PAPER Using Red Light with Fixed-site Video Cameras to Study the Behavior of the Spiny , argus, and Associated at Night and Inside Their Shelters

AUTHORS ABSTRACT Howard M. Weiss Fixed-site video cameras can be a powerful tool for studying marine animals in the sea 1 Project Oceanology without disturbing their behavior. Artificial light is required to use these cameras at night or Enrique Lozano-Álvarez in dark places such as inside dens. Red light is theoretically the best choice because Patricia Briones-Fourzán the eyes of many marine animals are relatively insensitive to light above 600 nm wavelength, Fernando Negrete-Soto red light penetrates water much further than infrared, and many video cameras are highly Universidad Nacional Autónoma de México2 sensitive to red light. This study found that video and red light can be used at night in the sea to study the behavior of , , without significant effects. The shelter occupancy rate of tethered was similar in continuous red light as in the dark and red light did not attract or repel free-living lobsters. Red light did attract a small Introduction additional number of fish which were already nearby the lobster shelters and did not appear ideo surveillance systems provide a to disturb the lobsters. Loss of P. argus from octopus predation was similar in red light as powerful tool for continuously monitoring the in the dark. Six species of predators (two triggerfishes, an octopus, two snappers, and a Vin situ behavior of marine animals over long moray eel) were recorded on videotape killing lobsters at shelters in the sea. Predation time periods, ranging from days to years. Un- usually occurred outside the shelters. Other species scavenged on the lobster remains after derwater video has been used since the 1950’s they were killed. A variety of animals frequently cohabited with lobsters inside shelters for to study the behavior, distribution, and abun- a few minutes to several days. The interactions of these animals with the lobsters rarely dance of marine and freshwater organisms involved any strong aggression or defensive behavior. (Myrberg, 1973). Today, inexpensive, highly sensitive and miniaturized CCD (charge study, and can be used at depths, in small maintain and operate than fixed-site camera couple device) cameras easily fit into small spaces (e.g., inside animal dens), and at times mounts. Furthermore, the thruster noise, watertight housings. They can be connected (e.g., during storms) which would be pro- lights, and motion of an ROV disturb the to large capacity digital recording and storage hibitive for divers. A complete video system, behavior of lobsters (Spanier et al., 1994) and devices which are relatively inexpensive and, including multiple cameras, fixed-site camera probably many other benthic animals. An in some models, portable and small enough mounts, time-lapse video recorder and multi- ROV can be left motionless at a study site for to be placed in watertight housings. These plexer, provides a permanent record which long periods of time to avoid these distur- technological advances have significantly im- can be repeatedly reviewed at various speeds bances. This is, however, an inefficient use of proved the capability, utility and availability and assessed by several independent viewers. the costly and sophisticated motility capabili- of underwater video in marine research. It also allows for simultaneous observations ties of an ROV. Underwater video cameras mounted at and recordings from cameras placed at differ- Inexpensive black and white 1/3–1/2" fixed locations on the seafloor have many ad- ent locations (e.g., experimental and control CCD video cameras commonly used in the vantages over direct diver observations or diver sites, and/or inside and outside of a shelter). As surveillance industry can be used at very low held cameras (Jury et al., 2001; Mills et al., a result, in situ mounted underwater video light intensities (typically 0.01–0.05 lux) and 2005). Fixed-site video cameras can be de- surveillance systems are being used in an in- are sensitive to the red and infrared portion of ployed for unlimited time, minimize the dis- creasing number of studies of marine animal the light spectrum (Figure 1). Color video turbance from divers on the behaviors under behavior (e.g., Burrows et al., 1999; Willis cameras of comparable price and size require and Babcock, 2000; Jury et al., 2001; Oliver more light (typically a minimum of 0.3 lux) Footnotes et al., 2005; Barans et al., 2005). and are not as sensitive to the longer wave- 1 Avery Pt., Groton, CT 06355 Some of these advantages can also be lengths of visible and near visible light. The 2 Instituto de Ciencias del Mar y Limnología, achieved by using cameras mounted to re- intensities of moonlight or starlight at the sur- Unidad Académica Puerto Morelos, PO Box motely operated vehicles (ROVs). However, face are approximately 3 × 10-3 to 2 × 10-4 lux, 1152, Cancún, QR 77500, México ROVs are much more expensive to purchase, respectively (McFarland, 1986; McMahon

