Beak Measurements of Octopus (Octopus variabilis) in Jiaozhou Bay and Their Use in Size and Biomass Estimation

XUE Ying1), REN Yiping1), *, MENG Wenrong2), LI Long1), 3), MAO Xia1), HAN Dongyan1),and MA Qiuyun1)



Beak Measurements of Octopus () in Jiaozhou Bay and Their Use in Size and Biomass Estimation

XUE Ying, REN Yiping, MENG Wenrong, LI Long, MAO Xia, HAN Dongyan,and MA Qiuyun

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Cephalopods play key roles in global marine ecosystems as both predators and preys. Regressive estimation of original size and weight of cephalopod from beak measurements is a powerful tool of interrogating the feeding ecology of predators at higher trophic levels. In this study, regressive relationships among beak measurements and body length and weight were determined for an octopus species (), an important endemic cephalopod species in the northwest Pacific Ocean. A total of 193 individuals (63 males and 130 females) were collected at a monthly interval from Jiaozhou Bay , China. Regressive relationships among 6 beak measurements (upper hood length, UHL; upper crest length, UCL; lower hood length, LHL; lower crest length, LCL; and upper and lower beak weights) and mantle length (ML), total length (TL) and body weight (W) were determined. Results showed that the relationships between beak size and TL and beak size and ML were linearly regressive, while those between beak size and W fitted a power function model. LHL and UCL were the most useful measurements for estimating the size and biomass of. The relationships among beak measurements and body length (either ML or TL) were not significantly different between two sexes; while those among several beak measurements (UHL, LHL and LBW) and body weight (W) were sexually different. Since male individuals of this species have a slightly greater body weight distribution than female individuals, the body weight was not an appropriate measurement for estimating size and biomass, especially when the sex of individuals in the stomachs of predators was unknown. These relationships provided essential information for future use in size and biomass estimation of, as well as the estimation of predator/prey size ratios in the diet of top predators.

; Jiaozhou Bay; beak measurement; body size; hood length; crest length

1 Introduction

Cephalopods play key roles in global marine ecosystems both as predators and preys, particularly in the deep oceans of the world (Clarke 1996; Boyle and Rodhouse, 2005; Chen., 2009; Hunsicker., 2010). They are known to be an important food source for many predators at higher trophic levels, such as whales, seals, seabirds, tuna, sharks and other fishes (., Clarke, 1980; Dunning., 1993; Guerra., 1993; Croxall and Prince 1996; Chen., 2009; Daneri., 2012). They are also voracious predators of a wide variety of prey, including crustaceans, squid and juvenile fishes (Clarke, 1996; Hunsicker, 2009). Determining and quantifying their trophic role is therefore essential for understanding structure and function of marine ecosystems. In recent years, more and more research efforts have been focused on this sub-ject (Cherel and Hobson, 2005; Jackson., 2007; Christian and Friedemann, 2010; Xavier., 2011).

Most information of cephalopods are originated from analysis of stomach contents of their predators (Gröger., 2000; Jackson., 2007; Xavier., 2011), because direct sampling is difficult (Clarke, 1977; Xavier., 2007). Cephalopods have a few hard parts resisting digestion. For example, the paired beaks (chitinous mandibles) of cephalopods are extremely resistant to digestion, remaining in predator stomachs for a longer time (Smale., 1993;Gröger., 2000; Lu and Ickeringill, 2002). They are species-specific and particularly useful for providing information on the cephalopod species preyed upon (Gröger., 2000; Xavier., 2011). The original size and weight of cephalopods ingested by predators can be estimated with regression equations describing the relationship between beak measurements and prey size (Clarke 1986; Jackson., 1997; Gröger., 2000; Bowen 2000; Lu and Ickeringill, 2002; Liu and Chen, 2010; Potier., 2011; Chen., 2012). Reconstructed length and weight can provide valuable information of food intake, consumption rates, size spectra, prey/predator length ratios, as well as contribution by prey items, independently of the digestion state of preys (Potier., 2011; Chen., 2012). Since 1950s, much efforts have been dedicated to the development of methods which determine the original size of cephalopods based on beak measurements (., Akimushkin, 1955; Clarke, 1962, 1977, 1980, 1986; Wolff, 1984; Jackson., 1997; Lu and Ickeringill, 2002; Crespi-Abril., 2010; Xavier., 2007, 2011); however, the available relationships are still limited. The original sizes are often estimated with equations established for closely related species or species with a similar morphology (Potier., 2011; Xavier., 2011). Therefore, it is increasingly necessary to determine the allometric relationships between beak size and original length and weight of cephalopod species (Jackson., 2007).

