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Behavioural responses to visual stimuli by the snail Littorina irrorata
Anita. Behav., t982, 30, 752-760
BEHAVIOURAL RESPONSES TO VISUAL STIMULI BY THE SNAIL LITTORINA IRRORATA BY P. V. H A M I L T O N & M. A. W I N T E R
Department of Biology, University of West Florida, Pensacola, FL 32504 Abstract. The visual capabilities of gastropod molluscs and most other invertebrates possessing structurally simple eyes are poorly known. We studied vision in untrained marsh periwinkles (Littorina irrorata) in the laboratory, using oriented movements toward test shapes as the response measure. This intertidal species is active when exposed at low tide, both during the day and at night, and it travels vertically on plant stems with a tidal rhythm. In detection tests, the estimated response threshold for a single vertical bar was 0.9 ~, while the response threshold for an equal-size horizontal bar was 2.4 ~ or 3.7 ~, depending on bar position. Snails detected a 5~ bar in 4.3 lx of light and a 40~ square having about 95 % reflectance ('off-white') on a white (100 ~ nominal reflectance) background in 2800 lx. Discrimination tests revealed a strong preference for vertical bars over both diagonal and horizontal bars of the same width, but no preferences in several other situations. Various factors suggest that L. irrorata may see better than most other gastropods. The structurally simple eyes of gastropod molluscs and many non-arthropod invertebrates are often assumed to provide information on gross differences in light intensity, but not to form images. There are two weaknesses to this assumption. First, ideas about vision in gastropods are based primarily on superficial comparisons with the structurally complex vertebrate eye. Neurophysiological and behavioural data on the visual responses of gastropods are generally lacking. Second, the fact that 'there is no clear break in the spectrum of resolving power that different eyes show' (Land 1981) makes usage of the term 'image' ambiguous in comparative studies. Although vision has not been evaluated systematically in any gastropod, scattered behaviouraI, neurophysiological, and optical studies suggest an ability to see biologically relevant stimuli. Field experiments have demonstrated oriented responses to the sun in Littorina Bttorea (Newell 1958a, b), L. punctata (Evans 1961), and Nerita plicata (Warburton 1973), to unidentified celestial cues in Aplysia brasiliana (Hamilton & Russell 1982), to shoreline topographic features and nocturnal silhouettes of vegetation in L. punctata (Evans 1961) and N. textilis (Chelazzi & Vannini 1976), and to large areas of vegetation and individual plant stems in L. irrorata (Hamilton 1977a, 1978). Vision may help maintain a straight path when Strombus is escaping potential predators (Field 1977). Vision is apparently important in predation by heteropods (Land 1981). Laboratory experiments have demonstrated oriented re-
sponses to polarized light in Littorina and Nassarius (Burdon-Jones & Charles 1958; Baylor 1959; Charles 1961), to dark screens on a white background in Helix and Littorina (Bohn 1905; von Buddenbrock 1919; Bierens de Harm 1921; Geismer 1935; Charles 1966), and to darkened or lighted areas in Otala and Lymnaea (Hermann 1968; Stoll 1973). Electrophysiological studies have demonstrated responses traditionally associated with pattern detecting eyes, such as lateral inhibitory interactions, in Hermissenda (Dennis 1967; Stensaas et al. 1969) and Otala (Goldman & Hermann 1967). Optical measurements on the eye of L. littorea suggest that this species may be able to form sharp retinal images in air (Newell t965). Similar measurements for the nocturnal slug Agriolimax retieulatus suggest poorer visual acuity (Newell & Newell 1968). In this study of the marsh periwinkle, Littorina irrorata Say, we examine the responses of untrained animals to various test shapes presented under controlled lighting conditions. Our experimental design follows the recommendation of Riggs (1965) that detection tests of acuity should employ dark shapes against bright backgrounds. We studied innate oriented responses to shapes because, unlike vertebrates, Octopus, and insects, gastropods are difficult to train (Willows 1973). Studies on human infants (e.g. Teller et al. 1974) and octopods (e.g. Messenger & Sanders 1972) show that meaningful data can be obtained using untrained subjects. 752
HAMILTON & WINTER: VISUAL RESPONSES BY LITTDRINA
753
We chose L. irrorata for this initial evaluation of vision in gastropod molluscs because field data indicated that this species has a distinct response to discrete objects in the environment. This snail feeds on the bottom subs~rate in marshy intertidal zones on both daytime and night-time low tides, and hence is active in an air medium. It ascends surrounding plant stems on the advancing tide, thereby avoiding benthic predators (Hamilton 1976, 1977a). As noted above, orientation toward plant stems is visually mediated.
Methods Apparatus One of the six identical arenas in which tests were conducted is shown in Fig. 1. The top section contained the light source and filters; its walls were constructed of perforated masonite to facilitate cooling. The lamp was a 250-W ECA incandescent bulb having a 3200 K colour temperature. A blue filter shifted this light to 5000 K, thus simulating natural sunlight. A diffusing filter eliminated the possibility of polarized light entering the arena. Neutral density filters were added to obtain lowered light intensities when desired. For tests in complete darkness, the lamp remained on, but several layers of black paper were added to block all light entering the arena. A 50-cm=long section of flat-white PVC plastic pipe (29.5 cm internal diameter) was permanently attached to the top section. The middle section consisted of a 30-cm-long section of the same pipe bonded to a 6-cm-thick disc of clear Plexiglass. Test shapes were attached to the lower wall of this section. A removable Plexiglass disc (3 m m thick, 29 cm diameter) was placed on the bottom of this section for each trial; it comprised the surface over which the test animal crawled. Arena illumination w a s measured on the surface of this disc with a photocell having peak sensitivity to 550 nm light (Clairex 750 HI,). A diffusing filter was attached beneath this section to eliminate directional light reflection from below. The bottom section contained a mirror and a small viewport on the side to permit the viewing of the test animal's shadow on the bottom of the middle section. The middle section sat on the bottom section, which rested on a table. Adjustable legs on the bottom section permitted levelling of the entire arena. The top section could be raised to change crawling surfaces and test animals.
