PATTERNS OF ACTIVITY AND SPACE UTILIZATION ...

BULLETIN OF MARINE SCIENCE, 43(1): 61-76,1988

PATTERNS OF ACTIVITY AND SPACE UTILIZATION OF LEMON SHARKS, NEGAPRION BREVIROSTRIS, IN A SHALLOW BAHAMIAN LAGOON Samuel H. Gruber, Donald R. Nelson and John F. Morrissey ABSTRACT In an initial telemetry study we examined patterns of activity and space-utilization by the lemon shark, Negaprion brevirostris. using manual ultrasonic tracking. Nine sharks were tracked intermittently for periods of 1-8 days: The longest continuous tracking segment lasted 101 h. Total activity space per individual ranged from 9-93 km2, as determined by the maximum-area polygon method. All sharks tracked at Bimini showed some degree of site attachment. The two largest sharks tracked elsewhere, did not remain in the area of tagging but made deepwater excursions. At Bimini, sharks tracked during the day were located eastward of their nighttime activity spaces. They moved westward over the flats at sunset and back eastward at sunrise. These sharks appeared to use the sun as an orientation cue. The tracks of two sharks fitted with speed-sensing transmitters demonstrated that swimming speeds were two times faster than the corresponding point-to-point rates of movement. The highest rates of movement were recorded at evening and morning twilight periods: the average nighttime rate was higher than the daytime rate-although statistical significance could not be established. Underwater and aerial observations showed lemon sharks to be associated with each other, with other sharks and with te!eosts. Findings are interpreted in light of current information on space utilization, die! activity, social grouping, and energetics.

In ecological studies of aquatic predators, understanding the flow of energy from the environment to the species under consideration is of importance in assessing its impact on the community and its overall production (Grodzinski, 1975). Defining and balancing an energy budget may be the best way to understand the sources and partitioning of energy available to a species. In an energy budget, activity represents an important energy sink and is often determined in the laboratory by respirometry (Brett and Groves, 1979). This measurement of perfor-

mance can then be extrapolated to the field. However, if results are to be valid, the extrapolation must be based on knowledge of natural patterns of activity as determined, for example, by field studies (Davis and Warren, 1971). Few such quantitative behavioral observations have been made for fishes except under special circumstances such as in confined bodies of clear, calm water where continuous observations can be made on relatively sedentary species (Diana et aI., 1977; Priede and Young, 1977). We have been investigating the bioenergetics of sharks, a group of fishes which is difficult to observe directly in the field. To provide linking data between performance in the laboratory and activity in the natural environment, we conducted acoustic tracking oflemon sharks, Negaprion brevirostris, on a round-the-clock basis, in a natural, shallow-water habitat typical for the species. Sharks have been tracked before, but never in the context of evaluating their energetic requirements. Recently, however, using telemetered thermal data from a 4.6-m white shark, Carcharodon carcharias, tracked for 3.5 days, Carey et aI., (1982) estimated a relatively low metabolic rate. They suggested that a single, large meal might sustain the shark for a month or more. In their study oxygen consumption was not directly measured. In fact, few respirometry studies have been published in which the activity of even teleost fishes was correlated with 61

62

BULLETIN OFMARINESCIENCE, VOL.43, NO.1, 1988

their energy requirements. One exception is the telemetry study of Diana (1980) who showed that the pike, Esox lucius, is ordinarily a sedentary fish whose metabolic rate in the field can be predicted by its standard metabolic rate in the laboratory. The lemon shark makes a good experimental subject for quantitative studies because of its size, abundance, generalized structure, and good survival in captivity. In addition, unlike many other species, the lemon shark survives the rigors of hook and line capture-probably because it can ventilate its gills while resting on the bottom and thus "pay back" any oxygen debt incurred in struggling on the line. These facts have not gone unnoticed by others, and so the lemon shark has become one of the most thoroughly studied elasmobranchs (Gilbert, 1978). Yet its behavior in the natural environment is largely unknown. Other than anecdotes, deductions from fishery records, and observations in captivity, we know relatively little about its routine daily activities. This is generally true for all sharks (Nelson, 1977). Most of the published information on diel activity patterns of sharks has come from the relatively few studies using ultrasonic telemetry (Sciarrotta and Nelson, 1977; Nelson and Johnson, 1980; Tricas et a1.,

