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Ontogenetic difference of beak elemental concentration and its possible application in migration reconstruction for Ommastrephes bartramii in the North Pacific Ocean
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Zhou Fang1, 3, 4, 5, Bilin Liu1, 3, 4, 5, Xinjun Chen1, 2, 3, 4, 5, *, Yong Chen6
Acta Oceanologica Sinica | 2019, 38(10) : 43 - 52
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Acta Oceanologica Sinica | 2019, 38(10): 43-52
• Marine Biology •
Ontogenetic difference of beak elemental concentration and its possible application in migration reconstruction for Ommastrephes bartramii in the North Pacific Ocean
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Zhou Fang1, 3, 4, 5, Bilin Liu1, 3, 4, 5, Xinjun Chen1, 2, 3, 4, 5, *, Yong Chen6
Affiliations
  • 1 College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China
  • 2 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao) , Qingdao 266237, China
  • 3 National Engineering Research Center for Oceanic Fisheries, Shanghai Ocean University, Shanghai 201306, China
  • 4 Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources of Ministry of Education, Shanghai Ocean University, Shanghai 201306, China
  • 5 Key Laboratory of Oceanic Fisheries Exploration, Ministry of Agriculture, Shanghai 201306, China
  • 6 School of Marine Sciences, University of Maine, Orono, Maine 04469, USA
Published: 2019-10-25 doi: 10.1007/s13131-019-1431-5
Outline
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The migration route of oceanic squid provides critical information for us to understand their spatial and temporal variations. Mark-recapture and electronic tags tend to be problematic during processing. Cephalopod hard structures such as the beak, containing abundant ecological information with stable morphology and statolith-like sequences of growth increments, may provide information for studying spatio-temporal distribution. In this study, we developed a method, which is based on elemental concentration of beaks at different ontogenetic stages and sampling locations, to reconstruct the squid migration route. We applied this method to Ommastrephes bartramii in the North Pacific Ocean. Nine trace elements were detected in the rostrum sagittal sections (RSS) of the beak using laser ablation inductively coupled plasma mass spectrometry (LA-ICP-MS). For those elements, significant differences were found between the different ontogenetic stages for phosphorus (P), copper (Cu) and zinc (Zn). Sodium (Na), P and Zn were chosen as indicators of sea surface temperature (SST) and a regression model was estimated. The high probability of occurrence in a particular area represented the possible optimal squid location based on a Bayesian model. A reconstructed migration route in this study, combining all the locations at different ontogenetic stages, was consistent with that hypothesized in previous studies. This study demonstrates that the beak can provide useful information for identifying the migration routes of oceanic squid.

Ommastrephes bartramii  /  beak  /  trace element  /  ontogenetic stage  /  migration route
Zhou Fang, Bilin Liu, Xinjun Chen, Yong Chen. Ontogenetic difference of beak elemental concentration and its possible application in migration reconstruction for Ommastrephes bartramii in the North Pacific Ocean[J]. Acta Oceanologica Sinica, 2019 , 38 (10) : 43 -52 . DOI: 10.1007/s13131-019-1431-5
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1 Introduction
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The cephalopod, an important oceanic invertebrate species, plays an important role at the median trophic level in the marine ecosystem (Navarro et al., 2013). Oceanic species, especially Ommastrephids, support a high proportion of the world’s cephalopod fisheries, with catches from 2.0 million metric tons in the 1990s to a peak of 3.5 million metric tons in 2014 (http://www.fao.org/fishery/statistics).
In the North Pacific Ocean, a larger Ommastrephid species, Ommastrephes bartramii, is widely distributed and commercially exploited by the East Asian countries (Bower and Ichii, 2005; Chen et al., 2008; Jereb and Roper, 2010). Similar to other oceanic species, O. bartramii migrates a considerable distance over its ontogenetic stages (Ichii et al., 2009). The most popular methods to investigate cephalopod migration are external tag mark-recapture and electronic tags (Wearmouth et al., 2013; Mereu et al., 2015). However, jigging fishing activity cannot cover the entire spatial range of the squid feeding grounds, and the high rate of arm/tentacle breakage during jigging leads to a low recapture rate, making the external tag an unsuitable approach for squid study. Electronic tags in the squid’s mantle or fin are not easy to monitor as the tagged individuals are usually out of the range of recording devices (Semmens et al., 2007).