86 and Holanov, 1995). Therefore, artificial light- FIGURE 1 ing must be provided to use any of these cam- Spectra of: (1) sensitivity of the eyes of the spiny lobster, Panulirus argus (Cummins et al., 1984) and the eras underwater at night. octopus Octopus vulgaris (Hamasaki, 1968), (2) absorbance by the long-wavelength-sensitive pigment The use of red or infrared lighting with of a cichlid fish, Cichlasoma longimanus (Levine and MacNichol, 1982); (3) emission from the red light these video systems has several advantages, in- used in the present study, and (4) response of monochrome CCD video camera (Sony, Inc.). cluding: (1) CCD video cameras are very sensi- tive to these wavelengths; (2) the eyes of many marine animals are relatively insensitive to red light, and probably incapable of perceiving in- frared light; and (3) the scattering coefficient of light in water decreases as the wavelength in- creases. In the red and near infrared part of the spectrum, scattering can be virtually discounted (Auster et al., 1990). The major disadvantage of red and infrared light is that the attenuation coefficient and absorption of light in water in- creases dramatically as the light wavelength in- creases into the visible red region and then in- creases exponentially in the infrared region (Jerlov, 1976; Kirk, 1994). Mills et al. (2005), using data from Kirk (1994), calculated that 72% of 680 nm high-red light is transmitted in water at a distance of 1 m and this reduces to 14% at infrared wavelengths of 845 nm. Due to this differential absorption in water, visible 1990; Spanier et al., 1994; Meisel et al., 2003; Video monitoring is a powerful tool for red lights provide much brighter illumination Mills et al., 2005). studying the behavioral interactions and ac- than infrared lights for the same power con- Many fishes, unlike most invertebrates, tivity rhythms of lobsters and associated ani- sumption (Mills et al., 2005). have color vision. They are able to distinguish mals, including their predators, in their natu- The spectral sensitivity of the vision for colors because their eyes contain three differ- ral environment. Video recordings provide λ many animals has been determined in the labo- ent retinal pigments each with a different max precise measurements of the time of day and ratory by measuring the electrical responses of (Levine and MacNichol, 1982). The pigment duration of behaviors as well as a view of λ their eye receptors or the absorption spectra of with the longest max is sensitive to red light these behaviors which can be analyzed frame their visual pigments over a range of wave- (Figure 1). by frame in slow motion. Most lobster spe- lengths of light (Cronin, 1986). The vision The eyes of most marine animals can de- cies, including P. argus, are nocturnal ani- for most marine invertebrates reaches a maxi- tect light at very low intensities when adapted mals, remaining inside shelters during the λ mum sensitivity at wavelengths ( max) between to the dark (Cronin, 1986). Therefore, a red day and actively foraging outside their shel- 450 nm and 550 nm (Cronin, 1986). For light source may emit only a few photons of ters at night (Phillips et al., 1980). Many λ example, a max of 510 nm has been deter- light energy at wavelengths which are visible other animals living in Caribbean reef sys- mined for the Caribbean spiny lobster, to an animal, but this may be sufficient to tems have distinctive day-night activity Panulirus argus (Cummins et al., 1984) and excite the animal’s photochemical system rhythms (e.g., Robblee and Ziemann, 1984; for the , Homarus americanus (McFarland, 1986; Widder et al., 2005). The Nagelkerken et al., 2000). Some of these λ (Bruno et al., 1977). The max for the com- sensitivity threshold or absolute sensitivity of animals are potential predators on lobsters, mon octopus, Octopus vulgaris, is 480 nm a species to light of any spectral distribution is may share or compete with lobsters for shel- (Hamasaki, 1968). The spectral sensitivity usually determined by measuring its behav- ters, or may have other associations with curves reported for these species (Figure 1) ioral response, such as phototaxis (Cronin, lobsters. Video monitoring at night using show a very rapid decline at wavelengths longer 1986). However, there are few published stud- minimally obtrusive lighting is essential to than about 550 nm. From this it has been ies which experimentally assess the effect of fully understand the behavior of lobsters inferred, perhaps incorrectly, that lobsters, oc- red light on the behavior of marine animals in and associated animals. topuses and most other marine invertebrates the field. Widder et al. (2005) found that red Properties of shelters and shelter-related cannot perceive wave lengths greater than 600 light was detectable and aversive to fish in behavior have been widely studied in spiny nm and that their behavior is minimally or deep water (520 m) but that the fish avoided lobsters (e.g., Herrnkind and Butler, 1986; not at all affected by red light (Auster et al., white light significantly more than red light. Spanier and Zimmer-Faust, 1988; Eggleston

