Phuhet Marine Biological Center Special Publication 21(1): 103-112 (2000) 103

BEIIAVIOLIR OF JIwENILE CEPIIALOPODS: PREFERENCE FOR TEXTI,]RE AI\D BRIGIITNESS OF SI.]BSTRA. TA

Jaruwat Nabhitabhata & Pitiporn Nilaphat

Rayong Coastal Aquaculture Station, Ta-pong, Changwat Rayong 2100, Thailand.

ABSTRACT strata is referred to as epipsammon (on Behavioural preference for different types and sand) or epipelos (on mud). An important levels of brightness of substrata was studied in property for the inhabiting is the cultured, juvenile sepiid , Sepia suitability to move upon and to burrow in pharaonis and inermis. Sand, muddy the soft substrata. Substrata affect metabo- sand and mud represented types ofbenthic sub- lism and activity of the animals via their stratum. Both species ofcuttlefish preferred sand physico-chemical properties, particularly to mud in long term studies (24 hrs). White, grey and black plastic plates were used as substrata their resistance to activities such as representing high, medium and low levels of Iocomotion, respiratory ventilation, and bur- brightness. The cuttlefish preferred medium level rowing in benthic . Exposure ofbrightness during the early phase (up to 3 hrs) and water movement influences properties of the experiment. The degree of preference for of soft substrata. Therefore, habitat selec- substratum was higher in Sepia, living in the tion of aquatic animals is essentially the re- open sea, compared to the estuafine Sepiella. Iationship between behaviour and environ- Cuttlefish selected substrata in relation to ben- ment (Meadows & Campbell 1972). The ani- efrts, which we suggest are facilitated respira- mals are not able to differentiate between tion, crypsis, and energy conservation. Cultured bigfin , Sepioteuthis lessoniana, was stud- every variable they encounter in their erivi- ied as an outgroup on preference for brightness ronment. Meadows & Campbell(L972) corn- ofsubstrata. The bigfrn squid preferred medium mented that few animals are known to show level ofbrightness during the first 6 hrs and then lack of preferences. The preference may al- gradually changed to prefer low level of bright- ter depending upon physiological state as ness at night. We suggest that preference for well as previous experience and learning. brightness is associated with visual discrimina- The behavioural preference of individuals performing in- tion of depth in the pelagic squid may vary in rather unexpected ways but nate diurnal migration to greater depth. The preference species recognisable present results should be applied to painting of a has a culture tanks in order to reduce pattern. Closely related species living in the stress, promote grou'th and enhance the contrast same environment have different habitat of feed. preferences but changes in physiolory asso- ciated with preference are very little known. INTRODUCTION Cephalopods lie, burrow and attach to sub- The term "substratum" refers to structures strata. Hence, the type ofsubstratum affects to which organisms in question maintain, the behaviour of cephalopods in several temporarily or permanently, a close contact ways, e.g. in ritualised behaviour, in am- and does not include aquatic or nutritive bushing, and sheltering (crypsis, camou- media (Gerlach 1972). Animals may move flage). Most cephalopods can adjust the ap- on, o attach to the surface ofsolid substrata pearance of their bodies to match different called epilithion. The surface of soft sub- substrata. Female cephalopods attach their 704 Tlopical Marine Mollusc Programme (TMMP) egg capsules to various types of substrata; countering any types of soft substrata in sponge, coral, seaweed, and rock. The Thai order to avoid learning behaviour. pygmy squid, Idiosepius thq.ilondicus, ad- The bottom ofeach glass aquarium (35 x heres to seaweed fronds in ritualised behav- 60 x 36 cm) was divided into 3 sections. Each iour, in mating behaviour, and for transpor- section was randomly spread with one of the tation when the seaweed turns into a float- three types of substrata, sand, sandy mud ing substratum (Nabhitabhata 1998). and mud. One glass aquarium represented The eyes ofcephalopods are excellent and one replicate. The soft substrata had been have a structure and function comparable collected from Changwat Rayong, Thailand. to those of higher vertebrates, but The sandy mud was a mixture of collected cephalopods are colour-blind (Messenger ef sand and mud at the ratio of 1:1 by volume. aL.1973, Roffe 1975, Messenger 1977, Flores The trial consisted of 8 tests, each with 3 et al. 7978). However, they able to distin- replicates (24 replicates in total) for spine- guish the level of brightness (Messenger & less cuttlefish. For the pharaoh cuttlefish, Sanders 7972) and,the plane ofpolarisation the trial consisted of2 tests, one test with 3 of the substrata and other objects (Wells replicates and another with 2 replicates (5 1966). The retina of the cephalopod eye may replicates in total). Ten cuttlefish were re- possess a system for detection ofwavelength leased into one aquarium (replicate) and (Messenger et al. 7973). Different colours then the numbers of lying and burrowing appear as different degrees of brightness cuttlefrsh on each type of substratum were contrasting against the surrounding back- counted and the behaviour were observed. ground on a grey scale. Messenger & Sand- The observation from initial time lapse was ers (1972) reported that the eyes of at 0.05,0.15, 0.30, 0.45, 1.00, 1.30,2.00, 3.00, uulgaris were able to discriminate bright- 6.00, 9.00, 12.00, 18.00 and 24.00 hrs. The ness better than orientation ofshapes. Young time interval was 5, 10, 15, 15, 30, 60, 180, (1968) found that octopus tended to attack 180, 360 and 360 min respectively. Signifi- black objects more often than white ones if cance was tested by chi-square test at 95 Vo appearing against a white background. Such (P < 0.05) and at 99 7o (P < 0.01) for each difference was not present with a grey back- observation of the test. grou.nd. The appearance ofthe objects to the During the tests, water parameters were cephalopod eyes partly depends on the con- monitored every 6 hours. Water tempera- trast ofthe object against the surrounding ture, pH and salinity were determined by background. mercury thermometer, pH meter (HANNA electric paper) and refractometer (ATAGO MATERIALS AND METHODS S-10) respectively. Average temperature re- Soft substrata (terture) corded was 28.2 + 0.6 oC, average pH was The experimental cuttlefish were reared 8.0 t 0.1 and average salinity was 30 + 2 from hatchling tojuvenile at the age ofabout ppt. 30 days. The average size of the pharaoh cuttlefis[ Sepia pharaonis,was 3.68 t 0.33 Solid s ub strata ( b rightnes s) cm in mantle length and 8.67 + 2.79 g in The experimental cephalopods were reared weight. The average size of the spineless from hatchling to juvenile at the age of about cuttlefrsh, Sepiella inerrnis,was3.22 t 0.16 20 days. The rearing methods followed cm in length and 6.53 + 0.85 g in weight. Nabhitabhata (1978a,1996) for the bigfin The rearing method foliowed Nabhitabhata squid, Sepioteuthis lessoniana, and as pre- (1978b) and Nabhitabhata et al. (1984) re- viously mentioned for the other two species spectively. The animals were reared in con- of cuttlefish. The pelagic bigfrn were crete tanks and had no experience on en- tested as an outgroup for comparison. The Phuhet Marine Biological Center Special Publication 21(1): 103-112 (20OO) 105