--pp
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I
~
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' CP
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Fig. 1. Schematic diagram of one of six identical arenas used in this study. (AL = adjustable leg, BF = blue filter, CG = clear glass, CP = clear Plexiglass bottom, DF = diffusing filter, LB = light bulb, M = mirror, PP = PVC pipe walls, RD. = removable Plexiglass disc, TT = table top). We cut black test shapes from paper and produced the series of test shapes having different reflectances photographically by visual matching with the K o d a k grey scale. Regardless of size, we glued each test shape to a 10.3-cm square piece of white paper and laminated the composite in clear plastic. Then we attached the resulting test card to the lower wall of the middle section of the arena with two-sided tape
Test Animals and Procedure We collected adult L. irrorata (shell length /> 13 ram) from Juncus marshes bordering
754
ANIMAL
BEHAVIOUR,
Santa Rosa Sound, Escambia County, Florida. We transported snails to the laboratory and maintained them in plastic containers (26 x 20 x 15 era) containing about 5 cm of aerated sea water. We kept the containers in a holding chamber containing fluorescent light (2150 lx) operated on approximately the natural photoperiod for the collection date. We did not feed the snails but we always tested them within 96 h after collection. We conducted two kinds of tests with the snails. The detection series of tests measured the tendency of snails to orient toward a single test card located against a white background. The discrimination series of tests compared the tendency of snails to orient toward one of two test cards on a white background. The light intensity at the crawling surface was 2800 lx for all tests except for the one detection test where intensity was the variable studied. In each detection test, we varied a single parameter among the six arenas. For example, when the parameter of horizontal dimension was studied, one arena contained a 10.3-cm-high black shape that filled 40 ~ of horizontal arc, one contained a 20~ shape, one a 10 ~ one a 5 ~ and one a 2.5~ the sixth arena contained a completely white test card and thus served as the control (see Fig. 3A). We individually released 24 snails in the centre of each arena. We systematically rotated initial facing directions, with an equal number of snails released facing toward, 90 ~ to the right, 180 ~ away, and 90 ~ to the left of the test card. In each discrimination test, we placed two test cards in each arena, centred 80 ~ apart. We released snails individually in the centre of an arena and faced them directly between the test cards. The width of each test card was exactly 40 ~. However, the widths of the shapes which the cards contained were not identical for all pairs tested (for example, see Fig. 6, A-C). Thus, to enable a balanced analysis, we considered all snails reaching the arena's edge anywhere within the arc subtended by a test card (40 ~ to have responded to the shape on that card. We ignored those few snails reaching the arena's edge outside the arcs subtended by test cards. We tested enough snails for each pair of cards so that 20 responses were recorded with 'X right, Y left' and 20 responses were recorded with 'X left, Y right'. This procedure eliminated the possibility of any innate turning preference biasing the results.
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In both kinds of tests, we considered a snail to have responded once it travelled 13 cm from its release point 0.e. 1.75 cm from the arena wall). We discarded any snail not responding within 15 rain and we released a new snail in its place. Once a snail responded, we removed it and the plastic disc it had crawled over, from the arena. We misted the disc and recorded the direction of the snail's final position from the arena centre to the nearest 5 ~. For the detection tests, we recorded the mucus trail as described in Hamilton (1977b). We thoroughly cleaned and dried each plastic disc before reuse. We tested each snail only once.
Data Analysis For the detection series of tests, we wanted to use a response measure that incorporated the actual direction taken by each animal because a test card might influence the direction an animal takes without the animal moving directly toward (or away from) the card. A response criterion that scored an animal as hitting or missing the card would not be sensitive to this kind of influence. This consideration suggested the use of a statistical test for circular distributions of directions called the V-test (Batschelet 1972), a procedure which tests the null hypothesis that the directions taken by a group of animals were randomly oriented against the alternative hypothesis that the animals oriented in a specified direction On this case, in the test card's direction). The magnitude of the V-test statistic (u) is a measure of the group's tendency to orient in the card's direction, However, the maximum value u may attain lacks intuitive meaning and varies with the sample size (N). For example, if 24 animals all move directly toward a test card, the u statistic would equal 6.928; 12 animals orienting directly toward the card would yield a u statistic equal to 4.899. As defined by Batschelet (1972), u is a simple function of V', which is the component of the resultant vector in the predicted direction. The quantity V' is computed from the set of directions taken by the animals, as described by Batschelet. Our study modifies the standard Vtest procedure by defining a new test statistic, v', as follows: V ! V t
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H A M I L T O N & WINTER: VISUAL RESPONSES BY L I T T O R I N A
The quantity v' is the component of the mean vector in the predicted direction. If all animals in a group orient in the predicted direction (e.g. toward a test card's centre, then v' will equal 1.0 regardless of the sample size; if all animals orient directly away, v' will equal -- 1.0. Values of v' near zero indicate random orientation. Critical values of v' for hypothesis testing can be obtained directly from the critical values of u (as published in Batschelet 1972 or Zar 1974), using the following equation:
755
diagram. Figure 3A illustrates the six test cards and relates the horizontal dimensions of these cards to their corresponding response values. These data show that all cards possessing black shapes were responded to approximately equally, regardless of the shapes' horizontal dimensions. The threshold for a significant response (P---0.05) is about 0.9 ~. Figure 3B relates the vertical dimension of~a series of centrally-positioned shapes to their corresponding response values, and illustrates the six test cards. (Scatter diagrams are omitted for this and all subsequent detection tests to save space.) These data show a gradual decline in response proportional to vertical dimension, with a threshold at about 2.4 ~ When shapes having the same size and orientation were basallypositioned on the test cards (Fig. 3C), a similar gradual decline in response was evident, with a threshold at about 3.7 ~. The dip in the response curve at 40 ~ in Fig. 3C should not be interpreted as a significant change from the 20 ~ value, as the significance probabilities of both response values are less than 0.0001. We used the5~ shape from the horizontal dimension test (Fig. 3A) to explore the parameter of vertical dimension. Figure 3D relates the vertical dimension of a series of basallypositioned shapes to their corresponding re-
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Thus v' is the measure of oriented response used for all detection tests. For the discrimination series of tests, the numbers of snails responding to the two test cards were compared using the chi-squared test. Results The detection series of tests provided response curves and statistical thresholds for six stimulus parameters. Figure 2 shows scatter diagrams for the directions taken by L. irrorata in the horizontal dimension test. The degree of clumping of the directions around 0 ~ (the location of the test cards) is reflected by the v' value for each 0
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Fig. 2. Scatter diagrams showing the directions taken by six groups of 24 snails each in arenas having test shapes positioned at 0 ~ The test shapes, which varied in horizontal dimension, are illustrated in Fig. 3A. The letters A - F correspond between the two figures. The v' value is a measure of the degree of clumping of each group's directions toward the test shape.
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Fig. 3. (A) Relationship between the horizontal dimension of a 10.3-cmhigh test shape and the measure of oriented response to that shape (v'), based on the data shown in Fig. 2. A v' value of 0.238 (dashed line) is required for a circular distribution of directions (N = 24) to be significantly different from random at P = 0.05. This consideration leads to the estimate of 0.9~ (heavy arrow) as the response threshold for horizontal dimension. (B) Relationship between the vertical dimension of a 10.3-cm-wide, centrallypositioned test shape and the response to that shape. The response threshold is 2.4~ (C) Relationship between the vertical dimension of a 10.3-cm-wide, basally-positioned test shape and the response to that shape. The response threshold is 3.7~ (D) Relationship between the vertical dimension of a 1.3-cm-wide (5~ basally-positioned test shape and the response to that shape. The response threshold is 7.5| . sponse values, a n d illustrates the six test cards. A gradual decline in response was evident, with a threshold at a b o u t 7.5 ~ Collectively, Fig. 3 A - D shows that t h e snails' response is n o t based o n a single linear d i m e n s i o n o f a test shape.