Fall 2006 Volume 40, Number 3 87 et al., 1990; Eggleston and Lipcius, 1992; Methods A video camera and red light were placed Mintz et al., 1994) and American lobsters Our study site was located in Puerto 1.5 m in front of each crevice shelter. They (e.g., Karnofsky et al., 1989; Wahle and Morelos, Mexico (20° 51’N, 86° 55’W), in were attached to an aluminum frame anchored Steneck, 1992). Most of these studies have the reef lagoon between the shore and the to a cement base. The camera was mounted at been limited to diver observations from out- Mesoamerican Barrier Reef that extends along 80 cm above the seafloor and the light at 63 side the shelters in the field or have used the Caribbean coast of the Yucatan Peninsula. cm. The 1/2" CCD black and white video shelters in aquaria in the laboratory (e.g., Cobb Our studies were conducted in seagrass beds cameras (AW CCTV Model CC-2) have a 1971, 1981). It is especially important to about 150 m from shore and 2.5 m deep. 0.015 lux sensitivity, a 5 mm auto-iris wide understand the behavior of spiny lobsters These seagrass beds are typical habitat for ju- angle lens and a resolution of 500 horizontal inside their shelters since two or more lob- venile spiny lobsters which occupy crevice- TV-lines. They were placed in clear polycar- sters often occupy the same den and may type shelters among the seagrass. This habitat bonate watertight housings (Ikelight). The communally defend it against predators has been described in detail by Lozano-Álvarez recorded viewing cross-section at the front of (Zimmer-Faust and Spanier, 1987). How- and Spanier (1997). the shelter was 120 cm wide × 42 cm high. ever, it is difficult to make direct diver obser- Depending on the water clarity the viewing vations inside lobster shelters owing to their Effects of Red Light on the distance was up to about 10 m during the small size and low light levels. These charac- Behavior of P. argus and day and up to about 3 m at night using the teristics make them excellent candidates for Associated Animals red lights. studies using small video cameras with red To analyze the effects of red light on the The lights were 12 v, 50 w, type EXN light illumination. Lozano-Álvarez and behavior of P. argus and associated animals, we halogen flood bulbs (G.E. model Precise Briones-Fourzán (2001) and Segura-García used small, artificial crevice-type dens that pro- MR16 ConstantColor) with a peak luminous et al. (2004) have used this methodology in vided a shelter similar to the crevices used by intensity of 1450 candelas and a 40° angle the laboratory to study the in-shelter behav- juvenile lobsters throughout the sea grass beds. beam spread. These bulbs were mounted in a ior of two species of spiny lobsters, P. argus Four of the crevice shelters were placed on the brass watertight housing with a red filter disc and P. guttatus. bottom, 7 m apart from each other. Each shel- made of 1/8" (3 mm) thick Acrylite GP, Spiny lobsters employ a variety of defen- ter consisted of a cement building block 40 (CYRO Industries, Rockaway, N.J. 07866) sive behaviors when in the presence of poten- cm wide × 16 cm high × 20 cm deep with 3 mounted at one end. We measured the ab- tial predators, under attack, or in agonistic in- openings 8.5 cm wide × 8.5 cm high × 20 cm sorption spectrum of the red acrylic filter ev- teractions with another lobster (Atema and deep. A solid cement block the same size was ery 1.2 nm from 400 to 750 nm using an Cobb, 1980). The most typical response is for placed behind each building block to close off Aminco UV-Vis Spectrophotometer DW2. the lobster to point or wave its spiny antennae the back end of the openings and to anchor a The filters absorb 99.9 % of the light at wave- toward an approaching animal. A lobster may tether support frame (Figure 2). lengths under 585 nm and transmit light with also retreat from another animal by slowly walking away, or withdrawing into its shelter, FIGURE 2 or rapidly fleeing backwards by vigorously flip- In situ image of crevice-type shelter, camera and lamp used in study. The four black lines indicate the ping its tail one or more times. These behav- range of movement of the tethered lobster. iors can range from very mild to very strong, depending on the species and level of aggres- sion of the other animal. Panulirus argus also employs communal defense behaviors, with groups of lobsters formed in rosettes and queues, using their antennae to fend off at- tacks from predators (Herrnkind et al., 2001; Briones-Fourzán et al., 2006). The objectives of this investigation were: (1) to evaluate the effect of red light on the behavior of spiny lobsters and associated ani- mals at night in the sea; (2) to use video and red light to identify the predators of lobsters and animals which cohabit shelters with lob- sters; and (3) to observe the behavioral inter- actions of these animals outside and inside the shelters.