rearing tanks were painted sky-blue consid- licates for each species ofcephalopod. In each ered as neutral brightness in order to avoid replicate, the animals used were 24 pharao learning behaviour. The average size ofthe cuttlefish, 9 spineless cuttlefish, and 12 bigtin squids was 1.75 t 0.15 cm in mantle bigfin squids respectively. Other details as length and 1.20 t 0.34 g in weight. The av- well as water quality were the same as men- erage size of the pharaoh cuttlefish was 0.85 tioned for soft substrata. + 0.06 cm in length and 0.45 + 0.11 g in weight and of the spineless cuttlefish was RESULTS 1.35 t 0.18 cm, 0.85 t 0.27 g. Tnxr:uno oF sUBSTRATUM The bottom of each glass aquarium (35 x (sorr suesrRArA.) 60 x 36 cm) was divided into 3 sections. Each section was randomly spread with one of the Pharaoh cuttlefish, Sepia pharaonis three plastic plates ofwhite, grey or black Preference for mud dominated signifrcantly in colour representing the high, medium and over other substrata (P < 0.05) in the first low level of brightness respectively. One 15 minutes (Table 1) but after that the de- aquarium represented one replicate for the gtee ofpreference decreased to non signifi- cuttlefish test. The test for bigfrn squid was cant difference until 1.30 hrs (P > 0.10-0.35). held in circular concrete tanks of 1.50 m di- The preference increased to significant dif- ameter with 60 cm water depth. One tank ference again (P < 0.025) until 3.00 hrs. In represented one replicate for the squid test. nighttime through the daytime of the next Plastic plates of the three colours were ran- day (24.00 hrs), the preference for sand and domly and in equal numbers spread on the mud were not different (P > 0.05) but sig- tank bottom. nificantly different (P < 0.05) from sandy The trial consisted of one test with 3 rep- mud substratum. The highest degree of pref-

Table 1. Pharaoh cuttlefish, Sepia pharaonls. Test ofpreference on type ofsubstratum. There were 50 individuals in this trial. N = the number ofcuttlefish lying on substrata (swimming cuttlefrsh were excluded). *, x* indicate signifrcant difference (P < 0.05, 0.01) respectively; a,b,c indicate significant range difference (P < 0.05) as different consonants; n = nighttime; ns = non significant difference 1P > 0.05); x = maximum frgure.

