Anomalous infrared taxis of an aquatic animal, the giant jellyfish Nemopilema nomurai (Scyphozoa, Rhizostomeae).
Infrared (IR) sensitivity is known to be mediated by the so-called pit organs, which enable crotaline and boid snakes to apprehend homeothermic prey (1-7) and vampire bats to detect IR radiation from blood-rich locations (8), (9). More-over, similar mechanisms have been reported in some insects such as fine debris species of beetle (10-13), bloodsucking bugs (14), and some butterflies (15), (16). In aquatic animals, however, little is known about the IR sensitivity. This is the first report to describe an anomalous IR-tactic behavior in the giant jellyfish, Nemopilema nomurai, living in an aquatic environment.
Nemopilema nomurai Kishinouye 1922 is one of the largest scyphozoan jellyfish, measuring 1-2 m in diameter and weighing 100-200 kg. Massive blooms of this species have occurred almost annually since 2002, severely affecting coastal fisheries in the Sea of Japan. The life cycle of N. nomurai has been well established by us and our coworkers (17), (18), so the juvenile medusae are easily available. We thus used laboratory-reared juveniles (extended bell diameter, 8-15 mm) to examine the IR sensitivity of N. nomurai.
The experimental chamber (width = 30 cm, length = 24 cm, height = 16 cm) used to test IR sensitivity was made from transparent acryl resin plate (5 mm thick). It was filled with seawater to a depth of 3.5 cm and 20 to 35 juvenile individuals were added. The distribution of the medusae in the chamber was monitored by photographing them from above with a photographic strobe every 30 or 60 min. The IR wavelengths were obtained from a tungsten-filament lamp (40 W) by passing the light through a long-pass filter (50% cut-on at 990 nm; LIO-990, Asahi Spectra Co. Ltd.). The tungsten-filament lamp was fixed in a lightproof aluminum housing with a window, where the long-pass filter was mounted. All possible heat sources, except for the IR-wavelength source, were excluded from around the experimental chamber. Near-IR wavelengths, 940 and 850 nm, were obtained from two types of 1.2-W LEDs, LB12 - WP01 and LC12-WP01 (Ebisu Electronics Co. Ltd.), respectively. A near-IR image converter (NEC, NVR-2015) was used to observe the behavior of the medusae under visually dark conditions. The visible-light source was provided by a standard white LED (1 W, 10 mm). The distances between each wavelength source and the chamber wall were 150 mm in the case of the IR and visible light, and 65 cm in the case of the near-IR (850/940 nm), and were adjusted to just cover the whole surface of one 24-cm side of the chamber. The radiations from the sources were passed through the long axis (30 cm) of the chamber. A digital thermometer with a thermistor-type probe (Asone, AST-250T) was used to measure room and seawater temperatures. The rhopalia were observed using an inverted light microscope equipped with a Hoffman modulation-contrast device (Nikon, TS-100).
In the experiments to estimate IR sensitivity (Fig. 1), the seawater temperature in the chamber varied between 12.8 and 21.9 [degrees]C, and the room temperature varied between 11.2 and 13.4 [degrees]C and was always kept lower than the seawater temperature, unless otherwise stated. The reasons for this will be discussed later. Figure 1A-F shows the raw data obtained in a series of experiments performed successively for more than 7 h, and the results are summarized in Table 1. First, the medusae were scattered in the chamber by artificially stirring them, with 15 and 20 individuals distributed, respectively, in the left and right halves (L = 15, R = 20) (Fig. 1A). However, 60 min after turning on the IR source placed laterally to the left, the medusae flocked to the left half (L = 2 8, R = 7), especially along the side wall of the chamber (Fig. 1B). When the IR source was moved to the opposite (right) side, the medusae moved en masse toward the right-side chamber wall (Fig. 1C, 60 min after B; L = 5, R = 30). The same event occurred when the IR source was moved back to the left side (Fig. 1D, 60 min after C; L = 33, R = 2). This movement cannot be attributed to the water convection induced by differential heating between both sides because the convection current was negligible as observed by the movement of fine debris, and vigorous swimming of the medusae easily overcame it. It should be noted that the majority of the medusae kept close contact with the surface of the irradiated side of the chamber. During a 60-min experiment, the seawater temperature at a point 8 mm from the IR side of the chamber wall was always greater by 0.2-0.3 [degrees]C (dT in Table 1) than the corresponding point opposite. If the room temperature was elevated (21.8 [degrees]C in Fig. 1E) significantly above the seawater temperatures (16.8 [degrees]C in Fig. 1E), the IR taxis disappeared (Fig. 1E, IR source on left; L = 17, R = 18). This result is probably caused by thermal radiation from ambient air masking the radiation from the IR source. The temperature of the outer surface of the chamber on the side of the IR source, measured by infrared-radiation thermometer, ranged from 20 to 25 [degrees]C, which was comparable to that of the ambient air. If the room temperature dropped below that of the seawater, the IR taxis returned (Fig. 1F; IR source on right; L = 3, R = 32). All the results of the experiments to test the IR taxes are shown in Table 2. In all 52 trials (accumulated nos. = 1367), the majority of the medusae gathered on the IR-source half of the experimental chamber (average, 78.3%; variation, 63.3%-94.3%).