is one of the most abundant octopus species distributed in the northwest Pacific Ocean: China, Korea and Japan (Roper., 1984; Chen., 2009). This species is one of the three species reported in Chinese octopus catch and also important for Japanese fishery off Honshu (Roper., 1984). This octopus often lives in the shallow calm water with muddy bottom, burrowing a deep tunnel in which it hides itself, especially in the breeding season (Yamamoto, 1942; Chen., 2009).plays an important role in the marine ecosystem and food webs, being an important prey for various top predators such as sharks, eels and other carnivorous fishes (Wei and Jiang, 1992; Zhang., 2007; Xue., 2008; Jin., 2010). The morphological characters, biology and distribution ofhave been described by several authors (., Yamamoto, 1942; Dong, 1988; Chen., 2009). However, there is currently no published report of regressive relationships between beak measurements and body size for, despite it is highly profiled in marine food webs.

In this study, the relationships between body size and beak measurements were determined for. The aim of this study was to establish stochastic regressions for mantle length, total length and body weight offrom measurements of both upper and lower beaks. One of the principal applications will be the estimation of the original size and biomass ofbased on these measurements of beaks extracted from stomachs of predators at higher trophic levels.

2 Materials and Methods

2.1 Sample Collection and Processing

Specimens ofwere collected monthly by bottom trawl surveys in Jiaozhou Bay from Sep. 2008 to Aug. 2009. After capture, all specimens were immediately placed on ice and subsequently frozen for later analysis. A total of 193 individuals (63 males and 130 females) ofwere analyzed in this study.

After being defrosted in laboratory, total length (TL in mm), mantle length (ML in mm) and body weight (W in g) were recorded for each individual. TL was measured from the tip of the longest arm to the end of the mantle, and ML was from the tip of the mantle to the midpoint between the eyes (Dong, 1988; Lalas, 2009). Lengths were recorded to the nearest 1mm, and body weights were measured using an electronic balancer with an accuracy of 0.01g. Body weight was measured on intact specimens and any individual with missing arms was excluded from further analysis. Specimens ofwere separated into two sexual groups externally according to the presence or absence of the hectocotylised arm (Dong, 1988; Chen., 2009).

2.2 Beak Measurements

The beaks were extracted carefully from the buccal mass ofand cleaned with water to remove the surrounding tissue and membrane. The methods for extraction of beaks and terminology for beak measure- ments were from Clarke (1986). Four measurements were taken for each pair of beaks as defined by Clarke (1986) and Lalas (2009), which included upper hood length (UHL) and upper crest length (UCL) for the upper beak, and lower hood length (LHL) and lower crest length (LCL) for the lower beak (Fig.1). Beak dimensions, accurate to 0.1mm, were measured using digital calipers or an ocular micrometer. Additionally, upper and lower beak weight (UBW, LBW) were also measured using the precision electronic balancer with an accuracy of 0.01mg. These measurements were chosen because they are easy to measure and can be compared with previous works and across species (Lu and Ickeringill, 2002).

Fig.1 Profiles (left) and top views (right) of the upper beak (top) and lower beak (bottom) of Octopus variabilis showing beak measurements. UHL, upper hood length; UCL, upper crest length; LHL, lower hood length; LCL, lower crest length.

2.3 Statistical Analysis

The regressions among beak measurements and body size were made. The coefficient of determination was used to select the best relationship from linear, potential, exponential and logarithmic models. The significance was tested with F test for each measurement (Sokal and Rohlf, 1995). Regression equation was given when the slope of a regression line was significantly different from zero as was determined with the F-value. Resultingand number of cases () were also given, which should be considered in regressive estimation with these equations (Lu and Ickeringill, 2002). Analysis of covariance (ANCOVA) was applied to testing whether there were significant differences between sexes (Zar, 1999). All calculations and statistical analyses were carried out using Excel and the statistical package of SPSS 16.0.

3 Results

3.1 Relationships Among ML and TL, W

ML and TL of male individuals ranged from 37 to 144mm and from 242 to 1067mm, respectively. The weight of male individuals ranged from 17.5 to 391.7g. ML and TL of female individuals ranged from 40 to 143mm and from 339 to 935mm, respectively. The weight of female individuals ranged from 10.7 to 405.6g. The relationship between ML and TL was linear in both males and females, and there was no significant difference between sexes in these relationships (ANCOVA,>0.05) (Fig.2).