We used identical 5~ shapes in a test designed to determine the range o f light levels in which snails could orient visually. Figure 4 relates arena light intensity to the corresponding response values, a n d illustrates the test shape which was present in all arenas. A gradual
HAMILTON & WINTER: VISUAL RESPONSES BY L I T T O R I N A
decline in response was evident, with a threshold at about 4.3 lx. It should be noted that we computed the light intensities present in the four middle-intensity arenas by accounting for the effect o f the amount of neutral density filtration used, rather than by direct measurement. This was done because the photocell was sensitive to the small amount of long-wavelength light passed by the filters. Light intensity in the highestintensity arena was measured directly (2800 lx). Light intensity in the lowest-intensity arena was considered to be infinitely small, as layers of black paper blocked all light transmission. We used 40~ shapes having different reflectances to determine how much an object must contrast with a white background to elicit significant orientation. Figure 5 relates shape reflectance to the corresponding response values. The pure white (F) and pure black (A) cards are assigned reflectance values of 100% and 0% respectively, although these extreme values are not characteristic of any natural surfaces. A gradual decline in response with increasing reflectance was evident; a test card having less than 95%/00 reflectance was oriented towards significantly when located against the white (100 9/0 nominal) background of the arena walls. The results of the discrimination series of tests supported predictions generated from c o m p a r i n g the response thresholds from the detection tests. A vertical 10.3 x 1.3-cm black bar was oriented towards significantly more often than a centrally or basally-positioned horizontal bar of the same size (Fig. 6A, B). Interestingly, the same vertical bar was signifi1.0"
757
cantly preferred over a slanted bar reaching the same height (Fig. 6C), indicating that bar orientation was more important than bar length. However, with bars having an identical orientation (vertical), snails significantly preferred an 8-cm-high bar over one 4 cm high (Fig. 6D). Snails showed no preference between centrallyand basally-positioned horizontal bars (Fig. 6E). No significant preferences were exhibited in the final four discrimination tests. Equal triangles were responded to similarly when one was inverted (Fig. 6F). Squares were oriented towards as often as circles having equal areas and contour lengths (perimeters) (Fig. 6G, H). Finally, despite the distinctive spination in the right-side silhouette of a Melongena corona (a major predator on Littorina), there was no significant tendency to avoid this shape in favour of an oval shape having the same area (Fig. 6I). Discussion Kirschfeld (1976) noted a relationship between resolution and the distance between the centre of the eye and the ground (body height) which is independent of the type of eye possessed (lens versus compound). Our data for L. irrorata, whose lens-type eye is positioned about 2 mm above the ground in adults, fit this relationship well. The detection test for horizontal dimension gave a threshold estimate (P = 0.05) of 0.9~ threshold estimates for vertical dimension were 2.4 ~ and 3.7 ~, with the shape centrally- and basally-positioned, respectively. It should be noted that our resolution threshold estimates for L. irrorata are a measure of the smallest
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Fig. 6. Directional responses of nine groups of 40 snails each to pairs of test shapes, where the members of each pair were centred 80 ~ apart. Pairs A to E involve 1.3-emwide bars. Pairs G and I had equal areas and pair H had equal contour lengths (perimeters).
shape visible, while the resolution estimates for most species which Kirschfeld considered are a measure of the most closely-spaced pattern of stripes visible. A two-choice discrimination test indicated no preference between centrally- and basallypositioned shapes. However, the lower threshold estimate and different curve shape for the hori-~ zontal dimension test, and the significant preference for vertical over horizontal bars in discrimination tests, clearly show that L. irrorata can distinguish shape orientation. Figure 6C demonstrates that the different responses do not simply reflect a preference f o r absolute height over absolute width; the diagonal bar was as high as the vertical bar and had a greater horizontal dimension, yet the vertical bar was clearly preferred.
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The ecological importance of vertical plant stems to L. irrorata (Hamilton 1976) invites speculation about the significance of the vertical bar preference demonstrated in laboratory arenas. However, preliminary tests reveal that a significant preference for vertical bars over horizontal bars is also exhibited by the rocky intertidal littorinid, Tectarius murieatus. Also, Messenger & Sanders (1972) found that untrained Octopus preferred vertical rectangles over horizontal ones. Evans (1961) concluded that L. punctata could see silhouettes of terrestrial objects at night. Hamilton (1978) found that L. irrorata orient onshore at night with only a starlit sky, and that the same response during the day is visually mediated. However, our detection series of tests involving different arena light levels gave a threshold estimate of only 4.3 lx for the 5~ wide black test shape A lower threshold estimate might have been obtained if each snail had been given time to adapt to the light level present in its arena before testing. Instead, all test snails were exposed to illumination of about 2150 lx in the holding chamber for 2-10 h before testing. Detection tests using larger shapes than our 5 ~ wide black rectangles would presumably also give lower threshold estimates. The shape reflectance tests revealed unexpectedly good ability at detecting a difference at the high end of the reflectance scale. Test shape E in Fig. 5 corresponds to a value of 0.10 on the Kodak grey scale, which is an 'off-white' (Kodak scale values are inversely related to reflectance). This finding was predicted during control tests in the newly-constructed arenas. We found that great care had to be taken to ensure that the inner walls were homogeneously painted and that light reflecting upward from the mirror did not cause differential brightness of the walls. Ability to detect shoreline silhouettes at night would require equally good discrimination at the low end of the reflectance scale. The threshold estimates obtained in the current study should be conservative because change in the oriented movements of untrained animals comprises the measure o f response to visual stimuli. While test animals were maintained in the laboratory, we attempted to keep constant those exogenous factors presumably influencing 'motivation' to approach a dark object, but some variability in response still existed, even for stimuli well above threshold. However, the response thresholds obtained by our study are
HAMILTON & WINTER: VISUAL RESPONSES BY LITTORINA biologically meaningful, in p a r t because they are for n o r m a l (i.e. untrained) animals. I n o u r detection tests, the relative sizes o f the shapes varied d e p e n d i n g on the distances o f the test a n i m a l s f r o m them. The shape dimensions (degrees) given a b o v e were defined with reference to the a r e n a centre, which is where all snails were initially released. Snails whose p a t h s t o o k t h e m further a w a y f r o m a shape saw a relatively smaller shape, while snails whose p a t h s t o o k t h e m closer to a shape saw a relatively larger shape. W e believe that these position effects have n o t biased the d a t a because o f the balance achieved by initially facing a n equal n u m b e r o f animals t o w a r d , 90 ~ to the right, 180 ~ away, a n d 90 ~ to the left o f a test shape. D e t a i l e d analysis o f test snails' paths m i g h t p e r m i t d e t e r m i n a t i o n o f the actual distances at which directional 'decisions' are made. Such an analysis is p l a n n e d for the future. V a r i o u s considerations s u p p o r t the hypothesis t h a t L. irrorata sees better t h a n m o s t gastropods. I n t e r t i d a l species active at low tide experience substantial light levels during d a y t i m e activity periods, a n d significant convergence o f light at the cornea. Thus, these g a s t r o p o d s should have better vision t h a n n o c t u r n a l l a n d p u l m o n a t e s or s u b m e r g e d species. W h i l e L. irrorata is n o t the only intertidal g a s t r o p o d active in air, the slight slope o f its m a r s h h a b i t a t (less t h a n 3 ~) m a k e s geotactic o r i e n t a t i o n unreliable. This e n v i r o n m e n t a l factor m a y have resulted in greater dependence on vision in L. irrorata t h a n in g a s t r o p o d s i n h a b i t i n g steeply sloping intertidal areas. B e h a v i o u r a l studies o f g a s t r o p o d s occupying other habitats will test this hypothesis.
