Biol. Bull. 215: 182-190. (October 2008)
© 2008 Marine Biological Laboratory
Influence of Conspecific and Heterospecific Aggregation Cues and Alarm Odors on Shelter Choice by Syntopic Spiny Lobsters
Patricia Briones-Fourzán*,
Eunice Ramírez-Zaldívar and
Enrique Lozano-Álvarez
Unidad Académica Puerto Morelos, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México, PO Box 1152, Cancún, Q.R., 77500 Mexico
* To whom correspondence should be addressed. E-mail: briones{at}mar.icmyl.unam.mx
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Abstract
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In spiny lobsters, conspecific scents ("aggregation cues") may mediate gregarious diurnal sheltering, but scents from injured conspecifics ("alarm odors") may elicit avoidance behavior. In laboratory experiments, individuals of two coexisting species, Panulirus guttatus (a reef-obligate) and P. argus (a temporary reef-dweller), significantly chose shelters emanating conspecific aggregation cues and responded randomly to shelters emanating heterospecific aggregation cues. However, despite evidence that the two species perceived each other's alarm odors to a similar extent, P. guttatus responded randomly to shelters emanating either conspecific or heterospecific alarm odors, whereas P. argus significantly avoided both. This differential influence of alarm odors likely reflects interspecific differences in life history, sociality, and behavior. The less social, reef-obligate P. guttatus lobsters forage close to their reef dens, into which they retract deeply upon perception of risk. This cryptic behavior may offset the need to avoid conspecific (and heterospecific) alarm odors. In contrast, avoidance of conspecific alarm odors by P. argus is consistent with its ontogenetic habitat shifts and greater sociality. Furthermore, because reef-dwelling P. argus lobsters forage across open areas away from the reef, an ability to avoid alarm odors from P. guttatus upon returning to their reef dens may increase their fitness.
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Introduction
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Chemical interactions are one of the most primitive forms of communication among organisms. Chemical communication is carried out through a wide array of substances collectively called "infochemicals" (Dicke and Grostal, 2001). For example, in marine animals, infochemicals released by live conspecifics may mediate postlarval settlement (Burke, 1986; Jensen, 1989), aggregation and school formation (Hamner et al., 1983; Ratchford and Eggleston, 1998; Dicke and Grostal, 2001), reproduction (Dunham, 1978; Atema, 1995; Raethke et al., 2004), synchronization of egg hatching (Forward et al., 1987; Ziegler and Forward, 2007), and agonistic interactions (Karavanich and Atema, 1998; Zulandt Schneider et al., 2001). In contrast, infochemicals released by injured animals, for example during a predation event ("damage-released odors"), may be used by other organisms to assess and avoid predation risk (Chivers and Smith, 1998; Wisenden, 2000; Zimmer and Butman, 2000). Alarm infochemicals are of special significance because predation risk usually has important and immediate consequences on fitness, particularly for potential prey exposed to many generalist predators that they may have difficulty in perceiving accurately (Hazlett, 1994; Chivers and Smith, 1998; Dicke and Grostal, 2001).
Spiny lobsters (family Palinuridae) are large decapod crustaceans that sustain important fisheries throughout the tropical and subtropical seas of the world, where they inhabit shallow coral and rocky habitats. Spiny lobsters forage at night but remain in shelters during the day, presumably to reduce the risk of predation. Because spiny lobsters do not construct their own dens, they depend on available structured refuge such as crevices and caves, where they often aggregate. This gregarious diurnal sheltering is mediated by individuals homing in on chemical cues released from sheltered conspecifics, as shown for Panulirus interruptus (Zimmer-Faust et al., 1985), Panulirus argus (Ratchford and Eggleston, 1998; Nevitt et al., 2000), Jasus edwardsii (Butler et al., 1999), and Panulirus guttatus (Briones-Fourzán and Lozano-Álvarez, 2005). These chemical cues (referred to as aggregation cues) are apparently released with the urine (Horner et al., 2006). On the other hand, infochemicals released by damaged conspecifics (referred to as alarm odors) have been shown to elicit avoidance in Panulirus cygnus (Hancock, 1974), P. interruptus (Zimmer-Faust et al., 1985), and P. argus (Briones-Fourzán et al., 2006).
