonable to emphasize the impact of feeding behavior on the squid body size. Indeed, the morphological size would change under the background of climate change. However, the growth pattern change was seldom reported. Here, in this study, we found that the growth pattern of beak shape was changed in different climate events, regardless of UB and LB (Tables 2 and 3). Oceanic squid is a typical opportunist species and has a large feeding spectrum. A squid can utilize surrounding foods as possible to keep the fast growth rate, even in the circumstance of food deficiency (Watanabe et al., 2004, 2008). In this study, O. bartramii both changed its body size and beak shape. In addition, the body size had a strong resilience and could be largely changed within a short time. This phenomenon was also observed in the beak morphology (Figs. 4 and 5). Thus, the phenotypic plasticity of O. bartramii is a kind of response to the environmental change and can be regarded as a survival strategy.
Adams, D. C. & A. Nistri, 2010. Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology 10: 216.
Adams, D. C. & E. Otárola-Castillo, 2013. Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution 4: 393–399.
Adams, D. C., F. J. Rohlf & D. E. Slice, 2004. Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology 71: 5–16.
Adams, D. C., F. J. Rohlf & D. E. Slice, 2013. A field comes of age: geometric morphometrics in the 21st century. Hystrix, the Italian Journal of Mammalogy 24: 7–14.
Alabia, I. D., S. I. Saitoh, H. Igarashi, Y. Ishikawa & Y. Imamura, 2020. Spatial habitat shifts of oceanic cephalopod (Ommastrephes bartramii) in oscillating climate. Remote Sensing 12(3): 521.
Argüelles, J., R. Tafur, A. Taipe, P. Villegas, F. Keyl, N. Dominguez & M. Salazar, 2008. Size increment of jumbo flying squid Dosidicus gigas mature females in Peruvian waters, 1989–2004. Progress in Oceanography 79(2–4): 308–312.
Arkhipkin, A., J. Argüelles, Z. Shcherbich & C. Yamashiro, 2015a. Ambient temperature influences adult size and life span in jumbo squid (Dosidicus gigas). Canadian Journal of Fisheries and Aquatic Sciences 72(3): 400–409.
Arkhipkin, A. I., P. G. K. Rodhouse, G. J. Pierce, W. Sauer, M. Sakai, L. Allcock, J. Arguelles, J. R. Bower, G. Castillo, L. Ceriola, C. S. Chen, X. Chen, M. Diaz-Santana, N. Downey, A. F. González, J. G. Amores, C. P. Green, A. Guerra, L. C. Hendrickson, C. Ibáñez, K. Ito, P. Jereb, Y. Kato, O. N. Katugin, M. Kawano, H. Kidokoro, V. V. Kulik, V. V. Laptikhovsky, M. R. Lipinski, B. Liu, L. Mariátegui, W. Marin, A. Medina, K. Miki, K. Miyahara, N. Moltschaniwskyj, H. Moustahfid, J. Nabhitabhata, N. Nanjo, C. M. Nigmatullin, T. Ohtani, G. Pecl, J. A. A. Perez, U. Piatkowski, P. Saikliang, C. A. Salinas-Zavala, M. Steer, Y. Tian, Y. Ueta, D. Vijai, T. Wakabayashi, T. Yamaguchi, C. Yamashiro, N. Yamashita & L. D. Zeidberg, 2015b. World squid fisheries. Reviews in Fisheries Science & Aquaculture 23(2): 92–252.
Bolstad, K. S., 2006. Sexual dimorphism in the beaks of Moroteuthis ingens Smith, 1881 (Cephalopoda: Oegopsida: Onychoteuthidae). New Zealand Journal of Zoology 33: 317–327.
Bookstein, F. L., 1998. A hundred years of morphometrics. Acta Zoologica Academiae Scientarium Hungaricae 44: 7–59.
Bower, J. R. & T. Ichii, 2005. The red flying squid (Ommastrephes bartramii): a review of recent research and the fishery in Japan. Fisheries Research 76: 39–55.
Chen, X. J., B. L. Liu & Y. Chen, 2008. A review of the development of Chinese distant-water squid jigging fisheries. Fisheries Research 89: 211–221.
Chen, C. S., 2010. Abundance trends of two neon flying squid (Ommastrephes bartramii) stocks in the North Pacific. ICES. Journal of Marine Science 67: 1336–1345.