Cephalopods always seek a suitable habitat to maintain their daily activity to achieve an optimum oceanographic environment at all life stages, and consume prey to grow as fast as possible (Boyle and Rodhouse, 2005). Thus their surrounding environment and food availability are the two main drivers for squid movement and migration (Ichii et al., 2004; Watanabe et al., 2008). There is no doubt that oceanic squid are exposed to different environments at different life stages (Murata and Nakamura, 1998; Ichii et al., 2004). Female O. bartramii prefer to spawn in areas with an SST range from 21°C to 25°C, which is the optimum temperature for egg production (Vijai et al., 2015). After hatching, the paralarvae remain near the spawning ground with the current for the first 90 d at a preferred temperature of 20°C to 22°C (Nishikawa et al., 2014). The squid begin to prey on food when they have the ability of independent movement. It has also been reported that juvenile squid always inhabit food-rich areas with SST>21°C (Kato et al., 2014). Adult squid grow fast with a voracious feeding behavior, so they tend to gather in high productivity areas, which are those feeding grounds with SST 16–19°C, as has been suggested by most researchers in previous studies (Tian et al., 2009; Alabia et al., 2015). Temperature is an indicator that directly influences squid growth and their food distribution, and also indirectly influences squid migration.
Understanding the relationship between squid movement behavior and their key environment is thus a priority to study the possible migration routes. The statolith is often referred to as a “black box” because it records the ecological information of the whole life stages of the squid (Arkhipkin, 2005). The age and growth pattern can be analyzed through the increments in the statolith microstructure (Arkhipkin and Shcherbich, 2012), and the distinctive chemical composition also reveals the ambient experienced by the squid at different life stages (Liu et al., 2015a; Arbuckle and Wormuth, 2014). The Sr/Ca ratio is an important sea surface temperature (SST) indicator for investigating the migration strategies of different ommastrephid squid (Ikeda et al., 1997, 2002, 2003).
As an important hard structure in squid, the beak, which has a larger size than the statolith and a unique morphology, has become an alternative tool for investigating squid biology in recent years (Chen et al., 2012; Franco-Santos and Vidal, 2014; Liu et al., 2015b; Fang et al., 2016a). A sequence of growth increments were also observed in the microstructure in the rostrum sagittal sections of the beak, which suggests that the beak can be used in the study of age and growth for squid (Liu et al., 2015c; Fang et al., 2016b). Stable isotopes (δ13C and δ15N) in the squid beak also reflect the variation of trophic position and foraging areas at intra- and inter-species levels (Jennings and Cogan, 2015; Fang et al., 2016b). The beak is a compound that consists of protein and polysaccharide (chitin), and the pigmented part, which contains high-density catecholic-histidine cross linking, has also attracted the attention of researchers who have tried to apply it in new biomaterials (Miserez et al., 2007, 2008, 2010). Some studies have tried to explore the inorganic elements in the cephalopod beak, although this is not a common material for biochemical analysis. Rodríguez-Navarro et al. (2006) suggested that the trace element profiles (P and Se) in the beak could indicate a gradual descent to deeper waters during the life of the giant squid (Architeuthis sp.). Thus, analyzing the trace elements in the beak is a potential method to investigate the pattern of squid movements.
In this study, we quantitatively measured the main trace elements to estimate the category and concentration of the O. bartramii beak and compared the possible elemental difference at different life stages and hatching seasons. The migration route of O. bartramii was also reconstructed based on the relationship between sea surface temperature and selected beak elemental signatures. This study shows the potential of using microchemistry to improve our understanding of the migration pattern of O. bartramii in the Northwest Pacific Ocean.
2 Materials and methods
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2.1 Sample collection and measurements
A total of 62 squid samples were randomly obtained from the commercial oceanic jigging vessel F/V Jinhai 827 which operated in the Northwest Pacific Ocean (39°–44°N, 152°–157°E) from July to November in 2010 and 2011. Samples were immediately frozen at –18°C for future laboratory work.
Dorsal mantle length (ML) was measured to the nearest 1 mm after thawing in the laboratory. The upper and lower beaks were dissected from the buccal mass, washed with fresh water and stored in 75% ethyl alcohol. As the upper beak is larger than the lower beak, and age estimation has been tested on the rostrum of the upper beak in previous studies (Liu et al., 2015c; Fang et al., 2016b), we used the upper beak for the next step.