88 λ a max of 675 nm. We measured the emission lized in both the continuous and intermittent We hypothesized that the behavior of spectra of the halogen bulb alone and the lamp light regimes and the effect of tethering was spiny lobsters and associated animals would with filter using an SLM Aminco Spectro- presumably the same for each treatment. be similar with the use of continuous red light fluorometer. Light from the lamps was pro- The effect of the red light was determined and in the dark (i.e., at the instant the inter- jected to a barium oxide surface and detected by comparing the behavior of the animals re- mittent red light was turned on). Compari- with a fiber optic sensor. The emission spec- corded during the night in intermittent red light sons between the two light regimes included trum of the filtered light is shown in Figure 1. at two of the crevice shelters versus the behavior the proportion of observations in which teth- The intensity of the filtered light as measured of other animals recorded in continuous red light ered lobsters were in the shelters for each ob- at the light by a light meter (LI-COR Quan- at the other two crevice shelters. The intermit- servation time, the proportion of free-living tum sensor, model 192 SA) was 1050 µmol tent light was turned on for 5 min every 2.5 lobsters in the shelters, and the proportion of quanta m-2 s-1. hours (18:00, 20:30, 23:00, 01:30, 04:00, tethered lobsters killed by octopuses at night. Power and signal cables extended 25 m 06:30) during the night by a digital timer These data were compared with two-sided from the cameras and lights to a weatherproof (RadioShack Cat. No. 61-1065) over a period Fisher exact tests (FET). We also used contin- shed at the end of a dock. The signal cables of 7 days (January 15–22, 2003). The 06:30 gency tables with χ² to compare the number were connected to a digital time-lapse VCR data were not included in our final results be- of fish in view in continuous red light and at recorder (SONY Video Cassette Recorder cause the ambient light from sunrise was too the instant the intermittent red light was SVT-L400) and multiplexer (Panasonic Digi- intense to regard these as night observations. turned on, as well as the maximum numbers tal Video Multiplexer WJ-FS216). Electrical Therefore, there were five observations per night of fish in view throughout the 5 min period power was provided by four RadioShack Regu- per shelter throughout the duration of the ex- after the intermittent light was turned on. lated Power Supplies, 120 v AC to 13.8 v periment. The intermittent or continuous light In addition, because each tethered lobster DC, 10 amp. Up to 2 cameras and lights regime was assigned using random numbers to was observed up to five times over one night, could be powered by each power supply unit. the shelters each night and the light cables con- we subjected the shelter occupancy data for One lobster was tethered to each crevice nected to the timer were changed accordingly. each light regime of tethered lobsters to a shelter by locking a plastic cable tie around its The behavior of the animals in the continuous Cochran’s Q test which permits multiple ob- cephalothorax, between the second and third red light was determined at the same instant the servations of the same subjects (Zar, 1999). walking legs, and attaching 0.55 mm diameter intermittent lights were turned on. We consid- Lobsters inside their shelter were scored as a monofilament line to the cable tie using a swivel ered the behavior of the animals in the intermit- “1” and outside their shelter as a “0”. The null clip. Our tethering method was similar to that tent red light at the instant the lights were turned hypothesis was that the proportion of lobsters used in other lobster studies (e.g., Eggleston et on to be a sample of their behavior in the dark. in shelters would be the same for all five obser- al., 1992). The monofilament line was tied to a Lobsters used for tethering were collected vation times. Then, we conducted a pairwise swivel clipped to a cable tie at the end of a 2.0 in the lagoon from a habitat similar to but dis- comparison of the proportion of lobsters in- cm outside diameter PVC pipe which was sus- tant from our field study site. They were placed side their shelters between light regimes using pended over the shelter and supported by a in a large holding tank, fed ad libitum, and the data from the Q tests (Zar, 1999: 270). PVC pipe frame anchored to the rear cement selected for placement at a specific shelter using block. The entire tether, including line, cable random number tables. These lobsters (N = Behavior of Lobsters and Other tie and swivels was 62 cm long. The end of the 28) had a mean (± SD) carapace length (CL) of Animals Inside and Outside Shelters pipe where the tether line was attached was 55 44.5 (± 6.18) mm (range = 30.4–62.0 mm) To study the behavior of lobsters and other cm above the seafloor and 30 cm in front of the and had a male:female sex ratio of 2:1. There animals inside the shelter, we used, in addi- shelter. The tether allowed the lobsters to enter were no significant differences in the mean CL tion to the crevice-type den, a larger, cave- and go to the back end of the refuge openings or sex ratio of the lobsters exposed to intermit- type den that simulated the larger shelters as well as to walk around on top of the shelter tent or continuous light as determined by a found in coral heads occurring in the lagoon and on the seafloor within a circular area having Student’s t-test for the CL and a χ² test for the and in the reef. The cave-type shelters (Figure a radius of 40 cm (see Figure 2). Tethering re- sex ratio. Tethered lobsters were replaced each 3) consisted of an inverted plastic container stricts the movements of animals and therefore day between 15:00 and 16:00. (Rubbermaid Cat. # 2979) and two similar the response (e.g., mortality) to experimental Free-living, untethered lobsters also occa- structures we fabricated using reinforced ce- treatments using tethered animals cannot be sionally entered the shelters. These lobsters ment. The inside dimensions of the shelter assumed to be equivalent to that of untethered were part of the existing naturally occurring base at the seafloor were 51 cm wide × 36 cm animals. However, tethering techniques are ap- population and appeared to be in about the deep. The shelter height was 71 cm. The base propriate to compare response variables of teth- same size range as the tethered lobsters. We of the plastic shelter was bolted to a frame ered animals among treatments with equal considered a tethered or free-living lobster to made of 3.7 cm outside diameter PVC pipe, sample sizes of tethered animals (Aronson et al., be in the shelter if any part of its head or tail leaving a single opening to the shelter, 3.7 cm 2001). In our study, tethered lobsters were uti- was within the shelter entrance. high × 46 cm wide. The cement shelters had

Fall 2006 Volume 40, Number 3 89 FIGURE 3 lobsters were killed by predators. We used the definitions of behaviors listed in Atema and In situ image of cave-type shelter, cameras and lamps used in study. Cobb (1980) to categorize the responses of a lobster to a nearby animal. The general behav- ior of animals is described.