Many species of spiny lobster are sympatric and some are also syntopic, co-occurring locally in a particular habitat (e.g., Berry, 1971; George, 1974; Sekiguchi and George, 2005). For example, Panulirus guttatus (Latreille, 1804), the spotted spiny lobster, and Panulirus argus (Latreille, 1804), the Caribbean spiny lobster, coexist across the greater Caribbean region and share a local existence on coral reef habitats (Sharp et al., 1997; Acosta and Robertson, 2003; Lozano-Álvarez et al., 2007). However, P. guttatus is restricted to the coral reef habitat after settlement (Sharp et al., 1997), whereas P. argus undergoes ontogenetic habitat shifts. Early benthic P. argus juveniles remain widely dispersed in the settlement habitat (shallow seagrass-macroalgal habitats), but upon reaching 15–20 mm in carapace length (CL) they shift from algal-dwelling to crevice-dwelling over shallow reef lagoon and bay areas, and become gregarious (Childress and Herrnkind, 1996). Subadults (40–45 to 75–80 mm CL) move to coral reef habitats where, together with adults (
75–80 to >200 mm CL), they coexist with the reef-obligate P. guttatus. Relative to P. argus, P. guttatus is more abundant on the reef habitat, especially on fore-reef zones (Acosta and Robertson, 2003; Lozano-Álvarez et al., 2007), but its individuals are much smaller in size, reaching adulthood at about 38 mm CL and having a maximum size of 88 mm CL.
Local coexistence of closely related species is generally mediated by a differential use of resources at a particular scale or by ecological trade-offs (Kneitel and Chase, 2004; Lozano-Álvarez et al., 2007). Differential responses to infochemicals may also mediate local coexistence of related species, as shown for echinoderms (Campbell et al., 2001), hermit crabs (Hazlett, 1990; Rittschof et al., 1992), brachyuran crabs (Hazlett et al., 2000), freshwater crayfish (Hazlett, 1994, 1999; Acquistapace et al., 2004), and fishes (Chivers and Smith, 1998; Brown et al., 2001; Golub and Brown, 2003). However, responses of spiny lobsters to infochemicals from closely related, syntopic species have not been evaluated.
We conducted laboratory experiments to examine the influence of conspecific and heterospecific aggregation cues and alarm odors on the shelter choice of syntopic individuals of P. guttatus and P. argus. For each species, we hypothesized that individuals (1) would be significantly attracted to shelters emanating conspecific aggregation cues, (2) would significantly avoid shelters emanating conspecific alarm odors, and (3) would show a random response to shelters emanating heterospecific infochemicals, whether aggregation cues or alarm odors. Similar species often recognize each other's alarm odors as indicative of danger (e.g., Brown et al., 1970; Wisenden, 2000; Golub and Brown, 2003), but we did not expect this to happen between P. argus and P. guttatus because P. argus is only a temporary reef-dweller. However, we conducted further experiments to compare short-term behavioral responses of individuals of each species subjected to conspecific and heterospecific alarm odors.
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Materials and Methods
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Experiments were conducted in the Unidad Académica Puerto Morelos, Universidad Nacional Autónoma de México, located at Puerto Morelos, Mexico (20°54'N, 86°54'W). Using scuba apparatus, we collected lobsters by hand on the Puerto Morelos coral reef and immediately transferred the lobsters to the laboratory. Lobsters were segregated by species and held for 1–2 weeks in large outdoor tanks kept under shade and provided with multiple shelters for lobsters. A continuous seawater flow maintained ambient temperature in the tanks. During the holding period, lobsters were fed every other day with a mixture of clams, mussels, and crabs, but were not fed during the experiments. The size range of experimental lobsters was within the size range of lobsters observed on the reef habitat and was similar for both species. We only used lobsters in intermolt-early premolt (stages C–D1 in Drach's scale; see Lyle and MacDonald, 1983) to avoid confounding effects due to changes in behavior over the molt cycle. Molt stage was determined through microscopic observation of the tip of one pleopod (Lyle and MacDonald, 1983). At the end of each experiment, we marked the lobsters with T-bar tags and returned them to the coral reef habitat. Tags were applied to avoid using these lobsters if they were collected again.
