Feeding habits of juvenile Japanese common squid Todarodes pacificus: Relationship between dietary shift and allometric growth

Fisheries Research 152 (2014) 29–36

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Feeding habits of juvenile Japanese common squid Todarodes pacificus: Relationship between dietary shift and allometric growth Kazuhisa Uchikawa ∗ , Hideaki Kidokoro Japan Sea National Fisheries Research Institute, Fisheries Research Agency, 1-5939-22, 951-8121 Niigata, Japan

a r t i c l e

i n f o

Article history: Received 15 December 2012 Received in revised form 4 July 2013 Accepted 4 July 2013 Keywords: Todarodes pacificus Ecomorphology Allometric growth Feeding habits Dietary shift

a b s t r a c t In this study, ontogenetic dietary shifts in relation to morphological changes were examined in juvenile Japanese common squid Todarodes pacificus (<160 mm mantle length; ML) collected in the Sea of Japan. Ten morphometric characters were measured for 147 specimens of Japanese common squid. The allometric growth pattern of each character in relation to ML was studied by using the logarithmic form of the allometric growth model with piecewise regression analysis. The allometric growth pattern indicated that the body shape of T. pacificus changed from a rounded to a more streamlined shape, and only growth of the fin base length and fin width were positively allometric. Three morphological characters had an inflection point at 53–72 mm ML, indicating the transformation to an adult morphology. The digestive tract contents of 135 squids were examined for dietary shifts. T. pacificus smaller than 50 mm ML fed exclusively on crustaceans such as copepods, amphipods and euphausiids, and then shifted to a mixed diet of crustaceans and fish at 50–99 mm ML; after reaching 100 mm ML, fish were the most important prey items and crustaceans became less important. These suggest that the swimming performance of T. pacificus changes markedly at around inflection points, the size at which T. pacificus starts to feed on fish. Therefore, the dietary shift is suggested to be closely related to the ontogenetic change in swimming performance. © 2013 Elsevier B.V. All rights reserved.

1. Introduction Many animals shift their diet with growth and the shift often coincides with the ontogenetic changes in morphology (Emerson et al., 1994, and references therein). Dietary changes during growth are thought to occur because growth imposes a number of scaling constraints in foraging performance and energy demands (Persson et al., 1998; Svanbäck and Eklöv, 2002; Werner and Gilliam, 1984). Furthermore, animals that change their niche during ontogeny are often subjected to antagonistic demands that may result in reduced performance compared to animals that specialize in one niche throughout their ontogeny (Svanbäck and Eklöv, 2002; Werner and Gilliam, 1984). It is therefore important to understand why particular morphological patterns are associated with sets of ecological features and how morphology influences the behavioral abilities of individual animals. Understanding the functional significance of morphology is therefore a crucial step in identifying morphological constraints on the function of feeding structures, performance patterns and

∗ Corresponding author. Tel.: +81 25 228 0536; fax: +81 25 224 0950. E-mail addresses: [email protected] (K. Uchikawa), [email protected] (H. Kidokoro). 0165-7836/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.fishres.2013.07.001

resource use in animals. Such a conceptual link between morphology and ecology called ecomorphology, therefore, provides a tool for predicting processes within an animal’s way of life (Reilly and Wainwright, 1994; Wainwright, 1996). In the aquatic environment, many studies on fish feeding ecology have demonstrated that morphology shapes the behavioral capability, and the behavioral capability in turn shapes the resource use (Barnett et al., 2006; Christensen, 1996; Norton, 1991; Svanbäck and Eklöv, 2002; Wainwright, 1996; Wainwright et al., 2002). All squid species are carnivores exhibiting rapid growth and short life spans (usually about 1–2 years) (Mangold, 1987; O’Dor and Webber, 1986; Rodhouse and Nigmatullin, 1996). Changes in diet during growth have been broadly reported in many squid species (Cherel et al., 2009; Hunsicker et al., 2010; Quetglas et al., 1999; Ruiz-Cooley et al., 2006; Santos and Haimovici, 1997). Therefore, ontogenetic dietary shifts in squid may occur over a relatively short time span. Furthermore, several studies have shown that morphological change during ontogeny is closely related to locomotive ability and life history traits (Bartol et al., 2008; Boletzky, 1987; Hoar et al., 1994; O’Dor, 1988; Moltschaniwskyj, 1995; O’Dor and Hoar, 2000; Perez and O’Dor, 2000; Uchikawa et al., 2009; Vidal, 1994; Zeidberg, 2004). However, few studies to date have directly assessed associations between diet and body shape.