Results

Effects of Red Light At the observation times 18:00, 20:30, 23:00, 01:30 and 04:00 h, tethered lobsters were in the crevice-type shelter in continuous red light 72.7 %, 77.8 %, 77.8 %, 55.6 % and 55.6 % of the observations, respectively. In the dark these percentages were 91.7 %, 80.0 %, 60.0 %, 63.6 %, and 72.7 % respectively (Table 1). The proportion of observations in which teth- ered lobsters were inside the crevice shelters did not differ significantly between the continuous red light and the dark for any of the above obser- two openings at the base, one on each of the Continuous video observations were re- vation times (FETs, P = 0.317, 1.000, 0.628, wider sides, consisting of 10 cm diameter holes corded for 23 days (May 15–June 7, 1998) 1.000, and 0.642 respectively). cut into the cement. A video camera and red inside and outside the plastic cave and for 11 Table 1 includes data from all observation lamp were mounted over holes at the top of days (February 4–14, 2002) inside the two times when the lobsters were visible. How- each shelter. The camera viewed the entire in- cement caves. We quantified the numbers and ever, some lobsters were not visible at one or side volume of the shelter. A second camera, species of animals that approached the caves more observation times due to turbidity or mounted to an anchored aluminum frame and the time period in which they cohabited absence caused by predation. All data for a was placed 1.5 m in front of the plastic shelter. with lobsters, as well as the events in which lobster were excluded from the Cochran’s Q An array of red diodes (RadioShack Cat. # 276-086) with a peak emission wavelength TABLE 1 of 660 nm illuminated the outside area of the Shelter occupancy of tethered lobsters in observations with continuous red light and in the dark (i.e., at shelter in the view of this camera. The cam- the moment the intermittent red light was turned on). eras, red lamps, camera mount, signal and power cables, and recording electronics were Time Location of tethered lobsters Continuous red light Dark Total the same as described above for the crevice- 18:00 In shelter 8 11 19 type shelters. Out of shelter 3 1 4 Two lobsters were tethered at the plastic Total lobsters 11 12 23 20:30 In shelter 7 8 15 cave shelter, one outside and one inside the Out of shelter 2 2 4 shelter. The length of the tether line allowed Total lobsters 9 10 19 each lobster to reach the shelter entrance but 23:00 In shelter 7 6 13 not pass through it. The tethering method Out of shelter 2 4 6 was as described above. The lobsters placed in Total lobsters 9 10 19 the cement cave shelters were not tethered. A 01:30 In shelter 5 7 12 Out of shelter 4 4 8 wire mesh funnel was placed in the entrance Total lobsters 9 11 20 holes, restricting but not preventing the lob- 04:00 In shelter 5 8 13 sters and other animals from leaving the shel- Out of shelter 4 3 7 ter. Lobsters at either shelter which escaped or Total lobsters 9 11 20 a were killed were replaced. The lobsters (N = Totals of In shelter 32 40 72 above Out of shelter 15 14 29 15) placed at the cave-type shelters had a mean times Total observations 47 54 101 (± SD) CL of 48 ± 11 mm (range = 36–72 aThese totals include up to five observations per lobster. All numbers for mm) and a male:female ratio of 0.88:1. each of the above observation times include only one observation per lobster.

90 TABLE 2 TABLE 3 TABLE 5

Number of free-living lobsters in shelters in ob- Number of fish in view in observations with con- Survival of tethered lobsters overnight in continu- servations with continuous red light and in the tinuous red light and in the dark (i.e., at the mo- ous and intermittent red light. All lobsters that dark (i.e., at the moment the intermittent red light ment the intermittent red light was turned on). died at night were killed by octopuses. was turned on). Number of Continuous Lobster Continuous Number of free- Continuous fish in view red light Dark Total condition red light Dark Total living lobsters red light Dark Total Zero 77 127 204 Survived 9 11 20 Zero 151 147 298 One 82 39 121 Killed 4 3 7 One to two 36 23 59 Two to four 28 4 32 Total observations 13 14 27 Total observations 187 170 357 Total observations 187 170 357 test analysis if the lobster was visible fewer TABLE 4 differ significantly between continuous red light than all five observation times. Seven lobsters and dark (FET, P = 0.678). In continuous red Maximum number of fish in view during the en- were thus excluded from each treatment. With tire 5 min observation periods when intermittent light, four of the tethered lobsters (30.8 %) the data from the remaining seven lobsters per red light was on and during the same periods in were killed by an octopus, whereas three lob- treatment, the proportion of lobsters inside continuous red light. sters (21.4 %) were killed in the dark (Table 5). the shelters did not vary significantly with observation time, either in the dark (Q = 0.857, Number of Continuous Intermittent Predators and Lobster df = 4, P = 0.931) or in continuous red light fish in view red light red light Total Defense Behavior Zero or one 49 53 102 (Q = 4.615, df = 4, P = 0.329). More impor- Two 99 91 190 Thirty-one occurrences of a spiny lobster tantly, the pairwise comparison revealed that Three to five 39 26 65 being killed by a predator were recorded on the proportion of lobsters inside the shelters Total observations 187 170 357 videotape during the day and night. The preda- did not differ significantly between light re- tors are listed in Table 6. The majority of the gimes (df = 4, S = 1.291 < Sα = 3.080, where intermittent light regime were not significantly kills took place during the day (71 %) and χ different from the maximum numbers in view Sα is the square root of ²0.05, 4; Zar, 1999). outside the shelters (74 %), usually involving The proportion of observations in which over the same period in the continuous light lobsters which were prevented by the tether free-living lobsters were residing in the shel- (χ² = 2.289, df = 2, P = 0.318, Table 4). from entering a shelter. Triggerfishes (Balistes ters did not differ significantly between light In the crevice-type shelters, most nocturnal vetula and Canthidermis sufflamen) were the most regimes (FET, P = 0.156). There were one or killings of lobsters were done by octopuses. The frequent diurnal predators, and octopuses were two free-living lobsters in the shelters in 19.2 octopus species is probably O. vulgaris (M. the most frequent nocturnal predators. % of our observations in continuous light and Vecchione, personal communication) although When first approached by a fish predator, in 13.5% in the dark (Table 2). there is considerably uncertainty in the identi- lobsters outside of a shelter sometimes remained In contrast, the number of fish in view fication of an octopus from black and white motionless, apparently to avoid detection. Once was significantly greater in continuous red video images. The tethered lobsters were gener- under attack, a lobster usually turned to face light than at the instant the intermittent light ally in the shelter when the octopus arrived but the fish while vigorously poking, rasping and was turned on (χ² = 44.828, df = 2, P < left the shelter soon after, and most killings oc- scissoring it with its antennae. The lobsters also 0.001). No fish were within the camera field curred outside the shelter. The proportion of attempted to escape by using tail flips, darting of view in 74.7 % of the observations in the tethered lobsters killed by octopuses did not backwards away from the attacker. dark compared with 41.2 % of the observa- TABLE 6 tions in continuous light (Table 3). However, the range in number (0–4) and the species of Predators recorded on videotape killing lobsters. Times and locations of attacks are summarized. fish in view were the same in both light re- gimes. The fish species occurring in the vicin- N In In Out of Predator species Common name total crevice cave shelter Day Night ity of the shelters at night were predominantly Balistes vetula Queen triggerfish 15 6a 09 15c 0 Haemulon sciurus (bluestriped grunts), H. Octopus vulgaris Octopus 8 1 0 7b 17 chrysargyreum (smallmouth grunts), and Canthidermis sufflamen Ocean triggerfish 4 0 0 4 4 0 Lutjanus analis (mutton snappers). These fish Lutjanus analis Mutton snapper 2 0 0 2 2 0 were observed to feed in the seagrass beds and Ocyurus chrysurus Yellowtail snapper 1 0 0 1 0 1 had little or no interactions with the shelters or Gymnothorax vicinus Purplemouth moray 1 0 1 0 0 1 the lobsters. Moreover, the maximum num- Total 31 7 1 23 22 9 aTriggerfish pulls lobster out of shelter to kill bers of fish in view throughout the 5 min bLobster in shelter when octopus arrives; leaves shelter before octopus attacks period after the light was turned on in the cIncludes one killing at dawn

Fall 2006 Volume 40, Number 3 91 Feeding Frenzy ters in pairs or groups of up to five fishes of and to flee by using tail flips and by jumping Whenever a lobster was killed by a fish mixed acanthurid species. Moray eels, includ- back and forth between the floor of the shel- (N = 22) a large aggregation of fishes composed ing Gymnothorax vicinus, G. moringa, and ter and the roof. of a variety of species was attracted to the site other species, occurred in the shelters during and participated in a feeding frenzy. Many of the day and night. They usually remained for these fish were observed competing with the only a few minutes but sometimes for up to Discussion predator and each other for the consumption about an hour. Serranids, such as Mycteroperca Our results indicate that video and red of the remains of the lobster. Some species, such bonaci (black grouper), and Epinephelus light can be used at night to study P. argus as mutton snapper, queen triggerfish, and yel- guttatus (red hind), had a similar pattern of without significantly affecting their behavior. lowtail snapper, were recorded killing lobsters shelter occupancy as the moray eels. M. bonaci The shelter occupancy rate of tethered