Abstract
Remotely operated vehicle dive video recordings of deep-sea squid ink release were examined to determine species, ink release type, release depth, and accompanying behavior/s. Ink release was commonly observed between the surface and 1,842.1 m in Monterey Bay, CA, and surrounding waters. Six ink release types were observed: pseudomorphs, pseudomorph series, ink ropes, clouds/smokescreens, diffuse puffs and mantle fills. Each species released ink throughout all or most of its depth range; inking was not limited to shallow, sunlit waters. Individuals of each species produced one ink release type more commonly than other types, however, multiple ink types could be released by individuals of all species. Common behaviors preceded and/or followed each release type; pseudomorphs and pseudomorph series were generally associated with escape behaviors, while ink ropes, clouds, and puffs normally involved the animal remaining adjacent to or amid the ink. Deep-sea squids may use ink for defensive purposes similar to those of shallow-dwelling species when they release pseudomorphs, pseudomorph series, or large clouds, and may use ink puffs in intra-specific communication. The function of ink ropes and mantle fills is unknown.
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Ahl AS (1986) The role of vibrissae in behavior: status review. Vet Res Commun 10:245–268
Alldredge AL, Robison BH, Fleminger A, Torres JJ, King JM, Hamner WM (1984) Direct sampling and in situ observation of a persistent copepod aggregation in the deep-sea. Mar Biol 80:75–81
Anderson RL, Mather J (1996) Escape responses of Euprymna scolopes Berry, 1911 (Cephalopoda: Sepiolidae). J Molluscan Stud 62:543–545
Barham EG (1963) Siphonophores and the deep scattering layer. Science 140:826–828
Barham EG (1966) Deep scattering layer migration and composition: observations from a diving saucer. Science 151:1399–1403
Boletsky SW (1987) Juvenile behavior. In: Boyle PR (ed) Cephalopod life cycles, vol II: comparative reviews. Academic, London, pp 45–60
Caldwell RL (2005) An observation of inking behavior protecting adult Octopus bocki from predation by green sea turtle (Chelonia mydas) hatchlings. Pac Sci 59(1):69–72
Clarke MR (1977) Beaks, nets and numbers. Symp Zool Soc Lond 38:89–126
Dilly PN, Herring PJ (1978) The light organ and ink sac of Heteroteuthis dispar (Mollusca: Cephalopoda). J Zool Lond 186:47–59
Dubas F, Hanlon RT, Ferguson GP, Pinsker HM (1986) Localization and stimulation of chromatophore motoneurons in the brain of the squid Lolliguncula brevis. J Exp Biol 121:1–25
Dunning MC, Clarke MR, Lu CC (1993) Cephalopods in the diet of oceanic sharks caught off Eastern Australia. In: Okutani T, O’Dor RK, Kubodera T (eds) Recent advances in fisheries biology. Tokyo University Press, Tokyo, pp 119–131
Florey E (1969) Ultrastructure and function of cephalopod chromatophores. Am Zool 9:429–442
Forsythe JW, Hanlon RT (1997) Foraging and associated behavior by Octopus cyanea Gray, 1849, on a coral atoll, French Polynesia. J Exp Mar Biol Ecol 209:15–31
Gilly WF, Lucero MT (1992) Behavioral responses to chemical stimulation of the olfactory organ in the squid Loligo opalescens. J Exp Biol 162:209–229
Guerra A, Simon F, Gonzalez AF (1993) Cephalopods in the diet of swordfish, Xiphias gladius, from the Northeastern Atlantic Ocean. In: Okutani T, O’Dor RK, Kubodera T (eds) Recent advances in fisheries biology. Tokyo University Press, Tokyo, pp 159–164
Hanlon RT, Messenger JB (1996) Cephalopod behavior. Cambridge University Press, Cambridge
Herring PJ (1977) Luminescence in cephalopods and fish. Symp Zool Soc Lond 38:127–159
Huffard CL, Caldwell RL (2002) Inking in a blue-ringed octopus, Hapalochlaena lunulata, with a vestigial ink sac. Pac Sci 56:255–257
Hunt JC (1996) The behavior and ecology of midwater cephalopods from Monterey Bay. PhD dissertation, University of California, Los Angeles
Hunt JC, Seibel BA (2000) Life history of Gonatus onyx (Cephalopoda: Teuthoidea): ontogenetic changes in habitat, behavior and physiology. Mar Biol 136:543–552
Hunt JC, Zeidberg LD, Hamner WM, Robison BH (2000) The behaviour of Loligo opalescens (Mollusca: Cephalopoda) as observed by a remotely operated vehicle (ROV). J Mar Biol Assoc UK 80:873–883
Johnsen S (2001) Hidden in plain sight: the ecology and physiology of organismal transparency. Biol Bull 201:301–318
Johnsen S (2002) Cryptic and conspicuous coloration in the pelagic environment. Proc R Soc Lond B Biol Sci 269:243–256
Lucero MT, Farrington H, Gilly WF (1994) Quantification of l-Dopa and dopamine in squid ink: implications for chemoreception. Biol Bull 187:55–63
MacGinitie GE, MacGinitie N (1968) Natural history of marine animals. McGraw-Hill Book Company, New York
Moiseev SI (1991) Observation of the vertical distribution and behavior of nektonic squids using manned submersibles. Bull Mar Sci 49:446–456