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K. Uchikawa, H. Kidokoro / Fisheries Research 152 (2014) 29–36

logarithmic (log10 ) form of the allometric growth model (Huxley, 1932), using mantle length (ML) as the independent variable;

42

log y = log a + b log x

40

Sea of Japan

38

Honshu 36

34 130

Island

135

140

Fig. 1. Sampling locations in the Sea of Japan where Todarodes pacificus were collected. A closed circle indicates that sampling was carried out using both a midwater trawl and a LC-net.

In this study we focus on the diet and morphological development in relation to prey capturing ability of juvenile Japanese common squid Todarodes pacificus. The Japanese common squid, T. pacificus (Cephalopoda; Ommastrephidae) is an ecologically and commercially important squid around Japan. T. pacificus may undergo ontogenetic dietary shifts during its life, and capable of foraging on a wide variety of prey. Although size at which dietary shift occurs is unclear in T. pacificus, this squid is thought to be a zooplankton feeder as a juvenile, and when large enough it then shifts to a diet mainly consisting of fish and squid including its own species (Hamabe and Shimizu, 1966; Kidokoro and Uji, 1999). Therefore, we firstly examined the allometric growth pattern of morphological characters related to prey capture and locomotive abilities. Secondly, we examined the diet composition in detail to describe the dietary shift during growth. Finally, we discuss the interplay of diet and morphology during ontogeny in T. pacificus.

2. Materials and methods T. pacificus were sampled during four cruises of RV “MizuhoMaru” in April 2007, 2008 and 2009 and RV “Shunyo-Maru” in April 2009 conducted by the Japan Sea National Fisheries Research Institute (JSNFRI). In the “Mizuho-Maru” cruises, a midwater trawl modified to fish at the surface was towed for 30 min at each station (Fig. 1). The trawl had a horizontal opening of 10 m, a vertical opening of 10 m, and mesh size of 7 mm in the cod end. In the “Shunyo-Maru” cruise, an LC-net was towed for 30 min at each station. The LC-net had a horizontal opening of 10 m, a vertical opening of 10 m, and mesh size of 4 mm in the cod end. All sampling was operated near the surface at night. Specimens were frozen at sea, and then thawed in the laboratory. Some specimens were fixed in a 10% solution of buffered formaldehyde in water for dietary analysis. A total of 147 individuals were measured for ten morphological characters (Fig. 2). Linear regressions were performed on the

where x is mantle length (ML), y is the morphological character in length (mm), log a is the intercept of the line on the y-axis and b is the slope of the line (also known as the allometric coefficient). When x and y are mantle and organ sizes at different developmental stages, the allometric coefficient enables assessment of the differential growth ratio between the organ and the mantle. When an organ has a higher growth rate than the mantle (b > 1), the allometry is termed as positive and a lower growth rate (b < 1) as negative allometry, and when an organ grows at the same rate as the mantle (b = 1), the condition is called isometry. The x value where the slope changes is called the inflexion point. For a character that has an inflection point, the residuals have a patterned distribution (Fig. 3a) as has been shown by Shea and Vecchione (2002). To identify characters with inflection points of a regression line during squid growth, the residual sums of squares (RSS) were examined to estimate the inflection points. The points of inflection for the segmented relationships were determined by testing each inflection point iteratively to obtain the lowest sum of RSS value. Next, we calculated the equation of the line for segments before and after the inflection point. The inflection point was accepted if the 95% confidence interval (CI) of both coefficients did not overlap and ANCOVA (F-test for slope) detected any significant difference between regression lines. Also, t-tests were made to check whether the coefficients differed significantly from slope = 1 (b = 1). t-Statistic is calculated as; t=

