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Beak growth pattern of purpleback flying oualaniensis in the eastern tropical Pacific equatorial waters

Article in Fisheries Science · March 2015 DOI: 10.1007/s12562-015-0857-8

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Zhou Fang Xinjun Chen Shanghai Ocean University Shanghai Ocean University

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ORIGINAL ARTICLE Biology

Beak growth pattern of purpleback flying squid Sthenoteuthis oualaniensis in the eastern tropical Pacific equatorial waters

Zhou Fang · Luoliang Xu · Xinjun Chen · Bilin Liu · Jianhua Li · Yong Chen

Received: 29 August 2014 / Accepted: 13 December 2014 © Japanese Society of Fisheries Science 2015

Abstract beaks maintain a stable morphol- length, and lower lateral wall length, which showed lin- ogy, implying that they can be used to explore ecological ear relationships with ML. The relationships between BW influences on squid life history. Understanding the beak and the six beak variables were best fitted with power growth pattern can help us to improve knowledge of the functions, and these functions can be used to estimate trophic characteristics of and to estimate squid squid biomass from beak variable values. All of the beak biomass. Sthenoteuthis oualaniensis is widely distrib- morphological variables varied according to the maturity uted in eastern tropical Pacific equatorial waters and has stage of the squid. Results of a post hoc comparison sug- been caught commercially by Chinese squid jigging fleets gested that the values of beak morphological variables for since 2011. In this study, we randomly took 220 samples immature squids (maturity stages I and II) showed signifi- of S. oualaniensis with lengths (ML) of between cant differences from the corresponding values for mature 119 and 351 mm and body weights (BW) of between 45 squids (maturity stages III–V). These differences may and 1975 g and measured six beak morphological vari- result from changes in diet that occur during maturation, ables for each sampled squid. The relationships between which affect the relevant mandibular muscle strength. The ML and all of the beak variables were power functions, most common pigmentation stages (PS) encountered were except for upper lateral wall length (ULWL), upper crest II–V. The relationships of PS to ULWL and lower wing length were best described by exponential functions. Beak morphology and pigmentation of S. oualaniensis tended Z. Fang · L. Xu · X. Chen · B. Liu · J. Li College of Marine Sciences, Shanghai Ocean University, to change markedly with ontogenetic stage. It is easy to Hucheng Ring Road 999, Lingang New City, 201306 Shanghai, separate mature and immature squids based on their PS. China This study provides important biological information on S. oualaniensis. Z. Fang · L. Xu · X. Chen (*) · B. Liu · J. Li · Y. Chen Collaborative Innovation Center for Distant-Water Fisheries, 201306 Shanghai, China Keywords Sthenoteuthis oualaniensis · Beak · e-mail: [email protected] Morphology · Growth pattern · Pigmentation · Eastern Tropical Pacific X. Chen · B. Liu · J. Li The Key Laboratory of Shanghai Education Commission for Oceanic Fisheries Resources Exploitation, 999 Hucheng Ring Road, 201306 Shanghai, China Introduction

X. Chen · B. Liu · J. Li The Key Laboratory of Sustainable Exploitation of Oceanic The purpleback flying squid Sthenoteuthis oualaniensis is Fisheries Resources, Ministry of Education, 999 Hucheng Ring an oceanic that belongs to the Ommastre- Road, 201306 Shanghai, China phidae and is distributed in a broad band around the equa- tor from approximately 40°N to 40°S. Its range stretches Y. Chen School of Marine Sciences, University of Maine, Orono, predominately throughout the tropical and subtropical open ME 04469, USA waters of the Indo-Pacific region [1, 2]. Purpleback flying