Moynihan M (1985) Communication and non-communication in cephalopods. Indiana University Press, Bloomington
Moynihan M, Rodaniche AF (1982) The behavior and natural history of the Caribbean reef squid Sepioteuthis sepioidea. Adv Ethol 25:1–150
Nolen TG, Johnson PM (2001) Defensive inking in Aplysia spp.: multiple episodes of ink secretion and the adaptive use of a limited chemical resource. J Exp Biol 204:1257–1268
Prota G, Ortonne JP, Voulot C, Khatchadourian C, Nardi G, Palumbo A (1981) Occurrence and properties of tyrosinase in the ejected ink of cephalopods. Comp Biochem Physiol 68B:415–419
Robison BH (1993) Midwater research methods with MBARI’s ROV. Mar Technol Soc J 26:32–39
Robison BH (1995) Light in the ocean’s midwaters. Sci Am 273:60–64
Robison BH (1999) Shape change behavior by mesopelagic animals. Mar Fresh Behav Physiol 32:17–25
Robison BH (2004) Deep pelagic biology. J Exp Mar Biol Ecol 300:253–272
Robison BH, Reisenbichler KR, Hunt JC, Haddock SHD (2003) Light production by the arm tips of the deep-sea cephalopod Vampyroteuthis infernalis. Biol Bull 205:102–109
Russo GL, De Nisco E, Fiore G, Di Donato P, d’Ischia M, Palumbo A (2003) Toxicity of melanin-free ink of Sepia officinalis to transformed cell lines: identification of the active factor as tyrosinase. Biochem Biophys Res Commun 308:293–299
Seibel BA, Robison BH, Haddock SHD (2005) Post-spawning egg care by a squid. Nature 438:929
Shashar N, Hanlon RT, Petz A (1998) Polarization vision helps detect transparent prey. Nature 393:222–223
Tett P (1990) The photic zone. In: Herring PJ, Campbell AK, Whitfield M, Maddock L (eds) Light and life in the sea. Cambridge University Press, Cambridge, pp 59–87
Thompson KR (1994) Predation on Gonatus antarticus by Falkland Islands seabirds. Antarct Sci 6(2):269–274
Vecchione M, Roper CFE (1991) Cephalopods observed from submersibles in the Western North Atlantic. Bull Mar Sci 49:433–445
Vecchione M, Robison BH, Roper CFE (1992) A tale of two species: tail morphology in paralarval Chiroteuthis (Cephalopoda: Chiroteuthidae). Proc Biol Soc Wash 105:683–692
Voight J (1997) Cladistic analysis of the octopods based on anatomical characters. J Molluscan Stud 63:311–325
Voss GL (1967) The biology and bathymetric distribution of deep-sea cephalopods. Stud Trop Ocean 5:511–535
Watanabe Y, Baranov EA, Sato K, NaitoY, Miyazaki N (2004) Foraging tactics of Baikal seals differ between day and night. Mar Ecol Prog Ser 279:283–289
Wells MJ (1978) Octopus. Chapman and Hall, London
Wells MJ (1994) The evolution of a racing snail. In: Poertner HO, O’Dor RK, MacMillan DL (eds) Physiology of cephalopod molluscs: lifestyle and performance adaptations. Gordan and Breach Publishing Group, Basel, pp 1–12
Widder E, Bernstein S, Bracher DF, Case JF, Hiller-Adams P, Reisenbichler KR, Torres JJ, Robison BH (1989) Bioluminescence in Monterey Canyon: image analysis of in situ video recordings from a midwater submersible. Mar Biol 100:541–551
Widder EA, Robison BH, Reisenbichler KR, Haddock SHD (2005) Using red light for in situ observations of deep-sea fishes. Deep-Sea Research I 52:2077–2085
Young RE (1972) The systematics and areal distribution of pelagic cephalopods from the seas off Southern California. Smith Contr Zool 97:1–159
Young RE (1975a) Function of the dimorphic eyes in the midwater squid Histioteuthis dofleini. Pac Sci 29:211–218
Young RE (1975b) Transitory eye shapes and the vertical distribution of two midwater squids. Pac Sci 29:243–255
Young RE, Roper CFE (1976) Bioluminescent countershading in midwater animals: evidence from living squid. Science 191:1046–1048
Young RE (1983) Oceanic bioluminescence: an overview of general functions. Bull Mar Sci 33:829–845
Acknowledgements
We would like to thank the pilots and crews of the ROV Ventana/RV Point Lobos and ROV Tiburon/RV Western Flyer for their assistance in obtaining squid observations. We are grateful to the staff of the MBARI video lab for their help in viewing videos and preparing images for the manuscript. We thank R. Caldwell, E. Griffen, C. Martinez, C. Huffard, B. Williams, and especially D. Greenwood for comments on various stages of the manuscript. This study was made possible by members of MBARI’s midwater lab, supported by the David and Lucile Packard Foundation, as well as a National Science Foundation Graduate Research Fellowship to S. Bush. The experiments comply with the current laws of the United States.
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Communicated by P.W. Sammarco.
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Bush, S.L., Robison, B.H. Ink utilization by mesopelagic squid. Mar Biol 152, 485–494 (2007). https://doi.org/10.1007/s00227-007-0684-2
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DOI: https://doi.org/10.1007/s00227-007-0684-2