1981; Klimley and Nelson, 1984; Yano and Tanaka, 1986; McKibben and Nelson, 1986; Scharold and Carey, 1986). This paper describes an initial telemetry-tracking study on the lemon shark and includes the longest continuous tracking segment (101 hand 202 km) of any tropical shark species. Analysis ofthese trackings provided insights into preferred habitats, areal requirements, diel changes in activity and space utilization, social interactions, and possible orientational cues. This study represents one phase of an overall program to describe the ecological energetics of the lemon shark. A preliminary report on the program as a whole is given in Gruber (1982a; 1984a). The other phases, including tag-recapture, I age and growth (Gruber and Stout, 1983; Brown and Gruber, 1988),respirometry (Bushnell, 1982),circadian rhythms,2 feeding (Cortes, 1987), and calorimetry (Wetherbee et aI., 1988). MATERIALS AND METHODS Study Sites. - The study was conducted primarily at Bimini, Bahamas, an island cluster located on the western edge of the Great Bahamas Bank approximately 100 km east of Miami, Florida. We chose the Bimini site because of its abundant shark fauna and diversity of marine habitats varying from semi-enclosed shallow flats bordered by mangroves, to open banks on the east, to current swept harbor channels, and to coral reefs sloping to the deep pelagic zone of the Florida current on the west. The primary study site was the semi-enclosed area of flats known as Bimini lagoon (Fig. I). The lagoonal site may be described as a shallow-water, sandy habitat whose substrate is stabilized by turtle and manatee grass (Thalassia testudinumand Syringodiumfiliforme). The benthic invertebrate fauna has been termed the Strombus costatus community (Newell et al., 1959). Detailed ecological descriptions of the biological, geological, and hydrological characteristics of the Bimini area are given by Newell and Imbrie (1955) and Voss and Voss (1960) and more recently by Jacobsen (1987). Depths over the lagoon flats range from a few centimeters to 1.8 m depending on tide and location. Much of the lagoon is exposed during low tides. Two ofthe trackings were made at other locations: Shark #2 was tracked near Burrows Cay, 12 km south of the SE piont of Grand Bahama Island. Shark #8 was tracked between Triumph reef and Hillsboro Inlet on the SE coast of Florida. Logistics and Capture Methods. - Tracking personnel were based aboard one of two oceanographic research vessels: the 65-foot R/V CALANUSor the 137-foot R/V CAPEFLORIDA.Shark fishing operations

I Henningsen, A. D. and S. H. Gruber. Estimates of natural production in the lemon shark, Negaprioll brew',osrris. by mark-recapture techniques. Manuscript completed, to be submitted to Trans. Am. Fish. Soc. 'Nixon, A. J. and S. H. Gruber. Diel metabolic and activity patterns of the lemon shark, Negap,;on b,eVlrosl,;s. Submitted to J. Exp.

Zoo!.

63

GRUBER ET AL.: ACTIVITY OF LEMON SHARKS

N

{ o o

..

CORAL

REEFS

-' .-'

EAST BIMINI

/ :®-····7j"?J.,

/~.~ ~

\

~:c~;--~-~ CD

\ \

,~~y /

q \,~ ....

// '....

CORAL REEFS

./-'

/ \--.