1 3 Fish Sci squid tend to be concentrated in areas of high primary pro- and growth patterns of squid [24–26]. Beak morphological ductivity, with a patchy distribution observed [3]. characteristics are more reliable than the other hard parts Within this wide distribution, S. oualaniensis is also of squid, as they are large enough to be measured with the known to have a wide ecological range and a complex naked eye and they do not break down in the stomachs of population structure [4]. This structure includes three predators [27, 28]. Beaks have been widely used in taxon- major forms of S. oualaniensis based on differences in omy to identify squid species to family, , and species size at maturity [5]: (1) a giant form, mantle length (ML) levels [29–31]. The relationships between beak morpho- 400–500 mm, which occurs only in the northern Indian logical variables and both ML and body weight (BW) have Ocean; (2) a medium form (120–250 mm ML) that occurs been quantified using various models, and these relation- throughout the range of the species; and (3) a dwarf form ships are thought to have the potential to be used for stock (90–120 mm ML) that occurs in equatorial waters. The biomass estimation [32–36]. medium and dwarf forms may also be subdivided into two As it is a feeding organ that tears and bites food, the minor forms on the basis of dorsal and features of different parts of the beak change with the morphology [5]. ontogenetic state of the squid [37]. Another unique char- The total biomass of this squid is thought to be rela- acteristic that has been documented in previous studies is tively high. Nigmatullin et al. [6] previously estimated the the development of darkness or pigmentation in the crest, total stock of S. oualaniensis in the world’s oceans to be lateral wall, or wing of the beak [38–42]. After Hernández- between 8 and 11 million tonnes. Zuev et al. [7] once esti- García [42] defined eight stages of beak pigmentation, the mated the mass of the total stock of S. oualaniensis at 3–4 pigmented part was shown to be related to the stiffness of million tonnes (1.9–2.4 million tonnes for the middle-sized the beak—the tanned parts of the beak are harder than the form) in the and 5–7 million tonnes in the untanned parts [43, 44]. The development of beak pigmen- Pacific Ocean. This robust species may form joint schools tation is a sign of growth and changes in the diet of the with the similar-sized species Dosidicus gigas and Ommas- squid [42]. trephes bartramii, which have overlapping distributions The objective of the study reported in the present paper [7]. was to use beak growth patterns to estimate the length– At the periphery of the geographical range of S. ouala- weight relationship, sexual maturity stage, and changes in niensis, they are often caught as bycatch by D. gigas and diet, which can be used to help study predator–prey rela- O. bartramii fisheries [2, 8, 9]. Historically, S. oualaniensis tionships involving S. oualaniensis in the tropical Pacific has been commercially fished off Okinawa (in the Ryukyu Ocean. Specifically, the length–weight relationship and Chain), Taiwan (a province of China), and by Japa- sexual maturity stage tend to be correlated with distinguish- nese fishing vessels [10]. In 2003, Chinese squid jigging able beak characteristics. Changes in diet were determined fleets began to targetS. oualaniensis in the Indian Ocean using variations in the beak pigmentation of S. oualanien- and landed 5000 t from the northwest Indian Ocean dur- sis. Relating beak characteristics to trophic interactions ing 2003–2005 [11]. In the Pacific Ocean, purpleback fly- permits convenient estimation of the biomass of S. ouala- ing squid are retained as bycatch by fisheries that predomi- niensis using beaks alone in research and nately target D. gigas [9, 12]. potentially in fisheries surveys. The growth rate of S. oualaniensis is relatively fast, like those of other oceanic squids; daily food intake is estimated to be about 8–10 % of their total body weight [13]. The Materials and methods broad feeding spectrum of S. oualaniensis will change as the mantle length increases [8, 14]. Amphipods, euphausi- All samples of S. oualaniensis were taken at random from ids, and fish larvae are the main food for juveniles, whereas the catch of the Chinese commercial jigging vessel Puy- adults feed primarily on myctophids and sometimes exhibit uan 802 from April to June 2014. The fishing vessel was cannibalistic behavior [15–17]. S. oualaniensis has been operated in the equatorial waters of the East Pacific Ocean commonly found in the stomachs of various predators such (2°N–5°S and 110°–118°W, Fig. 1). A total of 220 samples as seabirds, large fish, and marine mammals [18–21], and it were collected from this area, comprising 204 females and plays important role in the marine ecosystems of the Indian 16 males. All samples were measured and dissected imme- Ocean and the Pacific Ocean as both a predator and a prey diately after they were landed on deck. Mantle length (ML) species [8, 14, 17]. and body weight (BW) were measured to the nearest 1 mm Hard structures in , especially the beak, are and 1 g, respectively. Sex was identified and sexual matu- composites of proteins and chitin fibers [22, 23]. These rity stage was determined by the naked eye based on mor- structures have increasingly been studied in recent years phological changes in the gonads defined by Lipinski and to determine length–weight relationships, age estimates, Underhill [45]. For female squid, ML ranged from 132 to