Experimental series 1: Influence of conspecific and heterospecific aggregation cues and alarm odors on shelter choice by each species
To test the influence of conspecific and heterospecific aggregation cues and alarm odors on the shelter choice by individuals of Panulirus guttatus and P. argus, we used four experimental units, each consisting of a fiberglass Y-maze with two independent head tanks (Ratchford and Eggleston, 1998, 2000; Briones-Fourzán and Lozano-Álvarez, 2005). The four units were in the open but enclosed in a tent. Each head tank (0.6 m long x 0.5 m wide x 0.5 m tall) held 90 l of water when filled to a standpipe height of 0.3 m. The Y-maze (2.0 m long x 0.8 m wide x 0.6 m tall) contained 500 l when filled to a standpipe height of 0.3 m. A panel measuring 1.0 m long x 0.6 m tall divided half the length of the Y-maze into two equal arms (Fig. 1). Seawater from a continuous, open system flowed into the head tanks and then from each head tank to an arm of the Y-maze. The water then mixed in an open area before flowing out through the standpipe located behind the start area of the Y-maze.
Two identical shelters were prepared, and one was placed in each arm at a distance of 1.8 m from the start area of the Y-maze (Fig. 1). One of the shelters received water that had flowed through a head tank containing the "stimulus" (either a live lobster or one-half of a freshly killed lobster), whereas the other received plain seawater that had flowed through a head tank that held no stimulus. Water flow into the head tanks was fixed at 1.5–2.0 l min-1. To prevent the possibility of lobsters using the corners in the start area of the Y-maze as refuges (Ratchford and Eggleston, 1998), a semicircular wire-mesh screen was positioned at the start area (Fig. 1). The head tanks and Y-mazes were completely opaque to preclude visual contact between lobsters and were mounted on different surfaces to eliminate the transference of vibrations. Also, to prevent transference of acoustic cues potentially produced by the stimuli, the water from the head tanks fell from a height of 5 cm above the water surface of the Y-maze.
Trials were conducted overnight. Lobsters were randomly assigned to specific treatments and to the left or right head tanks. The lobsters that were subjected to the stimulus were designated "test" lobsters. The stimulus was placed in the head tank 30 min before dark, and the test lobster was then placed in the start area of the Y-maze, where it was allowed to acclimatize for 2 h within a mesh cylinder (0.45 m in diameter, 0.40 m in height). The cylinder was then removed, leaving the test lobster free to roam the Y-maze. Previous research has shown that test lobsters tend to explore both arms of the Y-maze (Briones-Fourzán and Lozano-Álvarez, 2005). Between 0900 and 1000 the following morning, we recorded the position of the test lobster in the Y-maze and checked the flow rate into the head tanks. The test lobster was then removed and measured with calipers (carapace length, CL, from between the rostral horns to the posterior margin of the carapace, ± 0.1 mm). Lobsters were measured and molt-staged at the end of each trial to minimize handling stress. To ensure that no scents remained after each trial, the head tanks and Y-mazes were drained and thoroughly brushed, then water was allowed to flow at a high rate until the beginning of the next trial. No lobster was used more than once as a stimulus, and no lobster was used more than once as a test lobster.
The series consisted of eight experiments (Table 1). In experiments 1 and 2, the stimulus was a live conspecific; and in experiments 3 and 4, a live heterospecific. In experiments 5 and 6, the stimulus was one-half of a freshly killed conspecific bisected lengthwise to ensure the release of alarm odors; and in experiments 7 and 8, one-half of a freshly killed heterospecific. We used only one-half of a lobster per trial in experiments 5–8 to minimize the sacrifice of animals. The size range of the test lobsters was 38.8–75.9 mm CL for P. guttatus and 38.5–77.3 mm CL for P. argus. Responses to shelters emanating conspecific aggregation cues and alarm odors have already been tested in P. argus and P. guttatus (Ratchford and Eggleston, 1998; Nevitt et al., 2000; Briones-Fourzán and Lozano-Álvarez, 2005; Briones-Fourzán et al., 2006; Horner et al., 2006), but we included these treatments to provide a baseline with which to contrast the response of each species to shelters emanating heterospecific infochemicals.