Chen, X. J., H. J. Lu, B. L. Liu, Y. Chen, S. L. Li & M. Jin, 2012. Species identification of Ommastrephes bartramii, Dosidicus gigas, Sthenoteuthis oualaniensis and Illex argentinus (Ommastrephidae) using beak morphological variables. Scientia Marina 76(3): 473–481.
Collyer, M. L., D. J. Sekora & D. C. Adams, 2015. A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 115(4): 357–365.
Crespi-Abril, A. C., E. M. Morsan & P. J. Barón, 2010. Analysis of the ontogenetic variation in body and beak shape of the Illex argentinus inner shelf spawning groups by geometric morphometrics. Journal of the Marine Biological Association of the United Kingdom 90(3): 547–553.
Deser, C., M. A. Alexander, S. P. Xie & A. S. Phillips, 2010. Sea surface temperature variability: Patterns and mechanisms. Annual Review of Marine Science 2: 115–143.
Dryden, I. L. & K. V. Mardia, 1998. Statistical shape analysis. Wiley, West Sussex.
Fang, Z., B. Liu, J. Li, H. Su & X. Chen, 2014. Stock identification of neon flying squid (Ommastrephes bartramii) in the North Pacific Ocean on the basis of beak and statolith morphology. Scientia Marina 78(2): 239–248.
Fang, Z., L. Xu, X. Chen, B. Liu, J. Li & Y. Chen, 2015. Beak growth pattern of purpleback flying squid Sthenoteuthis oualaniensis in the eastern tropical Pacific equatorial waters. Fisheries Science 81(3): 443–452.
Fang, Z., B. Liu, X. Chen, Y. Jin, J. Li & Y. Chen, 2016a. Sexual asynchrony in the development of beak pigmentation for the neon flying squid Ommastrephes bartramii in the North Pacific Ocean. Fisheries Science 82(5): 737–746.
Fang, Z., J. Li, K. Thompson, F. Hu, X. Chen, B. Liu & Y. Chen, 2016b. Age, growth, and population structure of the red flying squid (Ommastrephes bartramii) in the North Pacific Ocean, determined from beak microstructure. Fishery Bulletin 114(1): 34–44.
Fang, Z., X. Chen, H. Su, K. Thompson & Y. Chen, 2017. Evaluation of stock variation and sexual dimorphism of beak shape of neon flying squid, Ommastrephes bartramii, based on geometric morphometrics. Hydrobiologia 784(1): 367–380.
Fang, Z., J. Fan, X. Chen & Y. Chen, 2018. Beak identification of four dominant octopus species in the East China Sea based on traditional measurements and geometric morphometrics. Fisheries Science 84(6): 975–985.
Fang, Z., X. J. Chen, J. Y. Qu, N. Li & J. H. Li, 2020. Annual variation of beak morphology and growth modals for neon flying squid (Ommastrephes bartramii) in north Pacific Ocean. Journal of Shanghai Ocean University 29(1): 109–120.
Frawley, T. H., D. K. Briscoe, P. C. Daniel, G. L. Britten, L. B. Crowder, C. J. Robinson & W. F. Gilly, 2019. Impacts of a shift to a warm-water regime in the Gulf of California on jumbo squid (Dosidicus gigas). ICES Journal of Marine Science 76(7): 2413–2426.
Gunz, P. & P. Mitteroecker, 2013. Semilandmarks: a method for quantifying curves and surfaces. Hystrix, the Italian Journal of Mammalogy 24(1): 103–109.
GroÈger, J., U. Piatkowski & H. Heinemann, 2000. Beak length analysis of the Southern Ocean squid Psychroteuthis glacialis (Cephalopoda: Psychroteuthidae) and its use for size and biomass estimation. Polar Biology 23(1): 70–74.
Hu, G., W. Yu, B. Li, D. Han, X. Chen, Y. Chen & J. Li, 2019. Impacts of El Niño on the somatic condition of Humboldt squid based on the beak morphology. Journal of Oceanology and Limnology 37(4): 1440–1448.
Igarashi, H., T. Ichii, M. Sakai, Y. Ishikawa, T. Toyoda, S. Masuda, N. Sugiura, K. Mahapatra & T. Awaji, 2017. Possible link between interannual variation of neon flying squid (Ommastrephes bartramii) abundance in the North Pacific and the climate phase shift in 1998/1999. Progress in oceanography 150: 20–34.