Acknowledgments W e t h a n k A. Clements a n d J. P e n n for suggestions a n d assistance, a n d D. D e a n a n d B. Russell for o b t a i n i n g p r e l i m i n a r y data. The research was s u p p o r t e d by an N S F G r a n t (BNS 7916358) to P V H .
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Bohn, G. 1905. Attractions et oscillations des animaux marins sous l'imqnence de la lumi6re. Mem. Inst. gen. PsychoL, 1, 1-111. yon Buddenbrock, W. 1919. Analyse der Lichtreaktionen der Heliciden. Zool. Jb. Abt. allg. Zool. Physiol., 37, 315-360. Burdon-Jones, C. & Charles, G. H. 1958. Light responses of littoral gastropods. Nature, Lond., 181, 129-131. Charles, G. H. 1961. The mechanism of orientation of freely moving Littorina littoralis (L.) to polarized light. J. exp. Biol., 38, 203-212. Charles, G. H. 1966. Sense organs (less cephalopods). In: Physiology ofMollusca, Vol. 2 (Ed. by K. Wilbur & C. M. Yonge), pp. 455-521. New York: Academic Press. Chelazzi, G. & Vannini, M. 1976. Researches on the coast of Somalia. The shore and dune of Sat Uanle. 9. Coastward orientation after displacement in Nerita textilis Dillwyn (Gastropoda, Prosobranchia). Monit. ZooL Ital. (NS), Suppl. 7, 161-178. Dennis, M. J. 1967. Electrophysiology of the visual system in a nudibranch mollusc. J. NeurophysioL, 30, 1439-1465. Evans, F. 1961. Responses to disturbance of the periwinkle Littorina punctata (Gmelin) on a shore in Ghana. Proc. Zool. Soe. Lond., 137, 393-402. Field, L. H. 1977. An experimental analysis of the escape response of the gastropod Strombus maculatus. Pac. Sci., 31, 1-11. Geismer, A. 1935. Die lokomotorischen Reaktionen von Helix pomatia auf Helligkeit und Dunkelheit. ZooL Jb. Abt. allg. Zool. Physiol., 55, 95-130. Goldman, T. & Hermann, H. 1967. Photic responses in optic nerve of Helicacea. Vis. Res., 7, 533-537. Hamilton, P. V. 1976. Predation on Littorina irrorata (Mollusca: Gastropoda) by CalIinectes sapidus (Crustacea: Portunidae). Bull. mar. Sei., 26, 403-409. Hamilton, P. V. 1977a. Daily movements and visual relocation of plant stems by Littorina irrorata (Mollusca: Gastropoda). Mar. Behav. Physiol., 4, 293-304. Hamilton, P. V. 1977b. Tile use of mucous trails in gastropod orientation studies. Malac. Rev., 10, 73-76. Hamilton, P. V. 1978. The role of vision in adaptive oriented movements of Littorina irrorata (MoP lusca: Gastropoda) when displaced from their natural habitat. Mar. Behav. Physiol., 5, 255-271. Hamilton, P. V. & Russell, B. J. 1982. Celestial orientation by surface-swimming ApIysia brasiliana Rang (Mollusca: Gastropoda). Y. exp. mar. Biol. Ecol., 56, 145-152. Hermann, H. T. 1968. Optic guidance of locomotor behavior in the land snail Otala lactea. Vis. Res., 8, 601-612. Kirschfeld, K. 1976. The resolution of lens and compound eyes. In: Neural Principles in Vision (Ed. by F. Zettler & R. Weiler), pp. 354-369. Berlin: SpringerVerlag. Land, M. F. 1981. Optics and vision in invertebrates. In: Handbook of Sensory Physiology, Vol. 6B (Ed. by H. Autrum), pp. 471-592. Berlin: Springer-Verlag. Messenger, J. B. & Sanders, G. D. 1972. Visual preference and two-cue discrimination learning in Octopus. Anita. Behav., 29, 580-585.
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Newell, G. E. 1958a. The behaviour of Littorina littorea (L.) under natural conditions and its relation to position on the shore. J. mar. BioL Ass. U.K., 37, 229-239. Newell, G. E. 1958b. An experimental analysis of the behaviour of Littorina littorea (L.) under natural conditions and in the laboratory. J. Mar. Biol. Ass. U.K., 37, 241-266. Newell, G. E. 1965. The eye of Littorina littorea. Proc. ZooL Soc. Loud., 144, 75-86. Newell, P. F. & Newell, G. E. 1968. The eye of the slug, Agriolimax reticulatus (Mull.). Symp. ZooL Soc. Lond., 23, 97-111. Riggs, L. A. 1965. Visual acuity. In: Vision and Visual Perception (Ed. by C. H. Graham), pp. 321-349. New York: John Wiley. Stensaas, L. J., Stensaas, S. S. & Trujillo-Cenoz, O. 1969. Some morphological aspects of the visual system of Hermissenda crassicornis (Mollusca :Nndibranchia) J. Ultrastr. Res., 27, 510-532.
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Stoll, C. J. 1973. On the role of the eyes and non-ocular light receptors in orientational behavior of Lymnaea stagnalis (L.). Proc. KoninkL Nederl. Akad. Wetenschappen Series C, 76, 203-214. Teller, D. Y., Morse, R., Borton, R. & Regal, D. 1974. Visual acuity for vertical and diagonal gratings in human infants. Vis. Res., 14, 1433 1439. Warburton, K. 1973. Solar orientation in the snail Nerita plicata (Prosobranchia: Neritacea) on a beach near Watamu, Kenya. Mar. BioL, 23, 93-100. Willows, A. O. D. 1973. Learning in gastropod mollusks. In: Invertebrate Learning, Vol. 2 (Ed. by W. C. Coming, J. A. Dyal & A. O. D. Willows), pp. 187-273. New York: Plenum Press. Zar, J. H. 1974. Biostatistical Analysis'. Englewood Cliffs: Prentice-Hall. (Received 8 September 1981 ; revised 14 December 1981 ; MS. number: A2717)
LUCAS: ANTLION PIT CONSTRUCTION PLATE
I
Fig. 2. Photograph of a completed antlion pit showing the distribution of fine (white) and coarse (black) sand grains. (A) Pit wall lined with white sand. (B) Position of black sand 'ring'. The white line marks the pit edge.
Lucas, Anita. Behav., 30, 3
ANIMAL
BEHAVIOUR, PLATE
30,
3
II
Fig. 5. Photograph of an antlion pit in construction showing the distribution of fine (white) and coarse (black) sand grains. (A) Position of antlion in trough of pit. The white line marks the pit edge.