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Table 1 Summary of features of eight experiments to test the influence of conspecific and heterospecific aggregation cues and alarm odors on individuals of Panulirus guttatus and Panulirus argus
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We ran at least 20 replicate trials in each experiment but discarded those in which the water flow at the end of the trial differed between the head tanks by more than ±0.25 l min-1. Also discarded were three trials in which the test lobster was found outside either shelter. Table 1 presents data on the valid replicate trials for each experiment. Results from experiments 1–4 were each subjected to a one-tailed binomial test (Zar, 1999) because we expected individuals of each species to be attracted to conspecific aggregation cues and to avoid conspecific alarm odors. Results from experiments 5–8 were each subjected to a two-tailed binomial test because we had no a priori reason to expect either attraction to or avoidance of heterospecific infochemicals.
Experimental series 2: Short-term behavioral changes in response to conspecific and heterospecific alarm odors
To compare short-term behavioral changes in individuals of P. guttatus and P. argus exposed to conspecific and heterospecific alarm odors, we used four experimental units, each one consisting of a glass aquarium (1 m long x 0.4 m wide x 0.3 m tall) that held 60 l of seawater when filled to a standpipe height of 0.15 m. The aquaria were inside a room with shaded windows. To provide visual isolation, the exterior of each aquarium was covered with an opaque sheet from the bottom to a height of 0.15 m, and the entire aquarium was covered with a black mesh. The bottom of each aquarium was lined with wire mesh to provide traction for the lobsters. A shelter constructed with dark PVC pipe, 5 cm in diameter and 15 cm in length, was fixed to the bottom at the short side of the aquarium next to the standpipe ("back side"). The shelter was short relative to the size of the lobsters to allow continuous observations of the lobsters. Filtered seawater fell into the aquarium through a pipe above the side of the aquarium opposite to the back side (i.e., "front side") and from a height of 5 cm above the water surface.
The size range of test lobsters, which were used only once, was 35.2–76.0 mm CL for P. guttatus and 39.3–72.3 mm CL for P. argus. We used males exclusively, because these experiments were conducted during the spring when many females of P. guttatus are ovigerous, and ovigerous females tend to be less active than non-ovigerous females or males (Atema and Cobb, 1980). Each test lobster was first subjected to a control solution (filtered seawater), then to a solution of alarm odors (stimulus). The stimulus was prepared with a freshly killed lobster blended in filtered seawater in a proportion of 1 g of wet weight per 8 ml of seawater (Bouwma and Hazlett, 2001). This solution was then passed through coarse filter paper to eliminate solid particles. To avoid changes in the nature of the odor upon freezing or refrigeration (Hazlett, 1994), we prepared fresh stimulus every day, sufficient to run four trials.
One test lobster was introduced into each aquarium at 1100 h and allowed to acclimatize for 24 h. When the trials began, the test lobsters were usually inactive inside or near the shelter. We started a trial by turning off the water flow and injecting 100 ml of control solution through two glass pipes fixed to the front side of the aquarium, allowing it to diffuse for 20 min. This period was determined in a previous test using stimulus with inert dye. We then began an observation period of 5 min (control period). At the end of the control period, water flow was turned on and water was allowed to flow at a high rate for 10 min. We then turned off the flow and injected 100 ml of stimulus, allowing 20 min for diffusion prior to a second observation period of 5 min (treatment period).
During all trials, the behavior of lobsters was videotaped with two cameras, one (Digital Handycam SONY, DCR-TRV17) located at the front side of the aquarium and the other (CCD SYSCOM) at the back side. The tapes were later viewed in a time-lapse videorecorder (SONY SLV-L4). For each control and treatment period, we quantified the amount of time (in seconds, s) that the test lobsters performed each of four behaviors associated with chemical perception and alarm: (1) antennule cleaning (grasping an antennule between the third maxillipeds and pulling it upward), which denotes perception of chemical stimuli (Atema and Cobb, 1980; Segura-García et al., 2004); (2) sheltering behavior, a response shown by several decapod species in a risky situation (Dicke and Grostal, 2001; Tomba et al., 2001); (3) nonambulatory movements (changes in body position or in general activity while the lobster remained on the same site), denoting an increase in awareness (Hazlett, 1994, 1999, 2000); and (4) locomotion/tailflipping, denoting exploratory behavior and escape (Atema and Cobb, 1980).
The series consisted of four experiments. Experiments 1 and 2 tested the behavioral responses of each species to conspecific alarm odors and were conducted during March–May 2005. Experiments 3 and 4 tested the behavioral responses of each species to heterospecific alarm odors and were conducted during March–June 2006. In each experiment, we compared each of the four behavioral responses within species between the control and treatment periods with separate Wilcoxon matched-pairs tests with normal approximation (Zar, 1999). We then compared the behavioral responses between species during the control and treatment periods with separate Mann-Whitney tests with normal approximation (Zar, 1999).