b−1 sb

where t is the t-statistic for a morphological character, b is the regression coefficient for the morphological character, and sb is the standard error of the regression coefficient (Zar, 1999). It has been pointed out that the linear ordinary least squares regression (type I regression) like the above analysis was not appropriate for the developmental relationship analyses, because it assumes that the independent variable is measured without error (Green, 1999; Sokal and Rohlf, 1995). However, the justification for using a type II regression is questionable when a causality relation exists between variables (Eberhard et al., 1999; Sokal and Rohlf, 1995). Thus, the major axis regression, which is one of the methods of the type II regressions, has also been used for assessing the allometric slope. Statistical tests, other than type II regression, were performed using the software package JMP v. 9.02 (SAS Institute Inc., Cary, NC). Major axis analysis was performed using the program (S)MATR, version 2.0 (Falster et al., 2006). The differences in segmented slope in type II regression were tested for homogeneity of slopes, which was equivalent of standard ANCOVA for type I regression. For dietary analysis, fixed specimens were used. Whole digestive tracts, esophagus, stomach, caecum and intestine were carefully removed and dissected. Dietary analysis of squid is difficult because prey items are fragmented by the actions of the beak and radula and are hard to identify. Preliminary analysis of digestive tract contents indicated that mandibles of crustaceans passed undamaged through the guts. Therefore, a method based on the identification of mandibles was developed. Crustaceans for this purpose were collected concurrently with squid by a NORPAC net and used specimens deposited at JSNFRI. A pair of mandibles was carefully dissected using tungsten needles under a stereomicroscope, and morphological characteristics were recorded. Amphipods and euphausiids were easy to identify, since only two species dominated for each taxa in the study area. For example,

K. Uchikawa, H. Kidokoro / Fisheries Research 152 (2014) 29–36

31

TL AL FAW

ED

MD

BMD

HW ML

FBL FW Fig. 2. Body measurements of Todarodes pacificus. ML, mantle length; TL, tentacle length; AL, arm III length; ED, eye diameter; FBL, fin base length; HW, head width; FW, fin width; FAW, funnel aperture diameter; MD, mantle diameter; BMD, buccal mass diameter.

Thysanoessa longipes has more robust mandibles than Euphausia pacifica, as has been described in Nemoto (1967). Copepods were the most diverse taxa in our results (Table 2), and they could generally be identified to genus or family level from mandible characteristics. But they could be identified to species when enough body parts for the identification of species remained. Zooplankton prey, including the taxa above mentioned, were also identified by key morphological characters described in Brodsky (1950), Park (1995), Baker et al. (1990), Vinogradov et al. (1996) and “An illustrated Guide to Marine Plankton in Japan” edited by Chihara and Murano (1997). All cephalopod prey could not be identified, because diagnostic parts such as lower beaks were highly damaged. In fish prey, sagittal otoliths were not found, possibly due to the squid behavior that discards the hard parts of prey (Bradbury and Aldrich, 1969; Kitagawa et al., 1992). However, some of fish remains had photophores on the body surface. They could be identified to Maurolicus japonicus, since M. japonicus is the only species with photophores on the body surface inhabiting in the study area. The prey items were counted and weighed to the nearest 0.01 mg. The numbers of individuals of each prey taxon were estimated from the numbers of prey morphological characters. If the numbers of different body parts of a prey taxon differed, the larger number was chosen to represent the number of prey. Diet was expressed using percent number (%N), percent mass (%M) and percent frequency of occurrence of a determined prey item in relation to the total number of individuals excluding empty digestive tracts (%F) (Hyslop, 1980). Based on these indices, for major prey categories, the index of relative importance (IRI; Pinkas et al., 1971) was calculated and standardized as %IRI (Cortés, 1997). The %IRI was calculated as; %IRIi =