2.2 Age estimation and back-calculation
The statolith is often used for cephalopod age estimation (Arkhipkin and Shcherbich, 2012), but the tiny size of a statolith and the cumbersome process protocol complicates the interpretation of the ageing results (Arkhipkin, 2012). Thus the utilization of other hard structures has been proposed (Moltschaniwskyj and Cappo, 2009). Liu et al. (2015c) suggested that the increments in the beak rostrum had a deposition pattern similar to a statolith increment, and Fang et al. (2016b) suggested that the beak could be a useful material for age estimation for O. bartramii. We used 40 upper beak rostrum sagittal sections (RSS) for ageing and back-calculating the hatching dates based on estimated age and date of capture. All the increments in the statolith sample were read by two researchers, and the result is the average age with standard deviation.
2.3 Sea surface temperature (SST) data
Sea surface temperature (SST) is considered to be an important factor affecting the incremental deposition in the statolith, as the squid take up trace elements at night on the sea surface (Bettencourt and Guerra, 2000). Perales-Raya et al. (2014a) reported that a high variation of SST coincided with the locations of the marks on the beak of Octopus vulgaris, and that beak growth was closely related to the environment, including SST (Perales-Raya et al., 2014b). Thus the SST has a high correlation with beak growth. Real-time SST data were recorded with a highly accurate conductivity and temperature recorder (SBE 37-SMMicroCAT; Sea-Bird Electronics, Bellvue, WA) at each sampling station. In order to get precise temperatures, the weekly SST in the Northwest Pacific Ocean during 2009 to 2011 was downloaded from the National Oceanic and Atmospheric Administration website (http://oceanwatch.pifsc.noaa.gov/) with spatial resolution of 0.1°×0.1°. The SST of the week to the nearest time when a back-calculated ontogenetic stage occurred was used as the SST for the life history stage.
2.4 Trace element analysis
All the 40 beak samples were selected for trace element analysis (Table 1). After reading the increments from the RSS of the beak, the polished RSS was washed in ultra-pure water for 5 min, and then rinsed at least twice before being air dried. Laser ablation was used to sample in different areas of the beak, the location representing each different ontogenetic stage as referred to by Young and Harman (1988) and Liu et al (2015c). The growth of the beak starts from the tip (Hernández-López et al., 2001; Perales-Raya et al., 2010), so the tip (0–5 increments) of the RSS represents the embryonic stage, the second spot, located in approximately the 30th increment represents the paralarval stage, the third spot located around the 60th increment represents the juvenile stage, the fourth spot located at about the 120th increment represents the sub-adult stage, and the intersection point between the hood and crest represents the sub-adult stage, and also indicates the capture time (Fig. 1).
Compared to the statolith, the main elements in a cephalopod beak are 43Ca, 23Na, 24Mg, 31P, 39K, 55Mn, 63Cu, 66Zn, 83Se, and 88Sr. Therefore, an analysis of the above ten elemental signatures was performed using a 193-nm frequency-quadrupled ArF exciter laser (GeoLas, 2005; Lambda Physik, Götingen, Germany) with pulse of 8 Hz, energy of 6.0 J/cm2, and sampling spot diameter of 44 μm. This laser ablation station was connected to an Agilent 7500a inductively coupled plasma mass spectrometer (ICP-MS) with sample gas Helium of 0.9 L/min and flow gas of Argon 0.92 L/min (Agilent Technologies, Santa Clara, CA). Each analysis incorporates 20 s of background acquisition followed by 60 s of sample ablation to the corrected sample concentrations (Elsdon and Gillanders, 2005; Liu et al., 2016). An ANOVA test and a t-test were conducted to evaluate the possible difference between the different ontogenetic stages and seasonal hatching groups, respectively.
2.5 Hypothesis and assumptions
Each of the ten elements (43Ca, 23Na, 24Mg, 31P, 39K, 55Mn, 63Cu, 66Zn, 79Se, 88Sr) on the tip of the RSS (spot 5) was analyzed, and stepwise multiple linear regression analyses were used to predict the optimal SST. The best fit model was selected by the stepwise removal of the elements based on Akaike information criterion (AIC) (Akaike, 1974). It is possible to estimate the optimal SST for the earlier ontogenetic stage on the basis of the relationship between SST and the relevant element. The possible spatial locations corresponding to the suitable SST can be determined according to the elemental concentration (Liu et al., 2016). As we know the elements concentration of squid beak in different life time, it is easily to find the suitable SST according to the established relationship between SST and relevant element. Considering the squid swimming ability, the possible location (longitude and latitude) of SST will also revealed in the SST database mentioned in above content using Bayesian model.