Time Time Brightness preference ratio N chi2 P lapse ofday (hr) (hr) high medium low 00.05 t2.05 1.0. 0.5. 2.5r x 16 6.50* <0.05 00.15 12.75 1.0.b 0.3b 1.6u x 20 6.10* <0.05 00.30 12.30 1.0 0.8 1.8 x 22 2.82 ns > 0.10 00.45 t2.45 l-.0 0.5 1.4 x 23 3.22ns > 0.10 01.00 13.00 1.0 0.3 1.1 x 22 3.91 ns > 0.10 01.30 13.30 1.0 0.4 \.2 x 24 2.25 ns > 0.25 02.00 14.00 l-.0. 0.6. 2.2h x 31 8.98* <0.025 03.00 15.00 1.0ub O.4" 2.0b x 37 13.35 ** < 0.005 06.00 n 18.00 1.0'x 0.2b 0.8' 38 9.52 ** < 0.01 09.00 n 21.00 1.0u x 0.1b 0.7" 20 7.89* <0.025 12.00 n 00.00 1.0'x 0.2b 0.7u 34 10.32 'k* < 0.01 18.00 n 06.00 1.0 0.5 1.1 x 26 2.39 ns > 0.025 24.00 12.00 1.0u x 0.2b 0.8' 42 g.5g ** < 0.01 (TMMP) 106 Tlopical Marine Mollusc Programm.e

Table2. Spinelesscuttlefish,Sepiellainermis.Testofpreferenceontypeof substratum. There were 240 individuals in this trial. N = the number of cuttlefish lying on substrata (swimming cuttlefish were excluded). ** indicate signifrcant difference (P < 0.05); a,b indicate signifrcant range difference (P < 0.05) as different consonants; n = nighttime; ns = non significant difference (P > 0.05); x = maximum figure.

Time Time Brightness preference ratio N chi2 P lapse ofday (hr) (hr) high medium Iow 00.05 72.05 1.0 1.1 x 0.8 195 3.82 ns > 0.10 00.15 72.L5 1.0 1.1 x 1.0 2O8 0.30 ns > 0.75 00.30 12.30 1.0 x 1.0 x 0.9 214 O.24 ns > 0.75 00.45 12.45 1.0 x 0.9 1.0 x 219 0.73 ns > 0.50 01.00 13.00 1.0 x 0.9 1.0 x 222 0.66 ns > 0.50 01.30 13.30 1.0 x 0.8 0.9 2Lg 1.34 ns > 0.50 02.00 14.00 1.0 x 0.8 0.9 226 2.46 ns > O.25 03.00 15.00 1.0 x 0.8 0.9 225 1.78 ns > 0.25 06.00 n 18.00 1.0 x 0.9 0.8 145 1.25 ns > 0.50 09.00 n 21.00 1.0 x 0.6 0.7 179 7.12 ns > 0.025 12.00 n 00.00 1.0 x 0.7 0.8 187 5.46 ns > 0.05 18.00 n 06.00 1.0 x 0.7 0.8 213 4.42ns > 0.10 24.00 12.00 L.0'x 0.5b 0.5b 231 31.28 ** < 0.005

Table 3. Pharaoh cuttlefish, Sepia pharaonis. Test ofpreference on type ofsubstratum. There were 72 individuals in this trial. N = the number ofcuttlefrsh lying on substrata (swimming cuttlefish were excluded). ** indicate significant difference (P < 0.05); a,b indicate significant range difference (P < 0.05) as different consonants; n = nighttime; ns = non significant difference 1t > 0.05); x = maximum figure.

Time Time Brightness preference ratio chi2 P lapse ofday (hr) (hr) high medium Iow 00.05 t2.05 1.0' 2.0" x I.4" 22 1.73 ns > 0.25 00.15 12.15 1.0" 1.2" x 0.9. 28 0.50 ns > 0.75 00.30 L2.30 1.0. 1.6u x 1.0* 39 1.85 ns > 0.25 00.45 12.45 1.0' L.4" x 0.7" 37 3.30 ns > 0.10 01.00 13.00 1.0. 1.6'x 0.9' 39 2.92 ns > 0.10 01.30 13.30 1.0' 3.3b x O.4" 43 26.56 ** < 0.005 02.00 14.00 1.0 x 1.2" x 0.8' 58 1.69 ns > O.25 03.00 15.00 1.0^ x 0.9' 0.8. 50 0.40 ns > O.75 06.00 n 18.00 1.0. t.2" x 0.4b 63 9.24 ** < 0.01 09.00 n 21.00 1.0'x 1.0'x 0.2b 42 10.71 ** < 0.005 12.00 n 00.00 1.0. I.2" x 0.7" 50 2.44 ns > 0.25 18.00 n 06.00 1.0. 1.1 0.6' 56 3.68 ns > 0.10 24.00 12.00 1.0. L.4" x 0.4b 59 12.44 ** < 0.005 Phuhet Marine Biological Center Specia.I Publication 21(1): 103-112 (2000) 107