ostracods, amphipods, euphausiids, decapods, chaetognaths, fish and cephalopods). 3. Results 3.1. Allometric growth patterns Of the nine body measures examined, only the residuals of mantle diameter (MD), head width (HW) and eye diameter (ED) were patterned (Fig. 3 and Table 1) and a segmented relationship with a single inflection point was observed in MD, HW and ED. Inflection points of these three characters were between 53 and 72 mm ML. In all cases, the allometric coefficients between pre- and postinflection points were significantly different (p < 0.05) and growth rates of the pre-inflection points were much slower than those of the post-inflection points. However, after post-inflection points, growth rates of these characters indicated still negative allometry. Coefficients of type II regression slopes were consistently higher than those of type I regression slopes. However, there was little difference in the estimates of allometric relationships of body characters between type I and type II regression, from comparison of 95% confidence intervals (Table 1). Growth of the fin base length (FBL) and the fin width (FW) were positively allometric in both results. Five morphological characters such as HW and MD grew with negative allometry (Table 1). Only tentacle length (TL) was isometric in type I regression (b = 1.019), but indicated weak positive allometry (b = 1.043) in type II regression (Table 1). 3.2. Dietary composition

100 × (%Ni + %Mi ) × %Fi

n

i=1

(%Ni + %Mi ) × %Fi

In our results, almost all unidentified material from contents was a mucus-like matter which did not contained any recognizable parts. In order to reduce the bias from mucus in the contents, unidentified material was excluded from the calculation of each index. The %IRI was calculated for eight prey categories (copepods,

Digestive tract contents of 135 individuals were examined microscopically, and 16 were empty. The diet of T. pacificus was comprised of eight major prey groups (Table 2) and copepods, amphipods, euphausiids, chaetognaths and fish were predominant (Fig. 4). Copepods were the most diverse prey group including 12 species such as Paraeuchaeta elongata and Paracalanus parvus. Copepods were numerically important prey of all size classes of

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K. Uchikawa, H. Kidokoro / Fisheries Research 152 (2014) 29–36

Table 1 Allometric coefficients for each character. CI in a parenthesis, 95% confidence interval for regression slope. Character

Inflection point (mm ML)

MD

71.9

HW

53.4

ED

57.1

FAW

–

BMD

–

FBL

–

FW

–

AL

–

TL

–

*

Type I

Type II

Slope(b) (CI)

Slope(b) (CI)

Segment 1

Segment 2

Segment 1

Segment 2

0.429* (0.376–0.482) 0.509* (0.383–0.635) 0.487* (0.389–0.586) 0.706* (0.677–0.735) 0.697* (0.671–0.723) 1.311* (1.291–1.331) 1.061* (1.043–1.079) 0.895* (0.870–0.920) 1.019 (0.983–1.055)

0.753* (0.699–0.807) 0.833* (0.777–0.889) 0.721* (0.670–0.772) –

0.446 (0.392–0.503) 0.555 (0.424–0.702) 0.520 (0.419–0.631) 0.721 (0.692–0.751) 0.709 (0.683–0.736) 1.318 (1.299–1.339) 1.067 (1.049–1.085) 0.907 (0.882–0.932) 1.043 (1.007–1.080)

0.781 (0.726–0.839) 0.880 (0.822–0.941) 0.756 (0.704–0.811) –

– – – – –

– – – – –

The slope of the fitted line is significantly different from 1 (P < 0.001).