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Results
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Influence of conspecific and heterospecific aggregation cues on shelter choice by lobsters
Individuals of Panulirus guttatus significantly chose shelters emanating conspecific aggregation cues (79.2% attraction, P = 0.003), but their response to shelters with heterospecific aggregation cues did not differ from random (48.0% attraction, P = 0.999; Fig. 2A). Similarly, individuals of P. argus significantly chose shelters with conspecific aggregation cues (80.0% attraction, P = 0.006) and responded randomly to shelters emanating heterospecific aggregation cues (47.1% attraction, P = 0.999; Fig. 2B).
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Figure 2. Results of Y-maze experiments investigating the effects of conspecific and heterospecific aggregation cues on shelter choice by individuals of (A) Panulirus guttatus and (B) P. argus. P values were based on one-tailed binomial tests for conspecific aggregation cues, and on two-tailed binomial tests for heterospecific aggregation cues.
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Influence of conspecific and heterospecific alarm odors on shelter choice by lobsters
Individuals of P. guttatus showed a random response to shelters with conspecific alarm odors (50.0% avoidance, P = 0.605) and also to shelters with heterospecific alarm odors (56.2% avoidance, P = 0.402; Fig. 3A). By contrast, individuals of P. argus significantly avoided shelters with conspecific alarm odors (71.4% avoidance, P = 0.039) and significantly avoided shelters with heterospecific alarm odors (73.9% avoidance, P = 0.035; Fig. 3B).
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Figure 3. Results of Y-maze experiments investigating the effects of conspecific and heterospecific alarm odors on shelter choice by individuals of (A) Panulirus guttatus and (B) P. argus. P values were based on one-tailed binomial tests for conspecific alarm odors, and on two-tailed binomial tests for heterospecific alarm odors.
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Short-term behavioral changes to conspecific alarm odors
When subjected to conspecific alarm odors, individuals of each species significantly increased the time spent performing antennule cleaning and nonambulatory movements, but showed no significant change in the time performing sheltering behavior or locomotion (Table 2). The amount of time performing each of the four behaviors did not differ significantly between species, either during the control periods (Mann-Whitney tests, range of P values = 0.225–0.794) or during the treatment periods (range of P values = 0.131–0.964).
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Table 2 Results of separate Wilcoxon match-paired tests with normal approximation (z) comparing the amount of time in seconds [median (interquartile range)] that individuals of Panulirus guttatus (n = 22) and individuals of Panulirus argus (n = 23) performed each of four behaviors between a 5-min (= 300 s) period subjected to conspecific alarm odors and a 5-min period subjected to seawater (control substance)
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Short-term behavioral changes to heterospecific alarm odors
When subjected to heterospecific alarm odors, individuals of each species significantly increased the time spent in antennule cleaning, nonambulatory movements, and locomotion, but showed no significant change in the time performing sheltering behavior (Table 3). The amount of time performing each of the four behaviors did not differ significantly between species, either during the control periods (Mann-Whitney tests, range of P-values = 0.233–0.932) or during the treatment periods (range of P values = 0.287–0.483).
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Table 3 Results of separate Wilcoxon match-paired tests with normal approximation (z) comparing the amount of time in seconds [median (interquartile range)] that individuals of Panulirus guttatus (n = 23) and individuals of Panulirus argus (n = 24) performed each of four behaviors between a 5-min (= 300 s) period subjected to heterospecific alarm odors and a 5-min period subjected to seawater (control substance)
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Discussion
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Shelters emanating aggregation cues elicited similar responses in Panulirus guttatus and P. argus. As expected, both species were significantly attracted to shelters with conspecific aggregation cues and responded randomly to shelters with heterospecific aggregation cues. The attraction of P. argus to conspecific aggregation cues had been previously observed in the laboratory (Ratchford and Eggleston, 1998, 2000; Horner et al., 2006) and in the field (Nevitt et al., 2000). Ratchford and Eggleston (1998) also found that conspecific attraction was independent of season and that P. argus lobsters were able to produce and respond to conspecific aggregation cues at sizes as small as 15 mm CL, which is roughly the size at which juvenile P. argus shift from solitary algal-dwelling to gregarious crevice-dwelling (Childress and Herrnkind, 1996). The minimum size at which P. guttatus is able to produce and to respond to conspecific aggregation cues has not been determined, but Briones-Fourzán and Lozano-Álvarez (2005) found that subadults and adults (35–79 mm CL) show this ability. They also found that, although conspecific attraction in P. guttatus varied seasonally, it was highest when reproductive activity was at its peak (i.e., spring) irrespective of the gender of the cue producers and receivers. On the basis of this finding, we conducted our experiments to test for the influence of conspecific infochemicals on shelter choice by P. guttatus during the spring (March–April; see Table 1).