Table 4. Spineless cuttlefish, . Test of preference on brightness of substratum. There were 27 indiyiduals in this trial. N = the number of cuttlefish lying on substrata (swimming cuttlefish were excluded). n = nighttime; ns = non sigrrifrcant difference (P > 0.05); x = maximum frgure.

Time Time Brightness preference ratio N chi2 P lapse ofday (hr) (hr) high medium low 00.05 12.05 1.0 1.5 x 0.0 5 1.12 ns > 0.50 00.15 t2.75 1.0 2.5 x 0.5 8 3.25 ns > 0.10 00.30 12.30 1.0 x L.2 x 0.5 16 1.63 ns > 0.25 00.45 t2.45 1.0 1.0 x 0.5 15 1.20 ns > 0.50 01.00 13.00 1.0 1.8 x 1.0 15 1.20 ns > 0.50 01.30 13.30 1.0 1.6 x 0.8 77 1.53 ns > 0.25 02.00 14.00 1.0 1.6 x 1.0 18 1.00 ns > 0.50 03.00 15.00 1.0 x 1.0 x 0.6 13 0.62 ns > 0.50 06.00 n 18.00 1.0 x 1.0 x 0.4 19 2.63 ns > 0.25 09.00 n 21.00 1.0 1.3 x 1.0 20 0.40 ns > 0.75 12.00 n 00.00 1.0 1.1 x 0.8 21 0.29 ns > 0.75 18.00 n 06.00 1.0 1.5 x 0.7 19 2.00 ns > 0.25 24.00 12.00 1.0 x 0.9 0.6 20 0.70 ns > 0.50

Table 5. Bigfin squid, Sepioteuthis lessoniana. Test of preference on brightness of substratum. There were 36 individuals in this trial. N = the number of squid lying on substrata (swimming squid were excluded). a,b indicate significant range difference (P < 0.05) as different consonants; n = nighttime; ns = non significant difference (P > 0.05); x = maximum fig'ure.