Lucas, Anita. Behav., 30, 3
BEHAVIOURAL RESPONSES TO VISUAL STIMULI BY THE SNAIL LITTORINA IRRORATA BY P. V. H A M I L T O N & M. A. W I N T E R
Department of Biology, University of West Florida, Pensacola, FL 32504 Abstract. The visual capabilities of gastropod molluscs and most other invertebrates possessing structurally simple eyes are poorly known. We studied vision in untrained marsh periwinkles (Littorina irrorata) in the laboratory, using oriented movements toward test shapes as the response measure. This intertidal species is active when exposed at low tide, both during the day and at night, and it travels vertically on plant stems with a tidal rhythm. In detection tests, the estimated response threshold for a single vertical bar was 0.9 ~, while the response threshold for an equal-size horizontal bar was 2.4 ~ or 3.7 ~, depending on bar position. Snails detected a 5~ bar in 4.3 lx of light and a 40~ square having about 95 % reflectance ('off-white') on a white (100 ~ nominal reflectance) background in 2800 lx. Discrimination tests revealed a strong preference for vertical bars over both diagonal and horizontal bars of the same width, but no preferences in several other situations. Various factors suggest that L. irrorata may see better than most other gastropods. The structurally simple eyes of gastropod molluscs and many non-arthropod invertebrates are often assumed to provide information on gross differences in light intensity, but not to form images. There are two weaknesses to this assumption. First, ideas about vision in gastropods are based primarily on superficial comparisons with the structurally complex vertebrate eye. Neurophysiological and behavioural data on the visual responses of gastropods are generally lacking. Second, the fact that 'there is no clear break in the spectrum of resolving power that different eyes show' (Land 1981) makes usage of the term 'image' ambiguous in comparative studies. Although vision has not been evaluated systematically in any gastropod, scattered behaviouraI, neurophysiological, and optical studies suggest an ability to see biologically relevant stimuli. Field experiments have demonstrated oriented responses to the sun in Littorina Bttorea (Newell 1958a, b), L. punctata (Evans 1961), and Nerita plicata (Warburton 1973), to unidentified celestial cues in Aplysia brasiliana (Hamilton & Russell 1982), to shoreline topographic features and nocturnal silhouettes of vegetation in L. punctata (Evans 1961) and N. textilis (Chelazzi & Vannini 1976), and to large areas of vegetation and individual plant stems in L. irrorata (Hamilton 1977a, 1978). Vision may help maintain a straight path when Strombus is escaping potential predators (Field 1977). Vision is apparently important in predation by heteropods (Land 1981). Laboratory experiments have demonstrated oriented re-
sponses to polarized light in Littorina and Nassarius (Burdon-Jones & Charles 1958; Baylor 1959; Charles 1961), to dark screens on a white background in Helix and Littorina (Bohn 1905; von Buddenbrock 1919; Bierens de Harm 1921; Geismer 1935; Charles 1966), and to darkened or lighted areas in Otala and Lymnaea (Hermann 1968; Stoll 1973). Electrophysiological studies have demonstrated responses traditionally associated with pattern detecting eyes, such as lateral inhibitory interactions, in Hermissenda (Dennis 1967; Stensaas et al. 1969) and Otala (Goldman & Hermann 1967). Optical measurements on the eye of L. littorea suggest that this species may be able to form sharp retinal images in air (Newell t965). Similar measurements for the nocturnal slug Agriolimax retieulatus suggest poorer visual acuity (Newell & Newell 1968). In this study of the marsh periwinkle, Littorina irrorata Say, we examine the responses of untrained animals to various test shapes presented under controlled lighting conditions. Our experimental design follows the recommendation of Riggs (1965) that detection tests of acuity should employ dark shapes against bright backgrounds. We studied innate oriented responses to shapes because, unlike vertebrates, Octopus, and insects, gastropods are difficult to train (Willows 1973). Studies on human infants (e.g. Teller et al. 1974) and octopods (e.g. Messenger & Sanders 1972) show that meaningful data can be obtained using untrained subjects. 752
HAMILTON & WINTER: VISUAL RESPONSES BY LITTDRINA
753
We chose L. irrorata for this initial evaluation of vision in gastropod molluscs because field data indicated that this species has a distinct response to discrete objects in the environment. This snail feeds on the bottom subs~rate in marshy intertidal zones on both daytime and night-time low tides, and hence is active in an air medium. It ascends surrounding plant stems on the advancing tide, thereby avoiding benthic predators (Hamilton 1976, 1977a). As noted above, orientation toward plant stems is visually mediated.
Methods Apparatus One of the six identical arenas in which tests were conducted is shown in Fig. 1. The top section contained the light source and filters; its walls were constructed of perforated masonite to facilitate cooling. The lamp was a 250-W ECA incandescent bulb having a 3200 K colour temperature. A blue filter shifted this light to 5000 K, thus simulating natural sunlight. A diffusing filter eliminated the possibility of polarized light entering the arena. Neutral density filters were added to obtain lowered light intensities when desired. For tests in complete darkness, the lamp remained on, but several layers of black paper were added to block all light entering the arena. A 50-cm=long section of flat-white PVC plastic pipe (29.5 cm internal diameter) was permanently attached to the top section. The middle section consisted of a 30-cm-long section of the same pipe bonded to a 6-cm-thick disc of clear Plexiglass. Test shapes were attached to the lower wall of this section. A removable Plexiglass disc (3 m m thick, 29 cm diameter) was placed on the bottom of this section for each trial; it comprised the surface over which the test animal crawled. Arena illumination w a s measured on the surface of this disc with a photocell having peak sensitivity to 550 nm light (Clairex 750 HI,). A diffusing filter was attached beneath this section to eliminate directional light reflection from below. The bottom section contained a mirror and a small viewport on the side to permit the viewing of the test animal's shadow on the bottom of the middle section. The middle section sat on the bottom section, which rested on a table. Adjustable legs on the bottom section permitted levelling of the entire arena. The top section could be raised to change crawling surfaces and test animals.
--pp
I I0 r
I
~
PP
RD
' CP
DF
.|
Fig. 1. Schematic diagram of one of six identical arenas used in this study. (AL = adjustable leg, BF = blue filter, CG = clear glass, CP = clear Plexiglass bottom, DF = diffusing filter, LB = light bulb, M = mirror, PP = PVC pipe walls, RD. = removable Plexiglass disc, TT = table top). We cut black test shapes from paper and produced the series of test shapes having different reflectances photographically by visual matching with the K o d a k grey scale. Regardless of size, we glued each test shape to a 10.3-cm square piece of white paper and laminated the composite in clear plastic. Then we attached the resulting test card to the lower wall of the middle section of the arena with two-sided tape
Test Animals and Procedure We collected adult L. irrorata (shell length /> 13 ram) from Juncus marshes bordering
754
ANIMAL
BEHAVIOUR,
Santa Rosa Sound, Escambia County, Florida. We transported snails to the laboratory and maintained them in plastic containers (26 x 20 x 15 era) containing about 5 cm of aerated sea water. We kept the containers in a holding chamber containing fluorescent light (2150 lx) operated on approximately the natural photoperiod for the collection date. We did not feed the snails but we always tested them within 96 h after collection. We conducted two kinds of tests with the snails. The detection series of tests measured the tendency of snails to orient toward a single test card located against a white background. The discrimination series of tests compared the tendency of snails to orient toward one of two test cards on a white background. The light intensity at the crawling surface was 2800 lx for all tests except for the one detection test where intensity was the variable studied. In each detection test, we varied a single parameter among the six arenas. For example, when the parameter of horizontal dimension was studied, one arena contained a 10.3-cm-high black shape that filled 40 ~ of horizontal arc, one contained a 20~ shape, one a 10 ~ one a 5 ~ and one a 2.5~ the sixth arena contained a completely white test card and thus served as the control (see Fig. 3A). We individually released 24 snails in the centre of each arena. We systematically rotated initial facing directions, with an equal number of snails released facing toward, 90 ~ to the right, 180 ~ away, and 90 ~ to the left of the test card. In each discrimination test, we placed two test cards in each arena, centred 80 ~ apart. We released snails individually in the centre of an arena and faced them directly between the test cards. The width of each test card was exactly 40 ~. However, the widths of the shapes which the cards contained were not identical for all pairs tested (for example, see Fig. 6, A-C). Thus, to enable a balanced analysis, we considered all snails reaching the arena's edge anywhere within the arc subtended by a test card (40 ~ to have responded to the shape on that card. We ignored those few snails reaching the arena's edge outside the arcs subtended by test cards. We tested enough snails for each pair of cards so that 20 responses were recorded with 'X right, Y left' and 20 responses were recorded with 'X left, Y right'. This procedure eliminated the possibility of any innate turning preference biasing the results.