Individuals of P. guttatus and P. argus rarely share dens on the reef habitat (Sharp et al., 1997; Lozano-Álvarez et al., 2007), but this is due to their differential use of shelter resources across the reef habitat and to the stronger attraction between conspecifics, not to interspecific competition (Lozano-Álvarez et al., 2007). In artificial dens shared by both species, individuals of P. argus tended to use the floor while those of P. guttatus tended to cling to the walls and ceiling, which could suggest a chemically mediated interference (Lozano-Álvarez and Briones-Fourzán, 2001). Each species, however, also shows this differential use of the den space on the reef habitat regardless of whether the dens harbor individuals of either or both species (Sharp et al., 1997; Lozano-Álvarez et al., 2007). This finding, in conjunction with the random response to shelters emanating heterospecific aggregation cues shown by both species in our Y-maze experiments, does not support the notion of an interspecific chemical interference.
In experimental series 2, P. guttatus and P. argus displayed similar short-term behavioral changes when subjected to conspecific and heterospecific alarm odors, but these results do not provide conclusive evidence that these species associate each other's alarm odors with predation risk. We do not know, for example, how these behaviors change in the presence of benign chemical cues such as food odors, of conflicting chemical cues such as a combination of food and alarm odors (Hazlett, 1999; Tomba et al., 2001; Acquistapace et al., 2004), or with activity level of lobsters (Zimmer-Faust et al., 1996). Therefore, the only evidence provided by experimental series 2 is that both species perceive conspecific and heterospecific alarm odors to a similar extent. Despite this similarity in short-term perception, however, each species showed different overnight responses to shelters emanating conspecific and heterospecific alarm odors in the Y-maze experiments. These contrasting results likely reflect interspecific differences in life history, foraging behavior, sociality, and vulnerability to predators.
In shallow lagoon and bay habitats, P. argus juveniles emerge from their dens to forage solitarily for short distances over open seagrass habitats where predation risk is high, but they use conspecific scents to find suitable shelter faster, thus reducing their exposure time (the "guide effect," Childress and Herrnkind, 2001). In addition, den-sharing confers antipredator benefits to individuals of P. argus, either through a dilution effect or through group defense, whereby individuals act in concert to fend off enemies from the den entrance (Dolan and Butler, 2006; Briones-Fourzán and Lozano-Álvarez, 2008). The guide effect and group defense of the den are expressions of the high level of sociality of P. argus, further evidenced by the massive single-file migrations undertaken by subadult-adult lobsters over shelterless areas, during which they show coordinated defensive displays (Herrnkind et al., 2001). However, avoiding conspecific alarm odors is a particularly effective antipredator strategy for gregarious species (Dicke and Grostal, 2001), and it is well known that P. argus is highly chemosensitive and can discriminate among complex mixtures of odors (e.g., Derby, 2000). Thus, as expected, our test individuals of P. argus significantly avoided shelters emanating odors from freshly killed conspecifics.
At the onset of the subadult phase, individuals of P. argus shift to a novel habitat, the coral reef, where they take shelter. Reef-dwelling P. argus lobsters, however, do not forage on the reef, but disperse to forage over shelterless areas for tens to hundreds of meters away from their reef dens, to which they return before dawn (Herrnkind et al., 1975; Cox et al., 1997). Because these lobsters share predators with P. guttatus (Lozano-Álvarez et al., 2007), there may be a strong selection pressure for reef-dwelling P. argus lobsters to quickly learn to avoid alarm odors from P. guttatus (Chivers and Smith, 1998; Wisenden, 2000). Fishes that undergo size-specific ontogenetic niche shifts also show ontogenetic changes in responses to heterospecific alarm cues, and some fishes have been trained in the laboratory to associate heterospecific alarm cues with predation risk (Mathis et al., 1996; Brown et al., 2001; Golub and Brown, 2003).