Time Time Brightness preference ratio chi2 lapse ofday (hr) (hr) hiSh medium low 00.05 L2.05 1.0. 11.0t x 6.0b 36 16.67** < 0.01 00.15 t2.15 1.0. 12.0b x 5.0" 36 20.67** < 0.01- 00.30 12.30 1.0. 26.0b x 9.0" 36 27.17** < 0.01 00.45 12.45 1.0u 8.0b x 3.0u 36 19.50** < 0.01 01.00 13.00 1.0u 4.6b x 1.8, 36 15.50** < 0.01 01.30 13.30 l-.0* 8.7b x 2.3" 36 25.L7** < 0.01 02.00 14.00 1.0u 4.8b x t.4" 36 18.17** < 0.01 03.00 15.00 1.0. 5.4b x 0.8" 36 29.17** < 0.01 06.00 n 18.00 1.0. 4.0b 7.0b x 36 13.50** < 0.01 09.00 n 21.00 1.0' L.4" 1.6" x 36 1.17 ns > 0.50 12.00 n 00.00 1.0'x 0.9' 0.6. 36 1.17 ns > 0.50 18.00 n 06.00 1.0. L.4" 2.L" x 36 3.50 ns < 0.10 24.00 12.00 1.0. I.7" 9.3'x 36 32.L7** < 0.01 (TMMP) 108 Tlopical Marine Mollusc Programrne erence during that period had shifted from the medium level of brightness and equal to mud to sand type. The exception was at preference for high brightness (at 3.00 and dawn (18.00 hrs) where the preference was 6.00 hrs). The exception was at 24.00 hrs not significantly different (P > 0.025) and where the highest degree of preference was the highest preference shifted to mud type. for high brightness. The degree ofpreference The degree of preference for sand and mud was comparatively higher for high bright- was higher than for sandy mud throughout ness than for low brightness. the test period. Bigfin squid, Sepioteuthis lessonianq, Spineless cuttlefish, Sepiella inermis The degree of preference for the medium The highest degree of preference shifted level of brightness was highest with high from sandy mud substrata at the first 30 min significance after the frrst 5 min (0.05 hr, P (0.30 hr) to sand type afterward (Table 2). < 0.01) to 3.00 hr (Table 5). Medium to low However, at 0.45 and 1.00 hr the degree of brightness were not differently preferred (P sand preference was equal to of mud prefer- > 0.05) by the squids at 0.05 hr and at 6.00 ence. The preference for type ofsubstratum hrs (at dusk). At night, the highest degree was not significantly different (P > 0.05). At of preference shifted from medium to low 24.00 hrs, the preference for sand was sig- Ievel of brightness except aL 12.00 hrs but nificantly different from mud and sandy the difference was not significant (P > 0.10). mud (P < 0.05). The preference for the lat- The change to low brightness preference at ter two substrata was not different (P > the highest degree was at 24.00 hrs with 0.05). From 1.30 hrs, the degree of prefer- high significance (P < 0.01). The preference ence for mud was always higher than or for high and medium brightness was not equal to sandy mud except at dusk, 6.00 and different at that time (P > 0.05). 9.00 hrs. DISCUSSION Bucnrxpss oF SUBSTRATUM Brightness of substratum (solro sussrnAre) Young (1968) reported that octopus, Octo- pus uulgari.s, showed preference for black or Pharaoh cuttlefrsh, Sepia pharaonis white objects (low andhighbrightness). The The degree ofpreference was highest for the preference varied with the brightness level medium level of brightness (Table 3). How- of the objects as well as the colour of back- ever, the difference was not significant (P > ground. In a white tank (high brightness 0.05) most of the time except at 1.30 hrs, at background), the octopus attacked black dusk 6.00-9.00 hrs, and 24.00 hrs (P < 0.01). objects (Iow brightness) more often than the During the exception period, preference for white. The mean was 44 Vo for white prefer- the medium level of brightness was not dif- ence. In grey tanks (medium brightness ferent (P > 0.05) from preference for the high background), the preference for white was Ievel but significantly different from low 56 Vo.The effrciency of discriminability was brightness (P < 0.05). The degree ofprefer- related to the level of contrast between the ence was comparatively higher on the high object and background. The probability of than on the low brightness. an attack on a particular shape might be further influenced by its brightness insofar Spineless cuttlefrsh, Sepiella inerrnis as brightness affected the discriminability The preference for brightness was not sig- ofthe shape from the background (Sanders nificantly different (P > 0.10) at any experi- 1975). Bradley & Messenger (1977) reported mental time (Table 4). The highest degree that Octopus uulgaris made significant at- ofdifference was observed at preference for tacks on rectangular test objects whose Phuket Marine Biological Center Special Publication 21,(1): 103-112 (2000) 109