T. pacificus examined (%N > 26%), but its gravimetric contributions were limited (%M < 8%). Euphausiids were the most important prey by frequency of occurrence in the diet of all size classes (%F > 37%), and were the most important by number and wet mass in the diet of <50 mm ML squid (%N = 30.0%, %M = 54.6%). The %N and %M of euphausiids was highest in the diet of <50 mm ML size class, and decreased gradually with increasing squid size. Micronektonic fish such as M. japonicus compensated for the decrease in %M of euphausiids, which were the most important prey by mass (%M > 67%) for 50–99 mm and ≥100 mm ML size classes. Amphipods were less important prey items compared with other prey groups mentioned above, but they were second to fourth importance by all indices in the diets of all squid size classes. Diet comparisons by %IRI between different sizes of T. pacificus revealed clear ontogenetic dietary shifts (Fig. 4). T. pacificus smaller than 50 mm ML fed exclusively on crustaceans such as copepods (%IRI = 10%), amphipods (%IRI = 26%) and euphausiids (%IRI = 64%), and then shifted to a mixed diet of crustaceans (%IRI = 13–34%) and fish (%IRI = 26%) at 50–99 mm ML; after reaching 100 mm ML, fish (%IRI = 44%) were the most important prey items and crustaceans became less important (%IRI = 9–20%). 4. Discussion 4.1. Allometric growth and functional morphology Coefficients obtained by type II regression agreed with those obtained by type I results. In tentacle, the coefficient by type I regression was isometric, whereas the coefficient by type II indicated weak positive allometry. However, it was assumed that the growth rate of tentacle did not change during the size range examined, since the tentacle coefficient by type II was nearly 1 (Table 1; b = 1.043). Tentacles and arms are crucial organs for prey capture and handling in squid (Foyle and O’Dor, 1988; Kier and Van Leeuwen, 1997; Nicol and O’Dor, 1985; Packard, 1972). We did not found positive allometry and inflection points in the growths of AL and TL. In contrast to our result, some squid species have been reported to exhibit a strong positive allometry in the growth of tentacles and arms (Rodhouse and Piatkowski, 1995; Shea and Vecchione, 2002). The allometric growth pattern of tentacles and arms would reflect interspecific differences in feeding strategies, although there are few studies relating morphology and diet with

growth in squids. Interspecific differences in diets, together with the allometric growth of arms and tentacles, may allow us to develop hypotheses of trophic strategies among squids. In our results, only FBL and FW were positive allometric, which implies a functional reason to attain a large fin size quickly. Positive allometric growth in fins has been also reported in various squid species such as Chtenopteryx sicula, Mastigoteuthis magna, Gonatus madokai, Illex illecebrosus and Loligo opalescens (Kubodera and Okutani, 1977; O’Dor and Hoar, 2000; Perez and O’Dor, 2000; Shea and Vecchione, 2002; Zeidberg, 2004). In T. pacificus, both the FBL and FW indicated positive allometry, and the growth rate in the longitudinal axis (FBL) was much faster than the width. Araya (1967) reported that the fin shape of T. pacificus varies through ontogeny, changing from a circular to a triangular form. Squid employ a unique dual-mode locomotory system involving jet-propulsion and movement of the lateral fins (Bartol et al., 2008), but the rudimentary fins of paralarvae are thought to contribute little to the production of thrust (Boletzky, 1987; Hoar et al., 1994). Jet-and-sink swimming predominates among paralarval and juvenile squid (Bartol et al., 2008; Yamamoto et al., 2012). As squid grow, their motions transform to climb-and-glide swimming, in which fins contribute substantially to the generation to thrust (O’Dor, 1988; Zeidberg, 2004). Additionally, squid fins are thought to have multiple functions such as rudders, stabilizers, generating lift and undulatory propulsion (Hoar et al., 1994). This suggests that the positive allometry in fins of juvenile T. pacificus probably reflects the transition from jet-and-sink to climb-and-glide swimming. The positive allometric growth in fins continued throughout the size range examined. Thus, the growth pattern in fins may indicate the continuous improvement of the locomotive maneuverability during the juvenile stage. Four characters in head, head width, eye diameter, buccal mass and funnel aperture were negatively allometric. The negative allometry of eye diameter is contrary to expectation, because T. pacificus is thought to detect prey visually. It is also possible that the acquisition of decreasing drag imposes a selection on head, which favors a change toward a slender shape and relatively smaller size with growth. Consequently, growth of organs in the head may be constrained by the overall head size. It is important to remember that an increase in absolute size of organs also acts on predator–prey interactions, as larger muscles can produce more power for its performance. However, smaller size in funnel aperture