On the other hand, there is also evidence for the conservation of alarm signals within taxonomic groups, especially in closely related, sympatric species, suggesting that the chemicals that serve as alarm cues are similar in these species (Brown et al., 1970; Burke, 1986; Mizra and Chivers, 2001; Golub and Brown, 2003). Thus, whether the avoidance response of P. argus to alarm odors from P. guttatus is learned or conserved remains undetermined. The conservation hypothesis could, however, partially explain the similar short-term behavioral responses to conspecific and heterospecific alarm odors shown by P. guttatus and P. argus, which appear to have coexisted regionally since the middle Miocene (18–8 Ma) (George, 2006). But why, then, would P. guttatus not significantly avoid either conspecific or heterospecific alarm odors?
Compared to P. argus, individuals of P. guttatus are more sedentary and have a higher level of shelter fidelity and a greater vulnerability to predators (Lozano-Álvarez et al., 2007). Thus, individuals of P. guttatus tend to forage within protective recesses on the reef (Wynne and Côté, 2007) and only for brief periods at night (Segura-García et al., 2004). Moreover, in P. guttatus, conspecific attraction varies seasonally, den sharing is less prevalent, and also—importantly—this species does not display group defense (Briones-Fourzán and Lozano-Álvarez, 2005, 2008; Briones-Fourzán et al., 2006). The most usual antipredator strategy of exposed individuals of P. guttatus is to retreat deeply into the nearest available reef crevice and remain still, regardless of the number of conspecifics using that den (Lozano-Álvarez and Briones-Fourzán, 2001). This cryptic defensive behavior would appear to be sufficiently adaptive to offset the need to avoid shelters with conspecific (and heterospecific) alarm odors and is consistent with the habitat specialization of P. guttatus, which possibly dates from the late Miocene/early Pliocene (8–2 Ma) (George, 2006).
Ours is the first study comparing the influence of conspecific and heterospecific infochemicals on the behavior of syntopic species of spiny lobster, but this issue has been more widely studied in freshwater crayfish. Interestingly, potentially invasive crayfish species like Orconectes rusticus and Procambarus clarkii show a stronger avoidance to heterospecific alarm odors than their noninvasive coexisting congeners do (O. propinquus and P. acutus acutus, respectively), suggesting that invasive species use a broader range of chemical information than noninvasive species do (Hazlett, 2000; Acquistapace et al., 2004). Invasive species also tend to have a lower vulnerability to predators than found in closely related noninvasive species (Kneitel and Chase, 2004), a trade-off similar to that shown between P. argus and P. guttatus (Lozano-Álvarez et al., 2007).
Two other spiny lobsters, P. cygnus and P. interruptus, have also been shown to avoid conspecific alarm odors (Hancock, 1974; Zimmer-Faust et al., 1985). These species, like P. argus, undergo ontogenetic habitat shifts and are highly gregarious, suggesting that avoidance of conspecific alarm odors is a common antipredator strategy for lobsters sharing these features. Responses to conspecific alarm odors have not, however, been examined in other less gregarious, habitat-specialist spiny lobsters such as P. guttatus. Because species of spiny lobster that differ in their habitat specialization coexist locally elsewhere, it would be interesting to investigate whether these species also exhibit differential responses to each other's infochemicals. If so, these differential responses may be an additional factor mediating their local coexistence.
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Acknowledgments
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We thank F. Negrete-Soto and C. Barradas-Ortiz for their invaluable technical support in field and laboratory activities. Additional help was provided by A. Osorio-Arciniegas, R. Domínguez-Gallegos, M. Pérez-Ortiz, J. Valladárez-Cob, K. Baeza-Martínez, and D. Placencia-Sánchez. This study was funded by Universidad Nacional Autónoma de México and Consejo Nacional de Ciencia y Tecnología, México (Project 40159-Q). Annual permits to capture experimental lobsters were issued by Comisión Nacional de Acuacultura y Pesca, México.
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Footnotes
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Received 15 November 2007; accepted 27 March 2008.
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Literature Cited
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Abstract
Introduction