Table 1 Summarized data for the experiment in Figure 1 Room temp Seawater dT Nos. Nos. temp on on ([degrees] C) ([degrees] Left half Right ([degrees] left right C) half C) half half A 11.8 20.5 20.5 0 15 20 B 11.9 16.9* 16.7 0.2 28 7 C 11.9 16.0 16.3* 0.3 5 30 D 12.0 14.4* 14.2 0.2 33 2 E 21.8 16.8* 16.8 0 17 18 F 15.5 16.2 16.4* 0.2 3 32 Asterisks (*) represent the IR-source side. d7* = (IR-side temperature) -- (anti-JR-.side temperature).
[FIGURE 1 OMITTED]
Taxis to near-IR wavelengths (940 and 850 nm) and visible light were also experimentally investigated. In these experiments, the light sources were regularly alternated between the left and right sides of the chamber, because the medusae tended to stay aggregated on either side irrespective of the direction of the light sources. The averages for the light-source side were 53.8%, 51.0%, and 50.3% for 940 nm, 850 nm, and visible light, respectively. These averages are fairly equal and the variations are extremely large (Table 2), indicating that the medusae moved randomly to the near-IR and visible-light sources.
Table 2 Taxes to various wavelengths Variations Total nos. Total nos. Averages on source side (%) (trials) (medusae) (%) Max Min Infrared 52 1367 78.3 94.3 63.3 940 nm 20 600 53.8 76.7 26.7 850 nm 22 770 51.0 82.9 11.4 Visible 10 350 50.3 82.9 22.9
Scyphozoan medusae have marginal lobe organs, termed rhopalia; in Aurelia aurita these have, since Romanes (19), been considered to be integrative loci for swimming activities, photoreception, and gravity sensitivity (20-26). Nemopilema, as well as Aurelia aurita, has eight rhopalia at the margin of the exumbrella (Fig. 2A, B). Nemopilema, however, lacks both a cup-ocellus and a spot-ocellus (Fig. 2B, C), which are assumed to be the photoreceptive organs in Aurelia (20), (21). A statolith is clearly seen in both species, although it is more reddish in Nemopilema (Fig. 2B, C). In Nemopilema., excision of the last of eight rhopalia by pinching it off with fine forceps resulted in failure of spontaneous swimming contraction, indicating that the rhopalia are integrative loci for motor activity, as is the case for Aurelia.
[FIGURE 2 OMITTED]
The IR taxis of juveniles of Nemopilema under visually dark conditions were observed with a near-IR image converter. After IR irradiation was started, each Nemopilema individual first appeared to wander randomly within the experimental chamber; namely, none appeared to swim in an oriented manner. As time proceeded, however, the mass of the medusae gradually shifted toward the irradiated side. It took about 60 min until a clear pattern of distribution was established in the chamber. The smaller the chamber, the faster the establishment of the distribution; for example, in the preliminary experiments, in which the chamber used (20 cm wide) was smaller than the one used here (30 cm wide), it took about 30 min.
It is uncertain whether the IR taxis of Nemopilema is due to topotaxis to the IR source. During the 60-min experiment, the seawater temperature at the IR-source end of the chamber increased by 0.2 [degrees] C on average (variation, 0.1-0.3 [degrees]C) compared to that on the corresponding anti-IR-source end. However, far-IR wavelengths are almost completely absorbed by water and thus never reached the other side of the experimental chamber across a path of 30 cm, indicating that the far-IR wavelengths could not be a cue for the topotaxis. On the other hand, according to the observations using the near-IR image converter, the near-IR did reach the other side through the seawater in the chamber. Although the near-IR wavelengths might play a role in the topotaxis. the fact that both the 850- and 940-nm wavelengths induced no selective movement (Table 2) argues against it. Furthermore, the IR taxis disappeared when the ambient room temperature was elevated far above that of the seawater in the experimental chamber (Fig. 1). This is probably because far-IR wavelengths emitted from the ambient air masked those from the IR source, suggesting that the far-IR wavelengths are principally responsible for the IR taxis. It is probable that visible light had no effect on the taxis, because the juvenile medusae of Nemopilema lack ocelli (Fig. 2). Similarly, the near-IR wavelengths (850/940 nm) are probably unrelated to the IR taxis, because they belong to the category of retinal photoreception as reported in fish, such as the common carp and Nile tilapia (27). It is thus likely that the medusae first swam randomly within the chamber and reached the IR-source side by chance, and then received far-IR radiation that kept them there. It is conceivable that the medusae head all together toward the IR source along the IR-radiation gradient formed locally on the IR-source end. On the other hand, NemopitemaJuveniles might have extremely high IR-radiation sensitivity that enables them to orientate toward the IR source. In fact, it has been reported that the pit organs of some snake species are capable of sensing temperature differences as little as 0.001 [degrees]C (1), (3), (7), (28), (29).