Fig.2 Relationships between mantle length (ML, mm) with A, total length (TL, mm) and B, body weight (W, g) for Octopus variabilis.

The equation

TL=6.33ML+120.40,

was used to describe such a relationship in which=0.85,=193, sex combined. The relationship between ML and W was linear only when ln-transformed data were used. Such a relationship was significantly different between two sexes (ANCOVA,<0.01) (Fig.2). The length-weight relationship for males can be described with

lnW=2.70lnML–7.54,

in which=0.87,=63; while that for females can be described with

lnW=2.14lnML–5.25,

in which=0.71,=130.

3.2 Relationships Among UHL, LHL and Body Size

UHL and LHL of male individuals ranged from 1.82 to 3.71 mm and from 1.29 to 2.98mm, respectively. UHL and LHL of females ranged from 1.51 to 3.63mm and from 1.25 to 2.65mm, respectively. The relationships among UHL, LHL and body lengths (ML and TL) were linear in both males and females (Fig.3).ANCOVA showed that such relationships were not significantly different between males and females (>0.05). Equations (both sex-independent and sex-combined) describing these relationships among UHL, LHL and body lengths were showed in Table 1.

In contrast, the relationships among UHL, LHL and W were appropriately described by a power function model which showed a dichotomy between males and females (<0.05) (Fig.3). It was not appropriate to describe the relationships among UHL, LHL and W with sex-com- bined equations. Plotting UHL, LHL vs. W in males and females, respectively, revealed that males reached a considerably greater W than females; however the upper and lower hood length was similar between males and females (Fig.3). Regression equations using ln-transformed UHL, LHL and W for both males and females were showed in Table 1.

3.3 Relationships Among UCL, LCL and Body Size

UCL and LCL of males ranged from 5.19 to 12.20mm and from 2.66 to 6.74mm, respectively. UCL and LCL of females ranged from 4.61 to 12.10mm and from 2.70 to 6.47mm, respectively.

Similar to the relationships among UHL, LHL and body lengths, those among UCL, LCL and ML, TL of both males and females were also linear (Fig.4). However, the relationships among UCL, LCL and W fitted a power function model and were linear only when natural logarithm transformed data were used. ANCOVA showed that these equations were not significantly different between males and females (>0.05). Equations describing the relationships among UCL, LCL and body size (both sex- independent and sex-combined) were showed in Table 1.

Fig.3 Relationships between A, mantle length (ML), B, total length (TL), C, body weight (W), with upper hood length (UHL: left) and lower hood length (LHL: right) for Octopus variabilis.

Table 1 Equations for the relationships between beak measurements and body size for Octopus variabilis in Jiaozhou Bay

()

()

Upper beakLower beak RelationshipSexnEquationr2RelationshipSexnEquationr2 C159lnW=3.58lnUCL−3.180.92C150lnW=3.32lnLCL−0.540.88 UCL vs WM49lnW=3.70lnUCL−3.410.93LCL vs WM48lnW=3.55lnLCL−0.880.92 F110lnW=3.47lnUCL−2.950.90F102lnW=3.08lnLCL−0.210.82 C159ML=5103UBW+50.280.80C145ML=7760LBW+48.460.82 UBW vs MLM50ML=4972UBW+49.880.86LBW vs MLM45ML=7833LBW+45.710.89 F109ML=5524UBW+49.160.72F100ML=8200LBW+48.220.71 C159TL=36220UBW+423.540.78C145TL=49370LBW+421.130.79 UBW vs TLM50TL=35319UBW+421.100.89LBW vs TLM45TL=50356LBW+416.860.87 F109TL=38683UBW+417.090.67F100TL=47649LBW+425.910.65 C159W=19829UBW−20.910.95C145W=27246LBW−20.610.93 UBW vs WM50W=19797UBW−19.210.96LBW vs W†M45W=28479LBW−20.850.92 F109W=19659UBW−20.900.91F100W=24160LBW−13.950.95

Notes: C, sexes combined; M, males; F, females;, sample size;significant difference between sexes,<0.05.

Fig.4 Relationships between A, mantle length (ML), B, total length (TL), C, body weight (W), with upper crest length (UCL: left) and lower crest length (LCL: right) for Octopus variabilis.