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351 mm with a mean of 196.1 mm, and BW ranged ranged length (LLWL), and lower wing length (LWL) (Fig. 2). All from 60 to 1975 g with a mean of 320.2 g. For male squid, of the beak morphometrics are shown in Table 1. Seven ML ranged from 119 to 254 mm with a mean of 175.2 mm, pigmentation stages (PS) of the beak for female squid were and BW ranged from 45 to 665 g with a mean of 244.1 g. defined as described by Hernández-García [42] (Fig. 3). Beaks were extracted from the buccal cavity and cleaned Both sexes were combined to establish the relationship with 75 % ethyl alcohol before measurement. Twelve mor- between beak morphometrics and ML or BW. Six beak phometric variables of beaks were measured with vernier length variables (UHL, UCL, ULWL, LCL, LRL, and calipers to an accuracy of 0.1 mm following Clarke [46]. LLWL) were used to quantify beak morphology because These measurements included upper hood length (UHL), they can be measured precisely using calipers. These six upper crest length (UCL), upper rostrum length (URL), variables have also commonly been used in previous stud- upper rostrum width (URW), upper lateral wall length ies [33, 44]. We used the following functions to quantify (ULWL), upper wing length (UWL), lower hood length the relationships between beak morphological variables (LHL), lower crest length (LCL), lower rostrum length and squid body size [47]: (LRL), lower rostrum width (LRW), lower lateral wall Linear function: y = a + bx (1)

Power function: y = axb (2)

Exponential function: y = aebx (3)

Logarithmic function: y = a ln(x) + b, (4) where x is one of the six beak variables, y is ML or BW, and a and b are two parameters to be estimated. Akaike’s information criterion (AIC) was used to compare different models [48, 49]. The model that had the smallest value of AIC was selected as the best model [50, 51]. AIC was cal- culated with the following function: AIC = 2θ + n ln(SSQ/n), where θ is the number of estimated parameters, n is the number of observations, and SSQ is the sum of the squared differences between the observed and estimated data. Fig. 1 Sampling stations of Sthenoteuthis oualaniensis in the equato- To for differences in sexual maturity stages between rial waters of the tropical Pacific Ocean. The small rectangle shown males and females, all twelve beak morphological variables top left denotes the region of the Pacific Ocean from which the sam- ples were taken; triangles indicate the locations of sampling stations were analyzed using analysis of variance (ANOVA) and a within that region post hoc comparison (Tukey HSD) of all possible pair-wise

Fig. 2 Schematic diagram of beak morphometric variables: A upper hood length (UHL), B upper crest length (UCL), C upper rostrum length (URL), D upper rostrum width (URW), E upper lateral wall length (ULWL), F upper wing length (UWL), G lower hood length (LHL), H lower crest length (LCL), I lower rostrum length (LRL), J lower rostrum width (LRW), K lower lateral wall length (LLWL), L lower wing length (LWL)