It is necessary to determine which organs are responsible for the remote and directional sensing of the 1R radiation. The rhopalia are the most likely candidates, because they are assumed to be integrative loci for swimming activity and sensory functions (20-26). This would be possible if the rhopalia have sensory nerves with thermo-sensitive ion channels as are reported in the pit organs (6). The rhopalia could receive the radiation from the IR source when the bell is extended without being shaded by the medusa body. Nemopilema juveniles could approach the IR source gradually if they could repeatedly modify their body angle so that all rhopalia received equal input from the IR source. This would be possible if each rhopalial pacemaker ganglion could regulate the contractions of each occupied perradius and interradius swimming muscle separately, in response to the inputs from the IR source.
The physiological and ecological meaning of the IR taxis of Nemopilema is uncertain. However, it is likely that the IR taxis prompts the juvenile Nemopilema to head toward warmer water-masses in the sea and to stay there. For this reason, juvenile medusae tend to aggregate near the surface in Chinese waters, which are a breeding and nursery area of Nemopilema, and remain held in low-salinity water masses offshore until they are conveyed northward to the Sea of Japan by the warm Tsushima Current (17). In addition, some kinds of jellyfish swarm on a huge scale and often crowd around electrical power plants, blocking the intake of cooling water and impeding plant operation. Such incidents might simply occur accidentally because of extraordinary blooms of these species, or there might be some natural or artificial conditions that directly cause these incidents. This question might be solved by reexamining the jellyfish swarming mechanisms from the viewpoint of the IR taxis.
We thank M. Nishizaki, a technician on the staff of Oki Marine Biological Station, Shimane University, for collecting Nemopilema nomurai. This research was supported by a research grant from the Ministry of Agriculture, Forestry and Fisheries, Japan.
(1.) Bullock, T. H., and F. P. J. Diecke. 1956. Properties of an infra-red receptor. J. Physiol. 134: 47-87.
(2.) Campbell, A. L., R. R. Naik, L. Sowards, and M. O. Stone. 2002. Biological infrared imaging and sensing. Micron 33: 211-225.
(3.) Grace, M. S., D. R. Church, C. T. Kelly, W. F. Lynn, and T. M. Cooper. 1999. The Python pit organ: imaging and immunocyto-chemical analysis of an extremely sensitive natural infrared detector. Biosens. Bioelectron. 14: 53-59.
(4.) Moiseenkova, V., B. Bell, M. Motamedi, E. Wozniak, and B. Christensen. 2003. Wide-band spectral tuning of heat receptors in the pit organ of the copperhead snake (Crotatinae). Am.J. Physiol. Regul Integr. Comp. Physiol. 284: R598-R606.
(5.) Amemiya, F., M. Nakano, R. C. Goris, X. Kadota, Y. Atobe, K. Funakoshi, K. Hibiya, and R. Kishida. 1999. Microvasculature of crotaline snake pit organs: possible function as a heat exchange mechanism. Anal. Rec. 254: 107-115.
(6.) Gracheva, E. O., N. T, Ingolia, Y. M. Kelly, J. F. Cordero-Morales, G. Hollopeter, A. T. Chesler, E. E. Sanchez, J. C. Perez, J. S. Weissman, and D. Julius. 2010. Molecular basis of infrared detection by snakes. Nature 464: 1006-1012.
(7.) Goris, R. C. 2011. Infrared organs of snakes: an integral part of vision. J. Herpetol. 45: 2-14.
(8.) Kishida, R., R. C. Goris, S. Terashima, and J. L. Dubbeldam. 1984. A suspected infrared-recipient nucleus in the brainstem of the vampire bat, Desmodus rotundus. Brain Res. 322: 351-355.
(9.) Kurten, L., and U. Schmidt. 1982. Thermoperception in the common vampire bat (Desmodus rotundas). J. Comp. Physiol. A 146: 223-228.
(10.) Vondran, T., K.-H. Apel, and H. Schmitz. 1995. The infrared receptor of Melanophila acuminata De Geer (Coleoptera: Buprestidae): ultrastructural study of a unique insect thermoreceptor and its possible descent from a hair mechanoreceptor. Tissue Cell 27: 645-658.