Jackson, G. D. & J. F. McKinnon, 1996. Beak length analysis of arrow squid Nototodarus sloanii (Cephalopoda: Ommastrephidae) in southern New Zealand waters. Polar Biology 16(3): 227–230.
Jackson, G. D., N. G. Buxton & M. J. George, 1997. Beak length analysis of Moroteuthis ingens (Cephalopoda: Onychoteuthidae) from the Falkland Islands region of the Patagonian shelf. Journal of the Marine Biological Association of the United Kingdom 77(4): 1235–1238.
Jereb, P. & C. F. E. Roper, 2010. Cephalopods of the world: An annotated and illustrated catalogue of cephalopod species known to date, Vol. 2. Myopsid and Oegopsid Squids, FAO Species Catalogue for Fishery Purposes, Rome: 269.
Ji, F., X. Guo, Y. Wang & K. Takayama, 2020. Response of the Japanese flying squid (Todarodes pacificus) in the Japan Sea to future climate warming scenarios. Climatic Change 159: 601–618.
Jones, J. B., G. J. Pierce, F. Saborido-Rey, P. Brickle, F. C. Kuepper, Z. N. Shcherbich & A. I. Arkhipkin, 2019. Size-dependent change in body shape and its possible ecological role in the Patagonian squid (Doryteuthis gahi) in the Southwest Atlantic. Marine Biology 166(5): 54.
Kelly, C. D., K. E. Folinsbee, D. C. Adams & M. D. Jennions, 2013. Intraspecific sexual size and shape dimorphism in an Australian freshwater fish differs with respect to a biogeographic barrier and latitude. Evolutionary Biology 40: 408–419.
Keyl, F., J. U. A. N. Argüelles, L. Mariátegui, R. Tafur, M. Wolff & C. Yamashiro, 2008. A hypothesis on range expansion and spatio-temporal shifts in size-at-maturity of jumbo squid (Dosidicus gigas) in the Eastern Pacific Ocean. CalCOFI Report 49: 119–128.
Keyl, F., J. Argüelles & R. Tafur, 2011. Interannual variability in size structure, age, and growth of jumbo squid (Dosidicus gigas) assessed by modal progression analysis. ICES Journal of Marine Science 68(3): 507–518.
Klingenberg, C. P., 2016. Size, shape, and form: concepts of allometry in geometric morphometrics. Development Genes and Evolution 226(3): 113–137.
Kim, Y. H., H. K. Jung & C. I. Lee, 2018. Changes in the Spawning Ground Environment of the Common Squid, Todarodes pacificus due to Climate Change. Ocean and Polar Research 40(3): 127–143.
Lefkaditou, E. & P. Bekas, 2004. Analysis of beak morphometry of the horned octopus Eledone cirrhosa (Cephalopoda: Octopoda) in the Thracian Sea (NE Mediterranean). Mediterranean Marine Science 5(1): 143–150.
Lipiński, M. R. & L. G. Underhill, 1995. Sexual maturation in squid: quantum or continuum? South African Journal of Marine Science 15(1): 207–223.
Liu, B. L., Z. Fang, X. J. Chen & Y. Chen, 2015. Spatial variations in beak structure to identify potentially geographic populations of Dosidicus gigas in the Eastern Pacific Ocean. Fisheries Research 164: 185–192.
Mantua, N. J., S. R. Hare, Y. Zhang, J. M. Wallace & R. C. Francis, 1997. A Pacific interdecadal climate oscillation with impacts on salmon production. Bulletin of the American Meteorological Society 78(6): 1069–1080.
Markaida, U., C. Quiñónez-Velázquez & O. Sosa-Nishizaki, 2004. Age, growth and maturation of jumbo squid Dosidicus gigas (Cephalopoda:Ommastrephidae) from the Gulf of California, Mexico. Fisheries Research 66(1): 31–47.
Martínez, P., A. Sanjuan & A. Guerra, 2002. Identification of Illex coindetii, I. illecebrosus and I. argentinus (Cephalopoda: Ommastrephidae) throughout the Atlantic Ocean; by body and beak characters. Marine Biology 141(1): 131–143.
Matias, R. S., S. Gregory, F. R. Ceia, A. Baeta, J. Seco, M. S. Rocha, E. M. Fernandes, R. L. Reis, T. H. Silva, E. Pereir, U. Piatkowski, J. A. Ramos & J. C. Xavier, 2019. Show your beaks and we tell you what you eat: Different ecology in sympatric Antarctic benthic octopods under a climate change context. Marine Environmental Research 150: 104757.