30,
3
In both kinds of tests, we considered a snail to have responded once it travelled 13 cm from its release point 0.e. 1.75 cm from the arena wall). We discarded any snail not responding within 15 rain and we released a new snail in its place. Once a snail responded, we removed it and the plastic disc it had crawled over, from the arena. We misted the disc and recorded the direction of the snail's final position from the arena centre to the nearest 5 ~. For the detection tests, we recorded the mucus trail as described in Hamilton (1977b). We thoroughly cleaned and dried each plastic disc before reuse. We tested each snail only once.
Data Analysis For the detection series of tests, we wanted to use a response measure that incorporated the actual direction taken by each animal because a test card might influence the direction an animal takes without the animal moving directly toward (or away from) the card. A response criterion that scored an animal as hitting or missing the card would not be sensitive to this kind of influence. This consideration suggested the use of a statistical test for circular distributions of directions called the V-test (Batschelet 1972), a procedure which tests the null hypothesis that the directions taken by a group of animals were randomly oriented against the alternative hypothesis that the animals oriented in a specified direction On this case, in the test card's direction). The magnitude of the V-test statistic (u) is a measure of the group's tendency to orient in the card's direction, However, the maximum value u may attain lacks intuitive meaning and varies with the sample size (N). For example, if 24 animals all move directly toward a test card, the u statistic would equal 6.928; 12 animals orienting directly toward the card would yield a u statistic equal to 4.899. As defined by Batschelet (1972), u is a simple function of V', which is the component of the resultant vector in the predicted direction. The quantity V' is computed from the set of directions taken by the animals, as described by Batschelet. Our study modifies the standard Vtest procedure by defining a new test statistic, v', as follows: V ! V t
m
N
H A M I L T O N & WINTER: VISUAL RESPONSES BY L I T T O R I N A
The quantity v' is the component of the mean vector in the predicted direction. If all animals in a group orient in the predicted direction (e.g. toward a test card's centre, then v' will equal 1.0 regardless of the sample size; if all animals orient directly away, v' will equal -- 1.0. Values of v' near zero indicate random orientation. Critical values of v' for hypothesis testing can be obtained directly from the critical values of u (as published in Batschelet 1972 or Zar 1974), using the following equation:
755
diagram. Figure 3A illustrates the six test cards and relates the horizontal dimensions of these cards to their corresponding response values. These data show that all cards possessing black shapes were responded to approximately equally, regardless of the shapes' horizontal dimensions. The threshold for a significant response (P---0.05) is about 0.9 ~. Figure 3B relates the vertical dimension of~a series of centrally-positioned shapes to their corresponding response values, and illustrates the six test cards. (Scatter diagrams are omitted for this and all subsequent detection tests to save space.) These data show a gradual decline in response proportional to vertical dimension, with a threshold at about 2.4 ~ When shapes having the same size and orientation were basallypositioned on the test cards (Fig. 3C), a similar gradual decline in response was evident, with a threshold at about 3.7 ~. The dip in the response curve at 40 ~ in Fig. 3C should not be interpreted as a significant change from the 20 ~ value, as the significance probabilities of both response values are less than 0.0001. We used the5~ shape from the horizontal dimension test (Fig. 3A) to explore the parameter of vertical dimension. Figure 3D relates the vertical dimension of a series of basallypositioned shapes to their corresponding re-
u V'erit - -
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Thus v' is the measure of oriented response used for all detection tests. For the discrimination series of tests, the numbers of snails responding to the two test cards were compared using the chi-squared test. Results The detection series of tests provided response curves and statistical thresholds for six stimulus parameters. Figure 2 shows scatter diagrams for the directions taken by L. irrorata in the horizontal dimension test. The degree of clumping of the directions around 0 ~ (the location of the test cards) is reflected by the v' value for each 0
0
.
0
180
180
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Fig. 2. Scatter diagrams showing the directions taken by six groups of 24 snails each in arenas having test shapes positioned at 0 ~ The test shapes, which varied in horizontal dimension, are illustrated in Fig. 3A. The letters A - F correspond between the two figures. The v' value is a measure of the degree of clumping of each group's directions toward the test shape.
756
ANIMAL
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Fig. 3. (A) Relationship between the horizontal dimension of a 10.3-cmhigh test shape and the measure of oriented response to that shape (v'), based on the data shown in Fig. 2. A v' value of 0.238 (dashed line) is required for a circular distribution of directions (N = 24) to be significantly different from random at P = 0.05. This consideration leads to the estimate of 0.9~ (heavy arrow) as the response threshold for horizontal dimension. (B) Relationship between the vertical dimension of a 10.3-cm-wide, centrallypositioned test shape and the response to that shape. The response threshold is 2.4~ (C) Relationship between the vertical dimension of a 10.3-cm-wide, basally-positioned test shape and the response to that shape. The response threshold is 3.7~ (D) Relationship between the vertical dimension of a 1.3-cm-wide (5~ basally-positioned test shape and the response to that shape. The response threshold is 7.5| . sponse values, a n d illustrates the six test cards. A gradual decline in response was evident, with a threshold at a b o u t 7.5 ~ Collectively, Fig. 3 A - D shows that t h e snails' response is n o t based o n a single linear d i m e n s i o n o f a test shape.