(11.) Schmitz, H., H. Bleckmann, and M. Murtz. 1997. Infrared detection in a beetle. Nature 386: 773-774.
(12.) Schutz, S., B. Weissbecker, H. E. Hummel, K.-H. Apel, H. Schmitz, and H. Bleckmann. 1999. Insect antenna as a smoke detector. Nature 398: 298-299.
(13.) Schmitz, H., and H, Bleckmann. 1998. The pholomechanic infrared receptor for the detection of forest (ires in (he beetle Melanophila acuminata (Coleoptera: Buprestidae) J. Camp. Physiol. A 182: 647-657.
(14.) Lazzari, C. R., and J. Nunez. 1989. The response to radiant heat and the estimation of the temperature of distant sources in Triatoma infestans. J. Insect Physiol 35: 525-529.
(15.) Schmitz, H. 1994. Thermal characterization of butterfly wings. I. Absorption in relation to different color, surface structure and basking type. J. Them. Biol 19: 403-412.
(16.) Schmitz, H., and L. Th. Wasserthal. 1993. Antennal thermoreceptors and wing-thermosensitivity of heliolherm buUerllies: their possible role in thermoregulatory behavior. J. Insect Physiol. 39: 1007-1019.
(17.) Kawahara, M., S. Uye, K. Ohtsu, and H. Iizumi. 2006. Unusual population explosion of the giant jellyfish Nemopilema nomurai (Scyphozoa: Rhizostomeae) in East Asian waters. Mar. Ecol Prog. Ser, 307: 161-173.
(18.) Ohtsu, K., M. Kawahara, and S. Uye. 2007. Experimental induction of gonadal maturation and spawning in the giant jellyfish Nomo-pilema nomurai (Scyphozoa: Rhizostomeae). Mar. Biol. 152: 667-676.
(19.) Romanes, G. J. 1876. Preliminary observations on the locomotor system of medusae. Philos. Trans. R. Soc. Loud. 166: 269-313.
(20.) Yamasu, T., and M. Yoshida. 1973. Electron microscopy on the photoreceptors of an anthomedusa and a scyphomedusa. Pitbl. Seto Mar. Biol. Lab. 20: 757-778.
(21.) Takasu, N., and M. Yoshida. 1984. Freeze-fracture and histofluo-rescence studies on photoreceptive membranes of medusan ocelli. Zool. Sci. 1: 367-374.
(22.) Spangenberg, I)., R. Phillips, and A. Kostas. 1989. Effect of graviceptor excision on Atirelia ephyra swimming/pulsing behavior at lg and during parabolic flight. Gravit. Space Biol. 2: 24 (Abstract).
(23.) Horridge, G. A. 1959. The nerves and muscles of medusae. VI. The rhythm. 7. Exp. Biol. 36: 72-91.
(24.) Passano, L. M. 1965. Pacemakers and activity patterns in medusae: homage to Romanes. Am. Zool. 5: 465-481.
(25.) Passano, L. M. 1973. Behavioral control systems in medusae: a comparison between hydro-and scyphomedusae. Puhl. Seto Mar. Biol. Lab. 20: 616-645.
(26.) Arai, M. N, 1997. A Functional Biology of Scyphozoa. Chapman & Hall, London.
(27.) Matsumoto, T., and G. Kawamura. 2005. The eyes of the common carp and Nile tilapia are sensitive to near-infrared. Fish. Sci. 71: 350-355.
(28.) de Cock Buning, T. 1983. Thermal sensitivity as a specialization for prey capture and feeding in snakes. Am. Zool. 23: 363-375.
(29.) Ebert, j., and G. Westhoff. 2006. Behavioural examination of the infrared sensitivity of rattlesnakes (Crotalus atrox). J. Comp. Physiol. A 192: 941-947.
KOHZOH OHTSU (1) * AND SHIN-ICHI UYE (2)
(1.) Oki Marine Biological Station, Faculty of Life and Environmental Science, Shimane University, 194 Kamo, Okinoshima-cho, Oki-gun, Shimane 685-0024, Japan; and (2.) Graduate School of Biosphere Science, Hiroshima University, 4-4 Kagamiyama 1 Chome, Higashi-Hiroshima, Hiroshima 739-8528, Japan
Received I August 2011; accepted 20 October 2011.
* To whom correspondence should be addressed. E-mail: firstname.lastname@example.org
|Printer friendly Cite/link Email Feedback|
|Author:||Ohtsu, Kohzoh; Uye, Shin-ichi|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 2011|
|Previous Article:||Evolutionary simplification of velar ciliation in the nonfeeding larvae of periwinkle (Littorina spp.).|
|Next Article:||Fine structure, histochemistry, and morphogenesis during Excystment of the Podocysts of the giant jellyfish Nemopilema Nomurai (scyphozoa,...|