brightness contrasted with that of the back- capability since mud should make the sur- ground. They suggested that the octopus did rounding water turbid during burrowing, not have an intrinsic brightness preference which involved rapid movement of both fins and the so-called preference was merely a and strong water jetting. The muddy turbid function of the background or substratum water also disturbed respiration since the brightness. cephalopod gills lack cilia for removing sedi- The present study revealed a tendency of ment. Sand was weII and continuously oxy- intrinsic preference for brightness of sub- genated by current (Bacescu 1972)being a stratum in both species of cuttlefrsh, con- good habitat for respiration-ventilation dur- sidered from overall consistency or stability ing burrowing. Although the sand substra- of the preference through the experimental tum might have excess brightness in pri- period. The pelagic bigfin squid tended to mary sensingbythe cuttlefish, the situation react in a different pattern. The preference should have turned into the advantage of for low brightness after dark was interpreted excess reflection to interspecific vision (ei- as innate migration to greater depth. Hence, ther predator or prey) after complete bur- the brightness of substrata might be associ- rowing. ated with visual discrimination of depth by Preference for medium brightness of the the squid. Moreover, the degree of prefer- spineless cuttlefrsh, Sepiella inermis, was ence for low brightness that lowered to non- not prominent since the preference was signifrcant difference (P > 0.10-0.50) during without significance (P > 0.10-0.75). Prefer- the nighttime and might relate to photop- ence rvas also low compared to pharaoh cut- ositive taxis behaviour in low light environ- tlefish. This pattern might reveal another ment, i.e. diurnal migration (Nabhitabhata view on lesser dependence on benthic sub- 1978b). Moynihan & Rodaniche (1985) also strata of this species compared to the open reported the same pattern of behaviour in seaSepiapharaonis. The preference for sub- the juvenile Caribbean bigfin squid, strata ofthe spineless cuttlefish should be Sepioteuthis sepioid.ea. The squids congre- added as a character of this species to be- gate in shallow water during the daytime haviour reported by Nabhitabhata (1997). and migrate offshore to deeper water at The habitat of this species is estuaries where night. They also came to ship lights at night current velocity and water turbidity are apparently rising from below (photopositive high. The level of underwater brightness in taxis in low light environment). turbid water is comparatively lower than in From the view oflevel ofbrightness, the clearer water ofthe open sea. So the prefer- sand, sandy mud and mud firpes of substra- ence could obviously not be an advantage in tum should, at a certain level, be compara- terms of camouflaging or crypsis. On the ble to high, medium and low level of bright- other hand, the preference for sand ofthis ness respectively. The sand preference ofthe species seemed to be opposite to its natural cuttlefish should have been interpreted as habitat, muddy estuary.' Nabhitabhata & high brightness preference, but the medium Polkhan (1983) and Nabhitabhata (1997) brightness was preferred during the bright- suggested that there might be two groups ness tests. Therefore, the preference behav- (populations?) of the spineiess cuttlefish. iour should vary as a function of physical One group was an estuarine population properties of the substrata as well as the (with mud preference) and another group brightness. Holmes (1955) and Boucaud- was an open sea population (with sand pref- Camou & Boismery (1991) reported that erence). sand substratum was the usual habitat of Sepia officinalis. The sand substratum was Physiology preferred obviously on basis of burrowing Habitat selection is essentially the relation- Programme (TMMP) 110 T?opical Marine Mollusc ship between behaviour and environment ement consumes energy since the (Meadows & Campbell1972).In an overall cephalopod chromatophores are complex "or- view, the selection sequences of preference gans" and part of the muscular systems. for substratum ofthe cuttlefish, on basis of Each chromatophore organ comprises an the physical properties of the substrata, elastic sacculus containing pigment gran- should fall in four categories: Iying capabil- ules surrounded by a series ofabout 15-25 ity, burrowing capability, respiration, and radial muscles (Hanlon & Messenger 1996). enerry conservation. On soft substrata (sand In cryptic dark patterning on low brightness and mud), both types of substratum offered substratum, the muscles contract and the capability for lying and burrowing. The sand sacculus is greatly expanded. In white was the better choice because of being com- patterning on high brightness substratum, pact for lying and creating less turbidity dis- the muscles relax and the energy stored in turbing the respiration-ventilation while the sacculus cause it to retract. burrowing. On the other hand, burrowing Overall, the cryptic activities consume in softer mud consumed less energy com- energy in an order reversed to the level of pared to burrowing in sand. In the mean- brightness: The higher the brightness the time, higher turbidity disturbed the respi- lesser the energy consumed. The preference ration. The preference for sand revealed that by cuttlefrsh for sand with high brightness the selection depended on respiration capa- should also be reasonable seen from this bility hence, physiology. This would be in point of view. Since the preference outcome accordance with Meadows & Campbell was medium brightness, there might have (1972) who stated that habitat preference been a compromise involved between risk of aquatic invertebrates depended upon of exposure and energy consumption in the physiological benefrts. cryptic process as well as the consequent stress. Crypsis In conclusion, the strategy of preference On solid substrata where burrowing could for substrata should depend on physical not be performed, colour selection should properties of the substrata at the first en- reveal capability for crypsis or camouflag- counter. On soft substrata where burrowing, ing instead. The capabilities for lying and and nearly complete c4rysis was feasible, the respiration were not different. For the cut- uninterrupted respiration was the point for tlefish, the possibility for crypsis on low the selection. On solid substrata where bur- brightness ofsubstratum would have been rowing was not feasible and the life was at the best choice. Cuttlefrsh would obtain the risk because ofa higher degree ofexposure, lowest degree of exposure by the lowest con- there should be a compromise between ca- trast between the animals and background. pability of crypsis and chronic energT con- In the meantime, crypsis is a process, sumption required by the crS,ptic component. which certainly consumes energy, and may cause chronic stress and lower growth. Ap p lic atio n in aquac ulture Nabhitabhata & Nilaphat (1999) suggested The present study should be applied in aqua- that no substratum was necessary for nor- culture for colouring or painting ofconcrete mal growth of cultured Sepia pharaonisbtft culture tanks. The purposes are to promote Iack of proper substrata might be involved, growth as weII as to reduce stress. This will to some degree, in a small final size of the yield good health of the animals in the long cuttlefish. The cryptic process involves a term. La Roe (1971) suggested that culture chronic body-patterning component that is tanks of the Caribbean bigfin squids, a combination of chromatic texture, posture Sepioteuthis sepioidea, should be coloured and locomotion elements. The chromatic el- dark and substrata should be present, such Phuket Marine Biological Center Special Publication 21(1): 103-112 (2000) 111