lob- on other occasions (see Table 6). Others, how- frequently arrived at the crevice-type shelters sters was the same in continuous red light as in ever, frequently occurred in the vicinity of the during the day along with a mixed school of the dark and red light did not attract or repel shelters but did not indicate any aggressive be- other species passing by the shelter. A grouper free-living lobsters. These results are in agree- havior toward the living lobsters. Many fish would split off from the school, back tail-first ment with predictions from electrophysiologi- were large enough to potentially capture a lob- into the crevice opening, and remain in the cal studies (Cummins et al., 1984) which ster, but were only observed to eat a lobster after shelter facing outward. Several minutes later, show that the relative spectral sensitivity of P. λ it was killed by another species. These opportu- when the next school of fish passed by the argus vision reaches a max at about 510 nm nistic scavenger species included H. plumierii shelter, the grouper darted out of the crevice and drops to under 4% at 590 nm. The rela- (white grunt), H. sciurus (bluestriped grunt), and rejoined the school. Invertebrates, includ- tive spectral emission of our underwater lamps, λ Lactophrys triqueter (smooth trunkfish), ing hermit , portunid crabs, and arrow constructed with a red acrylic filter, had a max parrotfishes (Sparisoma spp.), Diodon hystrix crabs (Stenorhynchus seticornis), also occasion- at about 655 nm and was under 1% at λ < (porcupinefish), and Dasyatis sp. (stingray). ally lived in the shelters for short periods of 597 nm. Apparently, the amount of visible Other fishes such as Thalassoma bifasciatum time, usually less than an hour. A king helmet light emitted by our lamps was not disruptive (bluehead wrasse), and several angelfish snail (Cassis tuberosa), and a long-spined ur- to spiny lobsters, which at shallow depths are (Pomacanthus spp.) and parrotfish species were chin (Diadema antillarum), remained in the probably well-adapted to seeing some ambi- too small or anatomically unsuited to capture a crevice-type shelters for over a day. ent moonlight and starlight at night. lobster. These fishes may have been feeding The lobsters usually did not react to the The red light did attract a small, but sta- either on lobster scraps or on small benthic or- presence of the animals which cohabited the tistically significant number of fish. Fish were ganisms exposed when the bottom sediments shelters. Occasionally the lobsters displayed a within the video field of view at the shelters in were disturbed by the activity of the larger fish. mild defensive reaction, typically pointing their continuous light about twice as often as at the Little or none of the lobster remains could be antennae toward a fish if it got too close. This shelters in the dark. This result is consistent found at the site after the feeding frenzy. was usually done rather slowly and casually with studies which show that fish eyes con- Feeding frenzies did not generally occur with the lobster otherwise remaining at rest. tain pigments which are sensitive to red light after lobsters were killed by an octopus (N = The only strongly aggressive behavior we ob- (Levine and MacNichol, 1982) and that deep- 7). The octopus retained the captured lobster served, out of several hundred observations of water fish react to red light in the ocean and ate all of the soft tissue before releasing the animals cohabiting the shelters, was the single (Widder et al., 2005). However, the species nearly intact shell. The shell did not attract attack and kill of a lobster by a moray eel (G. and range in the number of fish near the shel- scavenging animals and usually remained at vicinus) in a cave-type shelter. The lobster at- ters were the same in the red light and in the the shelter for a day or more. tempted to fend off the eel with its antennae dark. Furthermore, the maximum number of

Animals Cohabiting with Lobsters in the Shelters TABLE 7 A variety of fish and invertebrates entered Fish families recorded on videotape entering the shelters. Times and durations of stays are summarized. both the crevice-type and cave-type shelters and remained inside along with the lobsters Duration in shelter (min) for periods of time ranging from a few seconds Family Common name N Mean ± SD Range Time to over a day (Table 7). Acanthurids, includ- Acanthuridae Surgeon and doctorfishes 136 2.14 ± 3.66 0.08–31.83 Day ing Acanthurus bahianus (ocean surgeonfish), Muraenidae Moray eels 93 2.31 ± 6.73 0.05–50.52 Night & day Serranidae Groupers and hinds 56 5.29 ± 10.90 0.18–64.98 Night & day A. chirurgus (doctorfish), and A. coeruleus (blue Pomacanthidae Angelfishes 6 0.40 ± 0.15 0.18–0.58 Day tangs), frequently entered the shelters during Chaetodontidae Butterflyfishes 5 2.10 ± 1.49 1.15–3.82 Day the day and remained for short periods, aver- Various* 59 22.55 ± 81.06 0.03–465.00 Night & day aging 2 min. Sometimes they entered the shel- *Small, unidentified fishes.