K. Uchikawa, H. Kidokoro / Fisheries Research 152 (2014) 29–36

33

Table 2 Diet of Todarodes pacificus, represented as percent number (%N), percent mass (%M), percent frequency of occurrence (%F) of prey items and IRI for major prey groups in the different size classes. Prey

Size range (mmML) <50 %N

Copepoda (total) Calanus pacificus Calanus spp. Mesocalanus tenuicornis Neocalanus plumchrus Neocalanus spp. Calanidae (unid.) Clausocalanus sp. Centropages bradyi Paraeuchaeta elongata P. russelli Euchaetidae (unid.) Candacia bipinnata Eucalanus bungii Eucalanidae (unid.) Paracalanus parvus s.l. Oncaea spp. Corycaeus spp. Calanoida (unid.) Copepoda (unid.) Ostracoda Discoconchoecia pseudodiscophora

26.7 – – – – – 6.7 – – – – – – – – – 3.3 6.7 – 10.0 –

Amphipoda (total) Primno abyssalis Themisto japonica Hyperiidea (unid.) Amphipoda (unid.) Euphausiacea (total) Euphausia pacifica E. pacifica furcilia Thysanoessa longipes Furcilia larvae (unid.) Calyptopis larvae (unid.) Euphausiacea (unid.) Decapoda (total) Megalopa larvae Zoea larvae Malacostraca (unid.) Crustacea (unid.)

50–99 %M

%F

IRI

%N

16.7 – – – – – 4.2 – – – – – – – – – 4.2 4.2 – 12.5

481.3

–

–

–

23.3 – 16.7 6.7 –

39.7 – 32.8 6.9 –

20.8 – 12.5 8.3 –

1312.3

30.0 3.3 – 6.7 – – 20.0

54.6 4.2 – 26.1 – – 24.3

37.5 4.2 – 8.3 – – 20.8

3171.3

– – –

– – –

– – –

– 16.7

2.2 – – – – – 0.1 – – – – – – – – – +

0.1 – 2.0

– 3.6

– 20.8

+

17.6 – 2.9 – – 11.8 – – – 2.9 – – 5.9 2.9

+

+

IRI

%N

888.1

2.9 5.9 2.9 2.9 –

+ + +

– +

%M 0.7 0.1 + +

0.1 – + + + + +

– 0.1 – + + + +

0.2 – +

2.9

4.7

0.3

502.3

20.7 2.3 18.2 – 0.3

18.4

1361.0

6.8 3.8 0.3 2.0 – 0.4 0.3

5.5 4.0

1.2 0.9 0.3

+

14.0 0.8 11.7 0.8 0.8

7.3 6.5 0.7 0.1

23.5 2.9 14.7 2.9 2.9

14.8 2.3 – 3.1 0.8 – 8.6

12.4 2.3 – 6.1 0.1 – 3.9

50.0 8.8 – 8.8 2.9 – 32.4

– – –

– – –

– – –

0.8 1.6

0.1 0.5

2.9 5.9

19.7 19.7 –

4.2 4.2 –

8.8 5.9 –

+

36.2 4.6 0.3 3.5 0.8 – 0.5 0.4 0.8 0.5 0.4 – 1.4 – 0.5 10.7 4.4 4.2 3.3 –

–

+

18.3 – +

+

1.2 – +

0.3 + +

+

%F

IRI

34.8 8.7 4.3 8.7 8.7 – 4.3 4.3 4.3 4.3 4.3 – 13.0 – 4.3 17.4 13.0 26.1 13.0 –

1280.1

4.3

1.1

39.1 4.3 34.8 – 4.3

1530.8

52.2 30.4 4.3 21.7 – 4.3 4.3

642.6

13.0 8.7 4.3

15.2

0.3 0.3

0.4

4.3 4.3

211.5

27.6 25.0 2.6

1.3 1.2 0.1

21.7 13.0 8.7

628.7

3.3 – 3.3

–

Osteichthyes (total) Maurolicus japonicus Osteichthyes (unid.)