as grass, coral, rocks or rubble, which ex- Boucaud-Camou, E. & J. Boismery. 1991. The erted a calming influence. Matsumoto & migrations of the cuttlefrsh (Sepjo officinalis Shimada (1980) painted a net pattern in L) in the English Channel. Pages 179-189 in: black on the tank walls in order to reduce Boucaud-Camou, E. (ed.). The Cuttlefrsh, First International Symposium on the Cuttlefish skin damage after tank collision of the squid, Sepia. Centue de Publications de I'Universite Doryteuthis bleekeri. Hulet et (1979) al. and de Caen, Caen,358 pp. (1983) Hanlon et aL also used tanks with Bradley, E. A. & J.B. Messengen 1977. Bright- various colour patterns on the walls made ness preference in Octopus as a function ofthe with black paint in order to increase con- background brightness. - Marine Behaviour trast and make the walls more visible to the and Physiolo gy, 4: 243-251. squids, Loligo plei, L. pealei and Flores, E. E. C., S. Igarashi & T. Mikami. 1978. Lolliguncula breuis. The contrast and vis- Studies on squid behaviour in relation to fish- ibility of tank walls seemed to be more nec- ing. III On the optomotor response of squid, Todarodes pacificus essary to pelagic fast moving squids than Steenstrup, to various colors. - Bulletin of Faculty of Fisheries, benthic However, men- cuttleflsh. these Hokkaido University, 29(2): L3L-140. tioned techniques might not be suitable for Gerlach, S. A. 1972. Substratum. General intro- tanks used for various purposes. duction. Pages t245-1250 in'. Kinne, O. (ed.). Flores et al. (1978), Sirisaksophon et al. Marine Ecology A Comprehensive Integrated (1995) studied the response behaviour ofthe Treatise on Life in Oceans and CoastalWaters squid, Todarodes pacificus, to different Vol. I Environmental Factors Part 3. Wiley brightness ofobiects and substrata in order Interscience, London. to apply the findings for squid fishing where Hanlon, R. T. & J. B. Messenger. 1-996. contrast of the jig (feed-prey) against the Cephalopod Behaviour. Cambridge University Press, Cambridge, 232 pp. surrounding water was required. They re- Hanlon, R. T., R. F. Hixon & W. H. Hulet. 1"983. ported that the contrast threshold of the Survival, growth, and behavior of the loliginid squids was far better than of fish. Yang ef squids Loligo plei, Loligo pealei and. al. (1983) used tanks painted black to en- Lolliguncula breuis (: Cephalopoda) in hance detection ofthe translucent prey or- closed sea water systems. - Biological Bune- ganisms for the squid, Loligo opalescens. tin, 1,65: 637-685. Feedingthe cultured cephalopods with dead Holmes, W. 1955. The colour changes of - and artifrcial feed increased the importance cephalopods. Endeavour, 74: 58-62. of proper painting of the culture tanks by Hulet, W.H., M. R. Villoch, R. F. Hixon & R. T. Hanlon. 1979. Fin damage in captured and enhancing the contrast for visual attraction reared squids. - LaboratoryAnimal Science,29: in the same manner. Both objectives, stress 528-533. reduction with growth promotion and en- LaRoe, E. T. 1971. The culture and maintenance hancing contrast and visibility could be of the loliginid squids Sepioteuthis sepioidea achieved through painting the tanks in ap- andDoryteuthis plei. - Marine Biology, 9:9-25. propriate colour. On basis of the present Matsumoto, G. & J. Shimada. 1980. Further im- study, the appropriate colour for cuttlefrsh provement upon maintenance of adult squid should be medium brightness on a grey (Doryteuthis bleeheri) in a small circular and closed-system aquarium tank. - Biological Bul- scale. letin, 159(2): 3L9-324. Meadows, P. S. & J. I. Campbell L972. Habitat REFERENCES selection by aquatic invertebrates. Pages 271- Bacescu, M. C. L972. Substratum animals. Pages 382 in: Russell, F.S. & M. Yonge (eds.). Ad- ]-29l-1322 iz: Kinne, O. (ed.). Marine Ecolog5'. vances in Marine BioloryVolume l0.Academic A Comprehensive Integrated Treatise on Life Press, London. in Oceans and Coastal Waters Vol. I Environ- Messenger, J.B. 1977. Evidence that Octopus is mental Factors Part 3.Wiley Interscience, Lon- colour blind. - Journal of Experimental Biol- don. ogy,70: 49-55. tt2 Tlopical Marine Mollusc Programme (TMMP)