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Table 1 Data on beak Beak variable Female (mm) Male (mm) morphological variables for Sthenoteuthis oualaniensis Minimum Maximum Mean SD Minimum Maximum Mean SD ± ± UHL 10.38 26.31 15.10 2.68 9.23 19.25 13.21 3.33 ± ± UCL 13.09 34.29 19.43 3.47 12.42 25.91 17.25 4.40 ± ± URL 3.01 10.04 5.10 1.10 3.00 6.79 4.48 1.20 ± ± URW 2.14 6.09 3.67 0.76 2.30 4.64 3.15 0.70 UHL upper hood length, UCL ± ± ULWL 8.73 25.86 14.27 2.75 9.63 18.29 12.68 2.91 upper crest length, URL upper ± ± UWL 3.07 8.10 4.87 0.90 2.74 6.34 4.15 1.16 rostrum length, URW upper ± ± rostrum width, ULWL upper LHL 3.20 7.78 4.52 0.71 3.03 5.90 3.85 0.87 ± ± lateral wall length, UWL upper LCL 6.01 15.47 9.02 1.63 5.60 11.78 7.87 2.09 wing length, LHL lower hood ± ± LRL 2.66 7.84 4.54 0.92 2.61 6.16 4.04 1.06 length, LCL lower crest length, ± ± LRL lower rostrum length, LRW LRW 2.24 6.51 3.77 0.76 2.22 5.58 3.35 0.88 ± ± lower rostrum width, LLWL LLWL 7.75 24.16 13.51 2.43 8.37 17.58 11.86 3.05 ± ± lower lateral wall length, LWL LWL 4.38 13.15 7.18 1.33 3.92 9.74 5.97 1.58 lower wing length ± ±

and three beak morphological variables: UHL, UCL, and LRL (Table 2; Fig. 4a, b, d). The relationships between ML and the beak morphological variables ULWL, LCL, and LLWL were accurately described by linear functions (Table 2; Fig. 4b, c). Power functions were also the best- fitting models for the relationships between BW and the six beak morphological variables (Table 2; Fig. 4e–h).

Impact of sexual maturity on beak variables

Sexual maturity stages differed between samples of males and females. For males, 18.75 % were in the immature stages (I–II) and 81.25 % were in the mature stages (III– IV). For females, 36.76 % were in the immature stages (I–II) and 63.24 % were in the mature stages (III–IV). For a given size, males were more likely to be mature than females. The means and standard deviations of beak varia- bles at different sexual maturity stages are shown in Fig. 5. Fig. 3 Pigmentation changes with growth in cephalopod beaks. The All of the beak morphometrics showed significant differ- numbers shown are the pigmentation stages (PS) [cited from Hernán- dez-García [42], based on beaks with LRL values (mm) of 2.16, 2.52, ences among different sexual maturity stages (Table 3). 3.83, 3.31, 4.09, 4.50, 5.60, and 6.80 for 1–7, respectively] According to post hoc analysis, five variables (UCL, LCL, URW, UWL, and LWL) presented different growth patterns between immature (maturity stages I and II) and mature means. The relationships between pigmentation stage (PS) (maturity stages III–V) stages (Fig. 5). and each of the six beak variables were evaluated and com- pared. All of the above statistical analysis was conducted Relationships between beak pigmentation stage using SPSS 17.0. and morphological variables

Because of possible sexual dimorphism and the small Results sample size for males, we excluded male samples from the analysis. Of the 204 available female beaks, 188 Model selection for beak length versus ML and BW beaks could be used to determine PS. PS 2–5 accounted for 84.0 % of all samples. The other beak samples corre- The best models, based on the evaluation of AIC values, sponded to PS 1, 6, and 7; none of the beaks corresponded were power functions for the relationships between ML to PS 0. The dominate PSs at maturity stages I and II were