Mitteroecker, P., P. Gunz, S. Windhager & K. Schaefer, 2013. A brief review of shape, form, and allometry in geometric morphometrics, with applications to human facial morphology. Hystrix, the Italian Journal of Mammalogy 24(1): 59–66.
Neige, P. & J. L. Dommergues, 2002. Disparity of beaks and statoliths of some coleoids a morphometric approach to depict shape differentiation. Gabhandlungen Der Geologischen. Bundesanstalt 57: 393–399.
O’Dor, R. K., 1998. Chapter 11. Squid life-history strategies. In Rodhouse, P. D., E. G. Dawe & R. K. O’Dor (eds), Squid recruitment dynamic. FAO, Rome, Italy: 233–254.
Pecl, G. T., N. A. Moltschaniwskyj, S. R. Tracey & A. R. Jordan, 2004. Inter-annual plasticity of squid life history and population structure: ecological and management implications. Oecologia 139(4): 515–524.
Portner, E. J., U. Markaida, C. J. Robinson & W. F. Gilly, 2020. Trophic ecology of Humboldt squid, Dosidicus gigas, in conjunction with body size and climatic variability in the Gulf of California, Mexico. Limnology and Oceanography 65(4): 732–748.
Rohlf, F. J. & D. Slice, 1990. Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Biology 39(1): 40–59.
Takahara, H., H. Kidokoro & Y. Sakurai, 2017. High temperatures may halve the lifespan of the Japanese flying squid, Todarodes pacificus. Journal of Natural History 51(43–44): 2607–2614.
Villanueva, R., V. Perricone & G. Fiorito, 2017. Cephalopods as predators: a short journey among behavioral flexibilities, adaptions, and feeding habits. Frontiers in Physiology 8: 598.
Viscosi, V. & A. Cardini, 2011. Leaf morphology, taxonomy and geometric morphometrics: a simplified protocol for beginners. PLoS ONE 6: e25630.
Watanabe, H., T. Kubodera, T. Ichii & S. Kawahara, 2004. Feeding habits of neon flying squid Ommastrephes bartramii in the transitional region of the central North Pacific. Marine Ecology Progress Series 266: 173–184.
Watanabe, H., T. Kubodera, T. Ichii, M. Sakai, M. Moku & M. Seitou, 2008. Diet and sexual maturation of the neon flying squid Ommastrephes bartramii during autumn and spring in the Kuroshio-Oyashio transition region. Journal of the Marine Biological Association of the United Kingdom 88(2): 381–389.
Yu, W., X. J. Chen, C. Chen & Y. Zhang, 2017. Impacts of oceanographic factors on interannual variability of the winter-spring cohort of neon flying squid abundance in the Northwest Pacific Ocean. Acta Oceanologica Sinica 36(10): 48–59.
Yu, W., Y. Zhang, X. J. Chen, Q. Yi & W. Qian, 2018. Response of winter cohort abundance of Japanese common squid Todarodes pacificus to the ENSO events. Acta Oceanologica Sinica 37(6): 61–71.
Yu, W., X. J. Chen & Y. Zhang, 2019a. Seasonal habitat patterns of jumbo flying squid Dosidicus gigas off Peruvian waters. Journal of Marine Systems 194: 41–51.
Yu, W., X. J. Chen, Y. Zhang & Q. Yi, 2019b. Habitat suitability modelling revealing environmental-driven abundance variability and geographical distribution shift of winter–spring cohort of neon flying squid Ommastrephes bartramii in the northwest Pacific Ocean. ICES Journal of Marine Science 76(6): 1722–1735.
The support from the caption and crews in commercial jigging vessels in scientific surveys is gratefully acknowledged. This work was funded by the National Key R&D Program of China (2019YFD0901404), National Science Foundation of China (41876141) and Fund of Key Laboratory of Open-Sea Fishery Development, Ministry of Agriculture, P. R. China (LOF 2018-02).
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling editor: Iacopo Bertocci
Below is the link to the electronic supplementary material.
About this article
Cite this article
Fang, Z., Han, P., Wang, Y. et al. Interannual variability of body size and beak morphology of the squid Ommastrephes bartramii in the North Pacific Ocean in the context of climate change. Hydrobiologia (2021). https://doi.org/10.1007/s10750-021-04528-7
- Body size
- Morphological variation
- Climate change
- Ommastrephes bartramii
- Geometric morphometrics