All the samples were taken in a similar area and shared the same habitat. We identified that they belonged to the same cohort according to previous studies (Fang et al., 2016b). Therefore the squid are likely to experience a similar environment during their life history, even if they were not born at same time. Finally, the deduced migration routes were connected by combining the optimal locations (highest occurrence area in each stage) at all five ontogenetic stages.
The timing of each ontogenetic stage was estimated following Liu et al. (2016). The squid were assumed to swim in a range of defined suitable SST values, and the maximum swimming speed of O. bartramii, 20 km per day (Tanaka, 2001), was used for calculating the possible migration range. The possibility of a squid occurrence area was also calculated following Liu et al. (2016). The best model selections and migration reconstructions were all carried out with R 3.1.3 (R Core Team, 2015) using the package “MASS” (Venables and Ripley, 2002) and “geoR” (Ribeiro and Diggle, 2001), respectively.
3 Results
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3.1 Element concentration in the beak
The highest concentration of the analyzed elements was Ca, with an average±standard deviation (1 497.05±628.8)×10–6 (Table 2). Magnesium (Mg) had the second highest concentration with (597.21±279.34)×10–6 (Table 2). The other elements with concentrations higher than 100×10–6 were phosphorus (P), sodium (Na) and potassium (K) (Table 2). Strontium (Sr), of which there are high concentrations in the statolith, had the lowest concentration in the beak (Table 2). Concentrations of all the elements were unstable with a relatively high standard deviation in the results (Table 2). The concentration of Se in the RSS was too low to be measured.
3.2 Elemental signature difference among ontogenetic stages and hatching times
The elemental signatures at the embryonic and paralarval stage were lower than at the other ontogenetic stages, as the elements accumulated with squid growth. Mg/Ca mostly remained at the same level until the adult stage (Fig. 2a). The concentrations of Na/Ca and K/Ca increased during the juvenile and sub-adult stage, but decreased at the adult stage (Fig. 2a). Concentrations of P/Ca and Zn/Ca increased drastically from the paralarval to the juvenile stage, and then fluctuated between the juvenile and adult stage (Figs 2a and b). The concentration of Cu/Ca was highest in the juvenile stage, and then decreased (Fig. 2b). The ANOVA test showed that P/Ca, Cu/Ca and Zn/Ca had a significant difference at different ontogenetic stages (P<0.05), and the embryonic and paralarval stage had a significant difference when tested post-hoc.
All of the squid sampled in this study were hatched between May and October of the previous year. Thus we separated the samples into two seasonal groups, the winter hatching group (hatching time during October to February) and spring hatching group (hatching time during March to May). Statistical analysis showed that none of the elements differed between the two seasonal groups at every ontogenetic stage (P>0.05), although the concentration of P/Ca fluctuated in different patterns during the paralarval and adult stages (Fig. 3a), and the Cu/Ca showed a reverse pattern during the sub-adult and adult stages (Fig. 3b).
3.3 Migration route reconstruction
As the stepwise regression analysis describes (Table 3), sodium, phosphorus and zinc are suitable indicators of SST. The derived regression model can be described as follows: SST = 20.367 – 0.0076[Na] – 0.0009[P] + 0.0201[Zn] (R2=0.552, P<0.01).
The ages selected from the five analyzed locations on the RSS of the beak represented the five ontogenetic stages, with an age of 0 days for an embryo, 27 (18–35) d for paralarvae, 58 (45–70) d for juveniles, 124 (90 –139) d for sub-adults, and 162 (118 –180) d for adults (Table 4). The value range of Na/Ca, P/Ca and Zn/Ca is shown in Table 5. In the embryonic and paralarval stages, the value of Na/Ca is nearly unchanged although P/Ca and Zn/Ca increased steadily. The value of the three selected elements performed a “U-shape” tendency during the juvenile to adult stages. (Table 5).
The occurrence probability of squid at different ontogenetic stages was calculated and the results are shown in Fig. 4. The migration route can be described by connecting the highest occurrence probability during the consecutive ontogenetic stages (Fig. 5). A south-north migration trace for O. bartramii is shown in Fig. 5.