We used identical 5~ shapes in a test designed to determine the range o f light levels in which snails could orient visually. Figure 4 relates arena light intensity to the corresponding response values, a n d illustrates the test shape which was present in all arenas. A gradual
HAMILTON & WINTER: VISUAL RESPONSES BY L I T T O R I N A
decline in response was evident, with a threshold at about 4.3 lx. It should be noted that we computed the light intensities present in the four middle-intensity arenas by accounting for the effect o f the amount of neutral density filtration used, rather than by direct measurement. This was done because the photocell was sensitive to the small amount of long-wavelength light passed by the filters. Light intensity in the highestintensity arena was measured directly (2800 lx). Light intensity in the lowest-intensity arena was considered to be infinitely small, as layers of black paper blocked all light transmission. We used 40~ shapes having different reflectances to determine how much an object must contrast with a white background to elicit significant orientation. Figure 5 relates shape reflectance to the corresponding response values. The pure white (F) and pure black (A) cards are assigned reflectance values of 100% and 0% respectively, although these extreme values are not characteristic of any natural surfaces. A gradual decline in response with increasing reflectance was evident; a test card having less than 95%/00 reflectance was oriented towards significantly when located against the white (100 9/0 nominal) background of the arena walls. The results of the discrimination series of tests supported predictions generated from c o m p a r i n g the response thresholds from the detection tests. A vertical 10.3 x 1.3-cm black bar was oriented towards significantly more often than a centrally or basally-positioned horizontal bar of the same size (Fig. 6A, B). Interestingly, the same vertical bar was signifi1.0"
757
cantly preferred over a slanted bar reaching the same height (Fig. 6C), indicating that bar orientation was more important than bar length. However, with bars having an identical orientation (vertical), snails significantly preferred an 8-cm-high bar over one 4 cm high (Fig. 6D). Snails showed no preference between centrallyand basally-positioned horizontal bars (Fig. 6E). No significant preferences were exhibited in the final four discrimination tests. Equal triangles were responded to similarly when one was inverted (Fig. 6F). Squares were oriented towards as often as circles having equal areas and contour lengths (perimeters) (Fig. 6G, H). Finally, despite the distinctive spination in the right-side silhouette of a Melongena corona (a major predator on Littorina), there was no significant tendency to avoid this shape in favour of an oval shape having the same area (Fig. 6I). Discussion Kirschfeld (1976) noted a relationship between resolution and the distance between the centre of the eye and the ground (body height) which is independent of the type of eye possessed (lens versus compound). Our data for L. irrorata, whose lens-type eye is positioned about 2 mm above the ground in adults, fit this relationship well. The detection test for horizontal dimension gave a threshold estimate (P = 0.05) of 0.9~ threshold estimates for vertical dimension were 2.4 ~ and 3.7 ~, with the shape centrally- and basally-positioned, respectively. It should be noted that our resolution threshold estimates for L. irrorata are a measure of the smallest
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=2 0
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Fig. 5. Relationship between the reflectance of a 10.3-cm square test shape and the response to that shape. Dashed line and arrow as in Fig. 3. The response threshold is 95 %.
ANIMAL
758
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BEHAVIOUR,
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Fig. 6. Directional responses of nine groups of 40 snails each to pairs of test shapes, where the members of each pair were centred 80 ~ apart. Pairs A to E involve 1.3-emwide bars. Pairs G and I had equal areas and pair H had equal contour lengths (perimeters).
shape visible, while the resolution estimates for most species which Kirschfeld considered are a measure of the most closely-spaced pattern of stripes visible. A two-choice discrimination test indicated no preference between centrally- and basallypositioned shapes. However, the lower threshold estimate and different curve shape for the hori-~ zontal dimension test, and the significant preference for vertical over horizontal bars in discrimination tests, clearly show that L. irrorata can distinguish shape orientation. Figure 6C demonstrates that the different responses do not simply reflect a preference f o r absolute height over absolute width; the diagonal bar was as high as the vertical bar and had a greater horizontal dimension, yet the vertical bar was clearly preferred.
30,
3
The ecological importance of vertical plant stems to L. irrorata (Hamilton 1976) invites speculation about the significance of the vertical bar preference demonstrated in laboratory arenas. However, preliminary tests reveal that a significant preference for vertical bars over horizontal bars is also exhibited by the rocky intertidal littorinid, Tectarius murieatus. Also, Messenger & Sanders (1972) found that untrained Octopus preferred vertical rectangles over horizontal ones. Evans (1961) concluded that L. punctata could see silhouettes of terrestrial objects at night. Hamilton (1978) found that L. irrorata orient onshore at night with only a starlit sky, and that the same response during the day is visually mediated. However, our detection series of tests involving different arena light levels gave a threshold estimate of only 4.3 lx for the 5~ wide black test shape A lower threshold estimate might have been obtained if each snail had been given time to adapt to the light level present in its arena before testing. Instead, all test snails were exposed to illumination of about 2150 lx in the holding chamber for 2-10 h before testing. Detection tests using larger shapes than our 5 ~ wide black rectangles would presumably also give lower threshold estimates. The shape reflectance tests revealed unexpectedly good ability at detecting a difference at the high end of the reflectance scale. Test shape E in Fig. 5 corresponds to a value of 0.10 on the Kodak grey scale, which is an 'off-white' (Kodak scale values are inversely related to reflectance). This finding was predicted during control tests in the newly-constructed arenas. We found that great care had to be taken to ensure that the inner walls were homogeneously painted and that light reflecting upward from the mirror did not cause differential brightness of the walls. Ability to detect shoreline silhouettes at night would require equally good discrimination at the low end of the reflectance scale. The threshold estimates obtained in the current study should be conservative because change in the oriented movements of untrained animals comprises the measure o f response to visual stimuli. While test animals were maintained in the laboratory, we attempted to keep constant those exogenous factors presumably influencing 'motivation' to approach a dark object, but some variability in response still existed, even for stimuli well above threshold. However, the response thresholds obtained by our study are
HAMILTON & WINTER: VISUAL RESPONSES BY LITTORINA biologically meaningful, in p a r t because they are for n o r m a l (i.e. untrained) animals. I n o u r detection tests, the relative sizes o f the shapes varied d e p e n d i n g on the distances o f the test a n i m a l s f r o m them. The shape dimensions (degrees) given a b o v e were defined with reference to the a r e n a centre, which is where all snails were initially released. Snails whose p a t h s t o o k t h e m further a w a y f r o m a shape saw a relatively smaller shape, while snails whose p a t h s t o o k t h e m closer to a shape saw a relatively larger shape. W e believe that these position effects have n o t biased the d a t a because o f the balance achieved by initially facing a n equal n u m b e r o f animals t o w a r d , 90 ~ to the right, 180 ~ away, a n d 90 ~ to the left o f a test shape. D e t a i l e d analysis o f test snails' paths m i g h t p e r m i t d e t e r m i n a t i o n o f the actual distances at which directional 'decisions' are made. Such an analysis is p l a n n e d for the future. V a r i o u s considerations s u p p o r t the hypothesis t h a t L. irrorata sees better t h a n m o s t gastropods. I n t e r t i d a l species active at low tide experience substantial light levels during d a y t i m e activity periods, a n d significant convergence o f light at the cornea. Thus, these g a s t r o p o d s should have better vision t h a n n o c t u r n a l l a n d p u l m o n a t e s or s u b m e r g e d species. W h i l e L. irrorata is n o t the only intertidal g a s t r o p o d active in air, the slight slope o f its m a r s h h a b i t a t (less t h a n 3 ~) m a k e s geotactic o r i e n t a t i o n unreliable. This e n v i r o n m e n t a l factor m a y have resulted in greater dependence on vision in L. irrorata t h a n in g a s t r o p o d s i n h a b i t i n g steeply sloping intertidal areas. B e h a v i o u r a l studies o f g a s t r o p o d s occupying other habitats will test this hypothesis.