– – –

– – –

– – –

–

3.9 2.3 1.6

67.2 60.5 6.7

14.7 8.8 5.9

1045.3

4.2 3.5 0.8

72.0 66.5 5.5

43.5 30.4 13.0

3313.7

Cephalopoda Decapod cephalopoda

–

–

–

–

0.8

0.7

2.9

4.4

2.6

1.7

17.4

92.8

+

+

13.9

1.6

%F

7.5 – 0.5 – – 1.5 – – – 3.9 – – 1.5

Chaetognatha (total) Sagitta elegans Chaetognatha (unid.)

N. of unidentified material N. of empty digestive tracts N. of specimens examined

4.2 – 4.2

%M

42.9 – 2.3 – – 10.9 – – – 14.8 – – 8.6 0.8 0.8 1.6 1.6 1.6 –

–

100–150

28 13 61

14 3 51

2 0 23

<0.05.

is probably more functional. This is because the funnel aperture can force a larger volume of water faster through a tighter hole with higher pressures when the squid develops greater mantlecontracting abilities (Zeidberg, 2004). Three of nine characters, each of mantle diameter, head width and eye diameter had an inflection point (between 53 and 72 mm ML) over the size range examined. These inflection points may indicate that energy allocation to the organs changed at the inflection points. Although the allometric coefficients were still negative, the relative growth of the three characters increased more rapidly after the inflection points. In other words, mantle elongated at a much

faster rate before pre-inflection points compared to these characters. The relative allocation to mantle can be viewed as a transitional phase between paralarvae and adult shape. As squid grow, they move from a viscous to an inertiadominated fluid system. The former is favorable to a shape that minimizes surface area (i.e., a rounded, globular shape), and the latter is favorable to a streamlined shape (O’Dor and Hoar, 2000). During the jet-propulsion, squid suck water into the mantle cavity and then expel it under high pressure through the funnel. In this system, squid face antagonistic demands to obtain more powerful propulsion, with the need for larger water reservoirs in the

34

1.9 1.8 Log FW

1.7

mantle cavities for jetting and the need for a more streamlined body to decrease the drag. Elongated mantle is a trade-off between the two demands. Evidence has been provided that there is an obvious trade-off between increasing the mantle water volumes and decreasing the drag (e.g., O’Dor and Hoar, 2000). The negative allometry of mantle diameter against mantle length in T. pacificus also appeared to be influenced by the trade-off related to swimming performance.