4 Discussion
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The squid movement pattern is closely related to the ambient environment (Sim et al., 2001). The eggs and paralarvae passively drift with the current, and then the squid actively migrate in a relatively long journey in line with body growth (O’Dor and Balch, 1985). Feeding and spawning are the two reasons that cause the squid to migrate (Semmens et al., 2007). Thus a good understanding of migration routes can enhance our knowledge of squid population dynamics and spatial distribution leading to improved assessment and management of this important fisheries resource.
The composition of trace elements in the beak was quite different from those in the statolith (Table 2). Most of the metal elements, including magnesium, sodium, potassium, copper and zinc, had already been detected in the statolith, and some of the elements were taken up from the water mass and then deposited in the statolith (Liu et al., 2013; Arbuckle and Wormuth, 2014). Strontium is the second highest element in the statolith, but in this study the value of strontium in the beak was low (only about 10×10–6) (Table 2). Phosphorus is a remarkable trace element in the beak, which is rarely seen in the statolith (Table 2). Unlike the calcareous tissues of the statolith, the beak is a fully organic hard structure in which any mineral phases and metals are mostly absent (Miserez et al., 2007). Thus the beak would experience a series of protein syntheses to prompt cell proliferation and growth, and phosphorus plays an important role connecting different kinds of amino acid and promotes protein synthesis (VanBogelen et al., 1996). It is, therefore, easy to understand the reason for the high concentration of phosphorus in a squid beak. Selenium was not measured in this study. As the species and the environment become more varied, more element concentrations in the beak should be tested in the future.
Phosphorus, copper and zinc obviously fluctuated highly at the different ontogenetic stages, although only copper showed significant differences (Fig. 2b). These three elements increased greatly from the paralarval to the juvenile stage (Fig. 2). With squid growth, the transformation of feeding behavior of paralarvae to juveniles moves from a passive uptake of zooplankton to gradually active preying on small crustaceans and fish (Watanabe et al., 2008), and phosphorus increases to promote protein synthesis, allowing beak cells to grow faster to adapt to this behavior change. The hard and colored part of the beak enables the squid to eat large prey with hard skins. This beak pigmentation process is a kind of melanogenesis, and copper and zinc are two important trace elements for the speed of melanin biosynthesis (Swan, 1974; Slominski et al., 2004). The squid would then migrate from the hatching area to the feeding ground during the juvenile to sub-adult stage. In this phase, the food composition does not change too much but most of the nutrition is supplied for migration movement, so the concentration of the above three elements decreases, but is still higher than that at the paralarval stage (Fig. 2). Squid need enough food for gametogenesis during the sub-adult to adult stage. Therefore, the beak experiences a second round of growth and becomes stiffer to allow the squid to prey on larger fish and other squid (Watanabe et al., 2004; Fang et al., 2016c), so phosphorus and zinc increase again to a high level (Fig. 2). This may explain the “U-shape” tendency of P/Ca and Zn/Ca during the juvenile to adult stages. A decrease in copper may be caused by an antagonistic effect with zinc in an organism (Fig. 2).
It is possible to predict squid migration routes and timing with the development of new methodologies and devices. SST is an important environmental factor that limits the distribution of O. bartramii. Optimum SST controls the movement of squid, which is why specific locations and temperature for O. bartramii at different life stages have been investigated in previous studies (Table 6). Some suitable elemental signatures were selected as temperature indicators to predict areas of high probability of occurrence for different ontogenetic stages of O. bartramii in the North Pacific Ocean. The range of highest probability occurrence between embryonic and paralarval stages was similar (Fig. 4). It is well-known that squid at the early life stage (e.g., egg, paralarvae, even juvenile) lack the ability to actively swim and only passively move with the currents (Ichii et al., 2009; Nishikawa et al., 2014, 2015). So the locations in the two early life stages were in exactly the same area and a little northeastward at the paralarval stage, due to the direction of the Kuroshio Current (Fig. 4). At the juvenile stage, all the probability ranges were extended, especially to northward of 30°N (Fig. 4). Watanabe et al. (2008) described that for the winter-spring cohort of O. bartramii to actively prey on its food in summer, this migration orientation would be influenced by the Kuroshio and Kuroshio Extension that transports some individuals to an offshore area (eastward to 150°E) (Nishikawa et al., 2014), which is consistent with the results shown in this study (Fig. 4). The highest probability occurrence reached 40°N in the sub-adult stage, which is the nursery grounds for O. bartramii (Ichii et al., 2009). Finally, the adult squid were captured by fishing vessel at 40°N to 45°N (Fig. 4). The path of the migration route in this study is approximately consistent with the previously described study in that the winter-spring cohort of O. bartramii make a northward migration from a lower to a higher latitude in the northern hemisphere from the embryonic to the adult stage (Ichii et al., 2009).