Acknowledgments W e t h a n k A. Clements a n d J. P e n n for suggestions a n d assistance, a n d D. D e a n a n d B. Russell for o b t a i n i n g p r e l i m i n a r y data. The research was s u p p o r t e d by an N S F G r a n t (BNS 7916358) to P V H .
REFERENCES Batschelet, E. 1972. Recent statistical methods for orientation data. In: Animal Orientation and Navigation (Ed. by S. R. Galler, K. Schmidt-Koenig, G. J. Jacobs & R. E. Belleville), pp. 61-91. Washington, D. C.: National Aeronautics & Space Administration. Baylor, E. R. 1959. The responses of snails to polarized light. J. exp. Biol., 36, 369-376. Bierens de Harm, J. A. 1921. Phototaktische Bewegungen yon Tieren bei doppelter Reizquelle. Biol. Zbl., 41, 395-414.
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Bohn, G. 1905. Attractions et oscillations des animaux marins sous l'imqnence de la lumi6re. Mem. Inst. gen. PsychoL, 1, 1-111. yon Buddenbrock, W. 1919. Analyse der Lichtreaktionen der Heliciden. Zool. Jb. Abt. allg. Zool. Physiol., 37, 315-360. Burdon-Jones, C. & Charles, G. H. 1958. Light responses of littoral gastropods. Nature, Lond., 181, 129-131. Charles, G. H. 1961. The mechanism of orientation of freely moving Littorina littoralis (L.) to polarized light. J. exp. Biol., 38, 203-212. Charles, G. H. 1966. Sense organs (less cephalopods). In: Physiology ofMollusca, Vol. 2 (Ed. by K. Wilbur & C. M. Yonge), pp. 455-521. New York: Academic Press. Chelazzi, G. & Vannini, M. 1976. Researches on the coast of Somalia. The shore and dune of Sat Uanle. 9. Coastward orientation after displacement in Nerita textilis Dillwyn (Gastropoda, Prosobranchia). Monit. ZooL Ital. (NS), Suppl. 7, 161-178. Dennis, M. J. 1967. Electrophysiology of the visual system in a nudibranch mollusc. J. NeurophysioL, 30, 1439-1465. Evans, F. 1961. Responses to disturbance of the periwinkle Littorina punctata (Gmelin) on a shore in Ghana. Proc. Zool. Soe. Lond., 137, 393-402. Field, L. H. 1977. An experimental analysis of the escape response of the gastropod Strombus maculatus. Pac. Sci., 31, 1-11. Geismer, A. 1935. Die lokomotorischen Reaktionen von Helix pomatia auf Helligkeit und Dunkelheit. ZooL Jb. Abt. allg. Zool. Physiol., 55, 95-130. Goldman, T. & Hermann, H. 1967. Photic responses in optic nerve of Helicacea. Vis. Res., 7, 533-537. Hamilton, P. V. 1976. Predation on Littorina irrorata (Mollusca: Gastropoda) by CalIinectes sapidus (Crustacea: Portunidae). Bull. mar. Sei., 26, 403-409. Hamilton, P. V. 1977a. Daily movements and visual relocation of plant stems by Littorina irrorata (Mollusca: Gastropoda). Mar. Behav. Physiol., 4, 293-304. Hamilton, P. V. 1977b. Tile use of mucous trails in gastropod orientation studies. Malac. Rev., 10, 73-76. Hamilton, P. V. 1978. The role of vision in adaptive oriented movements of Littorina irrorata (MoP lusca: Gastropoda) when displaced from their natural habitat. Mar. Behav. Physiol., 5, 255-271. Hamilton, P. V. & Russell, B. J. 1982. Celestial orientation by surface-swimming ApIysia brasiliana Rang (Mollusca: Gastropoda). Y. exp. mar. Biol. Ecol., 56, 145-152. Hermann, H. T. 1968. Optic guidance of locomotor behavior in the land snail Otala lactea. Vis. Res., 8, 601-612. Kirschfeld, K. 1976. The resolution of lens and compound eyes. In: Neural Principles in Vision (Ed. by F. Zettler & R. Weiler), pp. 354-369. Berlin: SpringerVerlag. Land, M. F. 1981. Optics and vision in invertebrates. In: Handbook of Sensory Physiology, Vol. 6B (Ed. by H. Autrum), pp. 471-592. Berlin: Springer-Verlag. Messenger, J. B. & Sanders, G. D. 1972. Visual preference and two-cue discrimination learning in Octopus. Anita. Behav., 29, 580-585.
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Newell, G. E. 1958a. The behaviour of Littorina littorea (L.) under natural conditions and its relation to position on the shore. J. mar. BioL Ass. U.K., 37, 229-239. Newell, G. E. 1958b. An experimental analysis of the behaviour of Littorina littorea (L.) under natural conditions and in the laboratory. J. Mar. Biol. Ass. U.K., 37, 241-266. Newell, G. E. 1965. The eye of Littorina littorea. Proc. ZooL Soc. Loud., 144, 75-86. Newell, P. F. & Newell, G. E. 1968. The eye of the slug, Agriolimax reticulatus (Mull.). Symp. ZooL Soc. Lond., 23, 97-111. Riggs, L. A. 1965. Visual acuity. In: Vision and Visual Perception (Ed. by C. H. Graham), pp. 321-349. New York: John Wiley. Stensaas, L. J., Stensaas, S. S. & Trujillo-Cenoz, O. 1969. Some morphological aspects of the visual system of Hermissenda crassicornis (Mollusca :Nndibranchia) J. Ultrastr. Res., 27, 510-532.
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Stoll, C. J. 1973. On the role of the eyes and non-ocular light receptors in orientational behavior of Lymnaea stagnalis (L.). Proc. KoninkL Nederl. Akad. Wetenschappen Series C, 76, 203-214. Teller, D. Y., Morse, R., Borton, R. & Regal, D. 1974. Visual acuity for vertical and diagonal gratings in human infants. Vis. Res., 14, 1433 1439. Warburton, K. 1973. Solar orientation in the snail Nerita plicata (Prosobranchia: Neritacea) on a beach near Watamu, Kenya. Mar. BioL, 23, 93-100. Willows, A. O. D. 1973. Learning in gastropod mollusks. In: Invertebrate Learning, Vol. 2 (Ed. by W. C. Coming, J. A. Dyal & A. O. D. Willows), pp. 187-273. New York: Plenum Press. Zar, J. H. 1974. Biostatistical Analysis'. Englewood Cliffs: Prentice-Hall. (Received 8 September 1981 ; revised 14 December 1981 ; MS. number: A2717)
LUCAS: ANTLION PIT CONSTRUCTION PLATE
I
Fig. 2. Photograph of a completed antlion pit showing the distribution of fine (white) and coarse (black) sand grains. (A) Pit wall lined with white sand. (B) Position of black sand 'ring'. The white line marks the pit edge.
Lucas, Anita. Behav., 30, 3
ANIMAL
BEHAVIOUR, PLATE
30,
3
II
Fig. 5. Photograph of an antlion pit in construction showing the distribution of fine (white) and coarse (black) sand grains. (A) Position of antlion in trough of pit. The white line marks the pit edge.
Lucas, Anita. Behav., 30, 3