Messenger, J. B. & G. D. Sanders.7972. Visual Nabhitabhata, J. & P. Nilaphat. 1999. Life cycle preference and two-cue discrimination learn- of cultured pharaoh cuttlefrsh, Sepia pharaonis ing in octopus. - Animal Behaviour, 20(3): 580- Ehrenberg, 1831. - Phuket Marine Biological 585. Center Special Publication no. 19(1):25-40. Messenger, J. B., A. P. Wilson & A. Hedge. 1973. Nabhitabhata, J. & P. Polkhan. 1983. Biological Some evidence for colour-blindness in Octopus. studies on economic cephalopods-Il: survival - Journal of Experimental Biology, 59:77-94. and growth of cuttlefish, Sepiella inermis Fer Mo5mihan, M. & A. F. Rodaniche.1982. The Be- & d'Orb. in various salinity conditions. - Tech- haviour and Natural History of the Caribbean nical Paper No. 4/1983, Rayong Brackishwater Reef Squid Sepioteuthis sepioidea with a Con- l-5 Fisheries Station, Brackishwater Fisheries sideration ofSocial, Signal, and Defensive Pat- Division, Department of Fisheries. 36 pp. (In terns for Difficult and Dangerous Environ- Thai with English Abstract). ments. Verlag Paul Parey, Berlin, (Advances Nabhitabhata,J.,P. Polkhan & S. Kbinrum. 1984. in Ethology Supplements to Journal of Com- Culture, growth and behaviour of spineless parative Ethology No. 25, 151 pp. cuttlefish, Sepiella inermis Fer. & d'Orb. - Tech- Nabhitabhata, J. L978 a. Rearing experiment on nical Paper No. 5/I984,Rayong Brackishwater economic cephalopod -I: long-finned squid, Fisheries Station, Brackishwater Fisheries Sepioteuthis lessoniana Lesson. - Technical Pa- Division, Department of Fisheries. 48 pp. (ttt per 1978, Rayong Brackishwater Fisheries Sec- Thai with English Abstract). tion, Rayong Fisheries Station, Brackishwater Roffe, T. 1975. Spectral perception in Octopus: a Fisheries Division, Department of Fisheries. 41 behavioral study. - Vision Research, 15: 353- pp. (In Thai with English Abstract.) 356. Nabhitabhata, J. L978 b. Rearing experiment on Sanders, G. D. 1975. Cephalopods. Pages 1-101 economic cephalopod - II: Cuttlefish, Sepia in: Corning,W. C., J. A. Dyal & A. O. D. pharaonis Ehrenberg. - Technical Paper 1978, Williams (eds.). Invertebrate Learning VoI. 3 Brackishwater Fisheries Section, Rayong Cephalopods and Echinoderms. Plenum Press, Brackishwater Fisheries Station, Brackish- NewYork. water Fisheries Division, Department of Fish- Sirisaksophon, S., Y. Nakamura & K. Matsuike. eries. 62 pp. (In Thai with English Abstract). 1995. Visual contrast threshold of Japanese Nabhitabhata, J. 1996. Life cycle of cultured common sqtid, Todarodes pacificus Steenstrup. biglin squid, Sepioteuthis lessoniana Lesson. - - Fisheries Science, 6l(4): 57 4-577. Phuket Marine Biological Center Special Pub- Wells, M. J. 1966. Cephalopod sense organs. lication no. 16: 83-95. Pages 523-545 in: Wilbur, K. M. & C. M. Yonge Nabhitabhata, J .1997 . Life cycle of three cultured (eds.). Physiology of Mollusca Vol. 2. Academic generations of spineless cuttlefish, Sepialla Press, New York. inermis (Ferussac & d'Orbigny, 1848). - Phuket Yang,W.T., R.T. Hanlon,M. E. Krejci,R. F. Hixon Marine Biological Center Special Publication & W. H. Hulet. 1983. Laboratory rearing of no. 17(1): 289-298. Loligo opalescens,the market squid of Califor- Nabhitabhata, J. 1998. Distinctive behaviour of nia. - Aquaculture, 31: 77-88. Thai pygmy squid, ldiosepius thailandicus Young, J. Z.1968. Reversal of a visual preference Chotiyaputta, Okutani & Chaitiamvong, 1991 rn Octopus after removal of the vertical lobe. - - Phuket Marine Biological Center Special Pub- Journal of Experimental Biology, 49:413-419. lication no. 18(1): 25-40.