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Table 2 Estimated parameters Beak variable Model Mantle length (ML) Body weight (BW) and AIC values for models describing the relationships a b AIC a b AIC between squid body-size variables (mantle length ML, UHL body weight BW) and beak Linear 0.069 1.599 206.473 0.011 11.521 79.333 morphological variables for − Power 0.134 0.896 207.197 3.239 0.273 90.016 Sthenoteuthis oualaniensis − − Exponential 6.496 0.004 142.105 12.653 0.001 184.725 − Logarithm 13.554 56.196 160.941 4.108 7.797 53.253 − − − − UCL Linear 0.089 1.919 117.606 0.014 14.735 155.529 − Power 0.163 0.906 113.833 4.077 0.277 1.969 − Exponential 8.279 0.004 78.215 16.238 0.001 277.028 − Logarithm 17.505 72.632 32.934 5.312 10.161 63.685 − − − ULWL Linear 0.068 0.932 97.476 0.011 10.667 68.319 − Power 0.100 0.940 95.883 2.797 0.289 45.994 − − Exponential 5.898 0.004 78.791 11.856 0.001 180.715 − Logarithm 13.323 55.794 43.755 4.062 8.352 6.809 − − − LCL Linear 0.041 0.907 303.928 0.007 6.876 92.669 − − Power 0.078 0.899 305.079 1.920 0.275 230.198 UHL upper hood length, UCL − − Exponential 3.883 0.004 258.181 7.559 0.001 3.003 upper crest length, ULWL upper − − lateral wall length, LCL lower Logarithm 8.149 33.848 282.471 2.468 4.739 205.725 − − − − crest length, LRL lower rostrum LRL length, LLWL lower lateral Linear 0.022 0.242 431.133 0.003 3.414 296.654 wall length; AIC Akaike’s − − Power 0.031 0.943 431.607 0.899 0.288 382.131 information criterion, Linear − − linear function: y a bx, Exponential 1.884 0.004 403.082 3.790 0.001 225.501 = + b − − Power power function: y ax , Logarithm 4.332 18.238 422.240 1.304 2.723 367.528 Exponential exponential = − − − − function: y aebx, Logarithmic LLWL logarithmic= function: y a Linear 0.061 1.474 135.496 0.010 10.266 40.473 = − ln(x) b. Power 0.121 0.894 134.597 2.866 0.275 87.177 + − − Underlined values are the Exponential 5.819 0.004 106.995 11.290 0.001 141.493 − lowest AIC values, which Logarithm 12.051 49.882 98.327 3.676 6.980 46.824 correspond to the best models − − − −

PS 2 and 3, accounting for 90.5 and 82.3 % of the samples, study were within the range described by Nesis [5], which respectively. At maturity stages III and IV, the dominant is thought to be the full range for adult S. oualaniensis. PSs were 4 and 5, accounting for 83.7 and 75.7 % of the The precision of the estimated models in our study could samples, respectively. PSs 5–7 were dominant for stage V, be a result of the full range of adult samples we investi- and accounted for 89.6 % of all samples. The most obvi- gated. The estimated models describing the relationships ous changes in pigmentation in beak parts occurred in the between beak variables and ML and BW were devel- lateral wall in the upper beak and the wing in the lower oped using a combined data set including both males and beak, suggesting relationships of PS to ULWL and LWL, females. However, S. oualanienesis exhibits a potential respectively. Exponential curves best described these two sexual dimorphism in the medium form, as seen in our relationships (Fig. 6). study, even though the sample size for males in our study was pretty small (Table 1). Sexual dimorphism is common in other cephalopods, with differences in body size (ML Discussion and BW) and beak variables observed [33, 52, 53]. We did not include male squid in our analysis as S. oualaniensis Nesis [5] described the ML of mature medium-form S. may present different growth rates for males and females, oualanienesis as ranging from 120 to 150 mm for males with the fishery targeting the larger squid in our study area. and from 190 to 250 mm for females. The samples in our Future studies on S. oualaniensis need to investigate the

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(e) (a) 30 30 0.273 UHL = 0.134ML 0.896 UHL = 3.239BW R² = 0.947 R² = 0.909 25 25