92 fish in view in the 5 min period after the inter- confirm and document which animals are ac- that observed by Cobb (1981) in juvenile P. mittent light was turned on was not signifi- tual predators. cygnus and Segura-García et al. (2004) in P. cantly different from the maximum number Predators are able to enter lobster shelters guttatus. We did not observe any communal over the same period in the continuous light. and predation can occur inside the shelters. defense behaviors and our investigation was Therefore, we hypothesize that the fish at- We recorded a moray eel killing a lobster in- not designed to do so. This would, however, tracted to the red light were already nearby side one of our cave-type shelters in the sea. be a valuable subject for a future study using the shelters and quickly moved into the red lit Lozano-Álvarez and Briones-Fourzán (2001) in situ video monitoring. zone after the intermittent light was turned observed triggerfishes attacking P. guttatus in- on. None of these fish were observed to attack side cave refuges in tanks although none of lobsters and there is no evidence that the be- the lobsters were killed. However, we have Acknowledgements havior or survival of the lobsters were affected also observed these same predator species and This work was funded in part by a J. W. by the small numbers of fish attracted to the lobsters cohabiting without aggression in the Fulbright Senior Scholar Grant and by the red light. same shelters for periods of up to many hours, Universidad Nacional Autónoma de México Our results suggest that red light does not as have other authors (e.g., Berry, 1971; (UNAM). We thank the following individuals have a significant effect on P. argus loss from Eggleston et al., 1990; Mintz et al., 1994; for their invaluable assistance. Cecilia Barradas- octopus predation at night. This result is in Briones-Fourzán et al. 2000). Factors which Ortiz of UNAM provided technical assistance agreement with electrophysiological studies might determine whether a visitor inside a throughout this study. Roberto Iglesias-Prieto (Hamasaki, 1968) which demonstrate that lobster shelter behaves like a friend or enemy and Xavier Hernández-Pech of UNAM mea- O. vulgaris vision has a spectral sensitivity with may include, among others, the visitor’s state sured the spectra of the lights and filters. Michael λ max at 480 nm and is relatively insensitive to of hunger, the lobster’s condition (e.g., molt- Vecchione of the National Museum of Natural red light. ing stage, health), the time of day or season of History identified the species of octopus in the A variety of fish and invertebrates are con- the year, the relative size of the animals, and videos. Chi Tien Lui of C.T.L Electronics, Inc. sidered to be predators or potential predators the size of the shelter. For example, Eggleston recommended the video cameras and record- of P. argus (e.g., Eggleston et al., 1990; Mintz and Lipcius (1992) and Mintz et al. (1994) ing equipment. We appreciate the thoughtful et al., 1994; Arce et al., 1997). Some of these found that tethered lobsters were more vul- comments of the reviewers and have incorpo- species are identified as predators because lob- nerable to predation in large than in small rated many of their suggestions in this paper. ster remains have been found in their stomach shelters, relative to the size of the lobsters. Annual permits to collect and use spiny lob- contents. Others are included because of their However, Lozano-Álvarez and Spanier (1997) sters were issued by Comisión Nacional de high abundance in the vicinity of lobsters. found that, when fish predators and free, Acuacultura y Pesca, México. Very few are based on direct observations of a untethered lobsters share a shelter with lim- predator attacking and consuming a lobster in ited space, the shelter may protect the lobsters the field (Lozano-Álvarez and Spanier, 1997; against predation because the fish need open References Barshaw et al., 2003; Oliver et al., 2005) or in space to attack the lobsters. Further study is Arce, A. M., Aguilar-Davila, W., Sosa-Cordero, the laboratory (Lozano-Álvarez and Briones- needed to understand the dynamics of the E. and Caddy, J. F. 1997. Artificial shelters Fourzán, 2001; Briones-Fourzán et al., 2006). relationship between lobsters and the animals (casitas) as habitats for juvenile spiny lobsters The animals identified as predators in our that share their shelters. Panulirus argus in the Mexican Caribbean. study were observed and recorded on video- Panulirus argus are highly gregarious ani- Mar Ecol Prog Ser. 158:217–224. tape preying on P. argus. We also identified mals, often living in groups in the same shelter animals which scavenge the remains of lob- and walking close together in packs or lines Aronson, R. B., Heck, K. L. Jr. and Valentine, sters after the lobsters have been killed by the outside the shelters (review in Herrnkind et J. F. 2001. Measuring predation with tethering predators. Some of these scavengers, such as al., 2001). It is likely that they utilize commu- experiments. Mar Ecol Prog Ser. 214:311–312. bluestriped grunts, white grunts, and smooth nal behaviors to defend against predation Atema, J. and Cobb, J. S. 1980. Social behavior. trunkfish are frequently observed near the lob- (Eggleston and Lipcius, 1992; Lozano-Álvarez In: The Biology and Management of Lobsters, ster shelters and are large enough to poten- and Briones-Fourzán, 2001; Briones-Fourzán Vol. I, (eds.) J. S. Cobb and B. F. Phillips. tially prey upon the lobsters. These animals et al., 2006). In our study, free-living lobsters pp. 409–450. New York: Academic Press. may not attack lobsters for behavioral or ana- occasionally entered the crevice-type and cave- tomical reasons even though they have the type shelters and interacted with the tethered Auster, P. J., Good, D. H., LaRosa, S. C. and same opportunities as the predators. However, lobsters. Most of these interactions were pa- Sprunk, H. J. 1990. Observing animal behavior based on circumstantial evidence from stom- cific but some were antagonistic, in which one with ROV’s: minimizing impacts with red light. ach contents and abundance at shelters, they lobster aggressively pushed the other out of Proc. ROV ‘90 Conference. pp. 185–190. could be mistakenly inferred to be predators. the shelter or attempted to prevent another Washington: Marine Technology Society. Our study demonstrates the value of video to lobster from entering, in a manner similar to

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