Compared to the location of the spawning ground in the previous study (20°–25°N) (Ichii et al., 2009; Nishikawa et al., 2014; Igarashi et al., 2017), the location of the spawning ground in this study was located at a higher latitude (25°–30°N, Fig. 4). The habitat of squid is largely influenced by environmental variability at different spatial-temporal scales (Tian et al., 2013). Therefore the variations of optimal habitat were observed both in the spawning and the feeding ground (Alabia et al., 2015, 2016). This may be one of the reasons causing the above difference. Squid hatching in different months may also lead to latitudinal variation based on a particle tracking experiment (Nishikawa et al., 2014).
Biotic factor should be considered in the early life stage migration route, although some environmental factors may impact on the paralarvae/juvenile distribution (Nishikawa et al., 2014, 2015). Temperature is indeed the main factor influencing the survival of a squid embryo (Vijai et al., 2015). Some studies have also suggested that juvenile squid cannot choose their own habitat and only float with the current, having no swimming capability (O’Dor and Balch, 1985; Staaf et al., 2008). So a current that related to squid habitat should be added as an important factor for modelling. The elemental signature at the embryonic stage is less reliable than the velocity of current, which is considered to be a factor, due to egg hatching relying mainly on the nutrition in the yolk, which in turn depends on the predecessor (Zumholz, 2005). An individual-based biophysical-coupled model and a coupled physical-ecosystem model, which represented a more realistic methodology, were both used to simulate the possible distribution and movement of the larvae of O. bartramii (Kato et al., 2014; Nishikawa et al., 2015).
5 Conclusions
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We analyzed the category and concentration of elements in beaks of O. bartramii, and reconstructed the migration route based on the relationship between sea surface temperature (SST) and elemental signature. The beak mainly consists of the elements calcium, magnesium, phosphorus, sodium, potassium, copper and strontium, with the various concentrations ranking from high to low. Ontogenetic and hatching time variations were significant in the elements of phosphorus, copper and zinc. Three elements (sodium, phosphorus and zinc) were selected to fit the regression model with the corresponding SST, and the high probability occurrence range was simulated based on a Bayesian model. The reconstructed migration route was roughly consistent with previous studies, which presented a northward migration along the Kuroshio Current from the embryonic stage to the adult stage. Future study should analyze the beaks of different species of squid to compare the variation of element composition, and use more realistic methods (e.g., particle tracking simulation) to estimate the movement pattern of squid at early life stages.
Acknowledgements
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The support of the scientific surveys by commercial jigging vessel F/V Jinhai 827 is gratefully acknowledged.
Funding
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  • The National Natural Science Foundation of China under contract No. NSFC4147129; the China Postdoctoral Science Foundation under contract No. 2017M610277; the Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources (Shanghai Ocean University), Ministry of Education under contract No. A1-0203-00-2009-6; the Fund of Key Laboratory of Open-Sea Fishery Development, Ministry of Agriculture, China under contract LOF 2018-02.
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doi: 10.1007/s13131-019-1431-5
  • Receive Date：2018-02-09
  • Online Date：2026-04-01
  • Published：2019-10-25
Article Data
Affiliations
History
  • Received：2018-02-09
  • Accepted：2018-11-15
Funding
The National Natural Science Foundation of China under contract No. NSFC4147129; the China Postdoctoral Science Foundation under contract No. 2017M610277; the Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources (Shanghai Ocean University), Ministry of Education under contract No. A1-0203-00-2009-6; the Fund of Key Laboratory of Open-Sea Fishery Development, Ministry of Agriculture, China under contract LOF 2018-02.
Affiliations
    1 College of Marine Sciences, Shanghai Ocean University, Shanghai 201306, China
    2 Laboratory for Marine Fisheries Science and Food Production Processes, Pilot National Laboratory for Marine Science and Technology (Qingdao) , Qingdao 266237, China
    3 National Engineering Research Center for Oceanic Fisheries, Shanghai Ocean University, Shanghai 201306, China
    4 Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources of Ministry of Education, Shanghai Ocean University, Shanghai 201306, China
    5 Key Laboratory of Oceanic Fisheries Exploration, Ministry of Agriculture, Shanghai 201306, China
    6 School of Marine Sciences, University of Maine, Orono, Maine 04469, USA

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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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