20 20

15 15 UHL / mm UHL / mm

10 10

5 5 100 150 200 250 300 350 400 0 200 400 600 800 1000 1200 1400 ML / mm BW / g (b) 40 UCL = 0.089ML + 1.919 (f) 40 UCLLCL UCL LCL UCL = 4.077BW0.277 35 R² = 0.956 35 R² = 0.915 30 30 25 25 20 20 CL / mm 15 CL / mm 15 10 LCL = 0.078ML 0.899 10 LCL = 1.920BW 0.275 5 R² = 0.911 5 R² = 0.871 0 0 100 150 200 250 300 350 400 0 200 400 600 800 1000 1200 1400 ML / mm BW / g

(c) 30 (g) 30 ULWL LLWL ULWL = 0.068ML + 0.932 ULWL LLWL ULWL = 2.797BW 0.289 R² = 0.920 25 25 R² = 0.8861

20 20

15 15 LLWL = 0.061ML + 1.474 0.275 LWL / mm LLWL = 2.866BW

LWL / mm 10 10 R² = 0.917 R² = 0.881 5 5

0 0 100 150 200 250 300 350 400 0 200 400 600 800 1000 1200 1400 ML / mm BW / g

(d) 9 (h) 9 LRL = 0.031ML 0.943 LRL = 0.899BW0.288 8 8 R² = 0.835 R² = 0.787 7 7 6 6 5 5 4 4 LRL / mm LRL / mm 3 3 2 2 1 1 0 0 100 150 200 250 300 350 400 0 200 400 600 800 1000 1200 1400 ML / mm BW / g

Fig. 4 Relationships between the mantle length (ML) of Stheno- relationships between body weight (BW) and e UHL, f UCL and teuthis oualaniensis and six beak morphological variables: a UHL, LCL, g ULWL and LLWL, and h LRL. The solid and dotted lines b UCL and LCL, c ULWL and LLWL, d LRL. Also shown are the represent the curves of the upper beak and lower beak, respectively sexual differences in the relationships between beak vari- twelve beak variables and ML were linear, as also noted in ables and body size (ML and BW). other studies of cephalopods [32, 47, 52, 53]. A linear rela- Not all beak morphological variables showed isometric tionship suggests synchrony between the growth in ML and growth with the ML (Fig. 4a–d). Allometric growth patterns increases in beak variables. The present study found that are common for squid beaks [37]. Beaks of argentinus power functions best describe the relationships between have different growth patterns between the hood, crest, and the six beak variables and BW (Fig. 4e–h). Liu and Chen rostrum [32, 47]. This may be caused by pivoting due to the [47] also observed the same relationships between BW biting force, as driven by the mandibular muscles, which and beak variables for S. oualaniensis in the Northwest leads to different growth rates in different parts of the beak Indian Ocean. The relationship between beak size and BW [54, 55]. However, most of the relationships between the yields more accurate estimates of squid biomass than the

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Fig. 5 Mean and standard deviation values of beak variables during different sexual maturity stages. The results of post hoc tests are shown by subscript letters (upper beak) and numbers (lower beak): different letters or numbers indicate significant differences relationship between beak size and ML [37, 56]. Because changes observed (Fig. 5). The differences in the values of of the limited range of MLs encountered in this study, all beak variables between mature and immature samples may of the models developed here should only be used for the be related to changes in diet during the growth of the repro- range of sizes included in this study. ductive system [47]. The superior and inferior mandibular Beak morphology is also correlated with gonad matu- muscles, which are located between the hood and the wing, rity. Differences in beak variables occurred at different control the movement of the beak during opening and bit- sexual maturity stages, suggesting that beak morphology ing [54]. These muscles strengthen with the change in diet, undergoes distinct changes upon moving from immature which may influence hood and wing growth indirectly. stages to mature stages (Table 3). These changes are also Other members of the have also demon- shown in Fig. 5. Values for the beak variables for imma- strated this characteristic [57]. ture squid (stages I and II) were significantly different from Pigmentation of the beak is an adaptation that results those for the mature squid (stages III–V). However, the val- in beak hardening, allowing the consumption of larger ues for maturity stages I and II were not significantly dif- prey items [42, 43]. Schetinnikov [16] reported that the ferent from each other; neither were those for stages IV and main prey of small S. oualaniensis (ML 40–100 mm) are V (Fig. 5). CL (crest length) and WL (wing length) grew crustaceans and fish larvae. Medium-sized squid (ML faster during stage III, during which the squid are transi- 100–150 mm) rely much less on crustaceans as prey. tioning from immature to mature, with small morphological Myctophids dominate the diet of S. oualaniensis beyond