3.4 Relationships Among UBW, LBW and Body Size

UBW and LBW of males ranged from 1.45×10to 19.11×10×10to 11.70×10, respectively. UBW and LBW of females ranged from 1.00×10to 17.80×10×10to 13.89×10, respectively.

The relationships among UBW, LBW and body size (ML, TL and W) of both males and females were linear (Fig.5). ANCOVA showed that the equations describing the relationship between LBW and W were not significantly different between males and females (<0.05). Regression equations describing these relationships in both males and females were showed in Table 1.

Fig.5 Relationships between A, mantle length (ML), B, total length (TL), C, body weight (W), with upper beak weight (UBW: left) and lower beak weight (LBW: right) for Octopus variabilis.

4 Discussion

This study showed that the relationships between beak size and TL or ML ofwere linear, while the relationships between beak dimensions and W were better described by a power function model. Similar conclusions have been made for some other cephalopod species (Wolff, 1984; Lu and Ickeringill, 2002; Lalas, 2009; Liu and Chen, 2010).appears to be suitable for estimating size and biomass from beak measurements; most regression equations established in this study were appropriate for making these estimations.

To determine which beak measurements were most useful in dietary studies, both the significance of the regression lines and the durability of the dimensions in resisting digestion should be considered (Kashiwada., 1979). In this study, the lower hood length and upper crest length would be the most useful parameters for estimating the size offrom beak measure- ments, since they exhibit much less scatter about their regression lines. The upper and lower beak weights were testified to be better than other beak measurements to estimate the body weight of, since the determination coefficients of these regressions were all higher than 0.9 (Table 1). Unfortunately, because the wings and lateral walls of beaks are fragile and frequently damaged in stomachs, the beak weight often cannot be measured accurately after certain period of digestion. The durability of the beak in predators’ stomachs cannot be neglected and should be taken into account. For beaks taken from the stomachs of predators, the lower hood length and upper crest length dimensions were found to be the most durable and were usually undamaged (Kashiwada., 1979). They are, therefore, more valuable as tools for stomach analysis.

There was no significant difference between males and females in the relationships between beak measurements and body length in this study. Therefore the combined data for males and females should be useful to estimate the body length ofin predator studies. Some sexual dimorphism was found in the regressions between several beak measurements (UHL, LHL and LBW) and body weight (W) as male individuals have slightly greater body weight distribution than females for this species (Fig.2). This difference was so dramatic that a single regression could not be fitted to the pooled male and female data, which may make body weight a poor measurement for estimation particularly when the sex of the individual was unknown in the stomachs of predators. Similar phenomenon had been found in the beak analysis for squidand octopusfrom New Zealand waters (Jackson, 1995; Jackson., 1997; Lalas, 2009).

Potier. (2011) emphasized that within-species variance of the relationships between body size and beak measurements could be significant due to spatial variability for some cephalopod species. Therefore, these relationships found in this study should be used with caution in different areas. In addition, the beak remains recovered in the stomach should be examined carefully. Cephalopod beaks with eroded forms or broken wings have to be removed. These hard part structures are clearly fragments that accumulated over time and they can overemphasize the importance of some preys in the reconstructed diet of predators (Potier., 2011). They have to be excluded from the further analyses. In conclusion, when attempting to estimate size and biomass forbased on beak measurements, the limitations of such relationships need to be considered.

The equations provided here will be helpful in further biological and ecological studies on the octopus. Some further researches need to be carried out in the future to provide more useful information to study the role of cephalopod preys in marine food webs. It would be useful to obtain beak length and body size data from different geographical regions to see if a similar pattern could be observed for different populations. And the relationships between beak morphometrics and whole body attributes for more cephalopod specie need to be analyzed in the future.

Acknowledgements

This research was funded by The National Natural Science Foundation of China (41006083), The Shandong Provincial Natural Science Foundation, China (ZR2010 DQ026), The Fundamental Research Funds for the Central Universities (201022001, 201262004) and The Specialized Research Program for Marine Public Welfare Industry from the State Oceanic Administration, P. R. China (200805066).

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(Edited by Qiu Yantao)

10.1007/s11802-013-2194-9

ISSN 1672-5182, 2013 12 (3): 469-476

. Tel: 0086-532-82032960 E-mail: renyip@ouc.edu.cn

(October 29, 2012; revised December 12, 2012; accepted March 28, 2013)

© Ocean University of China, Science Press and Springer-Verlag Berlin Heidelberg 2013