0.15

2

0.10 Residual

a

K. Uchikawa, H. Kidokoro / Fisheries Research 152 (2014) 29–36

0.05 0.00 -0.05 -0.10

1.6

1

1.2

1.4 1.6 Estimate

1.8

2

1.5 1.4

4.2. Dietary shift and morphology

1.3

We found clear dietary shifts with ontogeny in T. pacificus. Smaller squids fed mainly on crustaceans, whereas larger ones shifted toward fish-based diets. We could not measured the prey size, but it was assumed that the maximum prey size in the two larger size classes is several times larger than that of the small size class. For example, maximum size of M. japonicus (a representative fish prey) is 60 mm in length (Yuuki, 1984), while a largest crustacean prey, Thysanoessa longipes is 22–30 mm (Baker et al., 1990). It is expected that the timing of the dietary shifts are consistent with morphological changes. We have demonstrated that, as T. pacificus grew in size, they exhibited an elongated and narrowed body and fins, and relatively smaller head. These changes in body morphology indicate that as the squid grow they attain a shape that favors higher performance in swimming. Also, the inflection points might be a signal of the approaching the adult shape. The range of inflection points (53–72 mm ML) is consistent with size at which T. pacificus starts to feed on fish. In contrast, tentacle and arm III showed slower relative growth rates and had no inflection points. Therefore, dietary shift with ontogeny of T. pacificus is closely related to the ontogenetic change in swimming performance rather than improvements of prey capture and handling abilities. In comparison with zooplanktivory, piscivory may be subjected to high acceleration, swimming speed and/or high maneuverability. Distinct predatory modes are therefore expected between feeding on zooplankton and fish. It has been reported that adult I. illecebrosus showed different feeding strategies depending on prey size (Foyle and O’Dor, 1988; Nicol and O’Dor, 1985). However, success in capturing large fish is not only due to high swimming performance, but also superior tactics of the squid (Foyle and O’Dor, 1988). Nevertheless, the improvement of swimming performance during development is important for aquatic predators to capture larger prey, since the upper limit of prey size is set by physical constraints of the predator, such as the size of the feeding apparatus and swimming capacity (Christensen, 1996; Lundvall et al., 1999). Predator and prey sizes can affect predator capacity at one or several levels of search, pursuit, attack, handling and ingestion phase of the foraging cycle. In adult I. illecebrosus, the prey pursuit behavior differs depending on whether the fish prey is large or small (Foyle and O’Dor, 1988). As I. illecebrosus approaches a large fish, the squid begins to track the fish decreasing its velocity and slowly closing the distance separating them (termed as “tracking phase”). On the contrary, the squid pursues a small fish with no tracking phase. Foyle and O’Dor (1988) suggest that squid must track the large prey due to the poor performance of their head-first attack when feeding on large prey. It is therefore suggested that acquisition of ability related to the pursuit component of the cycle is most important for juvenile squid to capture fish. Prey pursuit can be assumed to require some degree of accurate maneuvering and swimming speed by the predator. We thus propose that a critical locomotive threshold was reached at about 53–72 mm ML (inflection points) that enabled sufficient swimming capability to allow the T. pacificus to capture more mobile, larger prey. Our results show that morphology is closely related to feeding habits through the influence of behavioral performance. Growth

1.2 1.1 1 0.9 1.3 1.4 1.5 1.6 1.7 1.8 1.9 Log ML

1.9

Log MD

1.8 1.7

2.1 2.2 2.3

2

2.1 2.2 2.3

0.15

2

0.10 Residual

b

2

0.05 0.00 -0.05 -0.10 -0.15 1.3 1.4 1.5 1.6 1.7 1.8 1.9 Estimate

1.6 1.5 1.4 1.3 1.3 1.4 1.5 1.6 1.7 1.8 1.9 Log ML

Fig. 3. (a) Example of the piecewise linear regression method for fin width (FW) with no inflection point. The upper left of panel shows the residuals are not patterned (see text) and (b) the piecewise linear regression method for mantle diameter (MD) with an inflection point. The upper left of panel shows the residuals are patterned.

Fig. 4. Ontogenetic variation in the diets of Todarodes pacificus represented as %IRI composition for the prey major groups.

K. Uchikawa, H. Kidokoro / Fisheries Research 152 (2014) 29–36

toward the enlargement of fin and elongation of mantle may reflect selective advantage in the acquisition of locomotive maneuverability, faster and more efficient swimming. It is likely that additional inflection points occur as the squid grow to full size, since adult T. pacificus commonly attains 200–300 mm ML (Roper et al., 2010). Furthermore, we considered the length of characters only, but the mass of characters may be required to obtain more robust estimates because the use of mass can be seen as an indication of the investment of resources distributed to each body parts during growth. Therefore, the functional mechanisms behind the relationships are not fully understood and require further investigation.

Acknowledgments The authors are grateful to T. Fujino for his help in sample collection, captains and crews of “Mizuho-Maru” and “ShunyoMaru” for their assistance at sea. Thanks are due to Y. Sogawa for helping to measure the morphological characteristics of the squid. We also wish to thank H. Morimoto and T. Takahashi for providing zooplankton information and collection. This study was partly supported by the Japanese Ministry of Agriculture, Forestry and Fisheries.

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