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Table 3 Results of ANOVA for beak morphological variables of the beak to increase while still permitting flexible move- Sthenoteuthis oualaniensis at different sexual maturity stages ment [42, 55]. Beak pigmentation increases beak stiffness Beak variable Sum of squares F value Significance through high-density catechol–histidine crosslinking and dehydration [43, 44]. The crosslinking and dehydration UHL 784.770 46.768 P < 0.001 make the beak harder and less vulnerable, as shown in UCL 1358.622 49.779 P < 0.001 tensile and nanoindentation tests [22]. The stiff part of the URL 109.042 34.682 P < 0.001 beak (the tip) therefore strengthens the biting action. This URW 60.053 46.255 P < 0.001 adaptation is not uncommon in the marine environment; ULWL 791.019 46.534 P < 0.001 other marine animals also use pigmentation to harden their UWL 73.430 32.488 P < 0.001 beaks (e.g., Nereis spp., Lichtenegger et al. [58]; Glycera LHL 39.185 25.462 P < 0.001 spp., Wait et al. [59]). Cephalopods experience exponential LCL 288.410 45.229 P < 0.001 growth during maturation, during which time the pigmenta- LRL 84.669 42.216 P < 0.001 tion process proceeds rapidly too [41]. In our study, ULWL LRW 46.339 29.267 P < 0.001 and LWL showed rapid rates of pigmentation at maturation. LLWL 620.408 43.325 P < 0.001 In summary, power functions were found to fit best to LWL 181.812 36.873 P < 0.001 the relationships between ML and the beak morphological variables UHL, LCL, and LRL, whereas linear functions UHL upper hood length, UCL upper crest length, URL upper rostrum length, URW upper rostrum width, ULWL upper lateral wall length, were the best fit to the relationships between ML and the UWL upper wing length, LHL lower hood length, LCL lower crest beak variables ULWL, UCL, and LLWL. The relationships length, LRL lower rostrum length, LRW lower rostrum width, LLWL between BW and six beak variables were best described by lower lateral wall length, LWL lower wing length power functions. Different beak parts differ in their growth patterns. Sexual maturity stage significantly influenced all (a) 30 beak morphological variables. Immature samples showed ULWL = 8.731e 0.119PS significant differences from mature samples based on the R² = 0.772 25 results of post hoc analysis (Tukey’s HSD), which may be

20 due to the change in diet that occurs upon maturation. The PS advances rapidly during beak growth. The pigmentation 15 process mainly occurs during the period when the squid ULWL / mm matures, because the dominant PS tended to be different at 10 each stage of maturity. 5 0 1234567Acknowledgements Support for the scientific survey from Puyuan Pigmentation degree 802 is gratefully acknowledged. We thank the two anonymous refer- ees and the Editor for their detailed, constructive, and helpful com- (b) 14 0.113PS ments. This work was funded by the National Science Foundation of LWL = 4.492e China (NSFC41306127 and NSFC41276156), the National Science 12 R² = 0.713 Foundation of Shanghai (13ZR1419700), the Innovation Program 10 of the Shanghai Municipal Education Commission (13YZ091), the 8 Funding Program for Outstanding Dissertations in Shanghai Ocean University, the Funding Scheme for Training Young Teachers in 6 Shanghai Colleges, and the Shanghai Leading Academic Discipline LWL / mm 4 Project (Fisheries Discipline). The involvement of Yong Chen was 2 supported by the SHOU International Center for Marine Studies and the Shanghai 1000 Talent Program. 0 0 1234567 Pigmentation degree References

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