\

/

"

I I

\

-/-

GREAT BAHAMA BANK

-

.••...•.••...•

~ 1 km Figure I. Map of the Bimini study site showing the major features referred to in the text, including the observed overall activity spaces for sharks #1 (9 km2), #3 (93 km2), and #5 (18 km2). See Figure 3 for the complete polygon for shark #3. were conducted from smaller, outboard skiffs launched from the larger vessels. The actual trackings were usually conducted from an 18-foot inflatable boat powered by both an aircraft engine (Continental 90 hp) and an outboard motor (Evinrude 9.9 hp). We designed and fabricated this tracking craft to operate in the extremely shallow water of the flats where depth often precluded use of an outboard motor. Lemon sharks to be tracked were captured with baited hooks either on multiple-hook set lines or individual block rigs. The set lines consisted of a main line up to 1.5 km long, anchored at both ends. Branch lines with a single 10-0 stainless-steel hook were attached to the main line by metal snaps at 50-m intervals. The block rigs consisted of a concrete block to which a float, single hook, and line were attached. The block rigs were individually placed in channels while the set lines were fished along the borders oflarge flats. The gear was normally set at dusk and checked periodically throughout the night. Lemon sharks usually survived capture on both types of gear. Telemetry Equipment. - Ultrasonic transmitters used in this study were of the hybrid-circuit design similar to those described by Nelson (1978) and Nelson and McKibben (1981). Most of the transmitters

64

BULLETIN OF MARINE SCIENCE, VOL. 43, NO.1,

1988

Table 1. Summary of ultrasonic trackings of lemon sharks Days Distance con- Contact tracked (h) (km)* tact

No.

Date

Total length (em)

Sex

1.

June 79

150

F

3

17

24

East Bimini

shallow

2.

June 79

260

M

2

12

22

Burrows Cay

3.

230 180 168

F F F

8 2

113 6 19

202

5.

July 80 July 80 Aug 80

shallowdeepshallow shallow shallow shallow

6.

Aug 80

171

M

7. 8.

Oct 80 July 81t

178

M

9.

June 82

210

M

4.

4

3 3

7 60 14

39

13 156

Location

East Bimini East Bimini Bimini Harbor East Bimini Bimini Harbor East Bimini East Bimini Miami East Bimini

Depth

Remarks

transmitter self-ingested transmitter force fed

shallow shallow shallowdeepshallow shallow

speed sensor

speed sensor

'"Values represent a summation of the point·to-point position plots, not the linear distance. t Mature specimen, sex undetermined, estimated to be 240 em TL.

were simple pingers for location only, but two carried paddle-wheel-type sensors for telemetering instantaneous swimming speed. The transmitters were 3.2 em in outside diameter by 15.2 em in length with a crystal-controlled output frequency of 40 kHz, a pulse width of 10 ms, and pulse intervals in the range of800-1 ,200 ms. Transmitter life was about 10 days and under the best open-water conditions we measured ranges of 3 km. However in shallow water the range was reduced below I km and in extremely shallow water the range could drop below 100 m. Ultrasonic receivers utilized during the study included the Communications Associates, Inc. CR-40, Dukane N15A235A, and Burnett 512, the latter of which was occasionally used underwater by divers. In seven of the nine trackings the transmitter was attached firmly to the mid-line of the shark between the dorsal fins by two stainless-steel barbed darts (F1oy FH69). Transmitters for the remaining two sharks were stomach implanted, one by self ingestion in bait, the other by force feeding (Table I). Continuous trackings were conducted by two-man crews in shifts of about 6 h. We found that at least three two-men crews were necessary for effective round-the-clock tracking. Crew changeovers were done without interrupting the tracking by sending replacement personnel out from the research vessel in another small boat. Data Collection. -During tracking, positions were usually obtained at 15-min intervals. The tracking boat's position was fixed 1) by taking bearings from the boat with a high quality hand-bearing compass (Opticompass) on several landmarks including lighted buoys which we specifically placed on the flats and 2) by radar positioning of the tracking boat from the base research vessel. The shark's position relative to the tracking boat was estimated by signal bearing and amplitude. The areas (km') utilized by the sharks were determined from the individual plotted positions using the maximum-area polygon method (Sanderson, 1966). The areas of the maximum polygons were measured with a mechanical polar planimeter. Environmental Measurements. - Tidal currents (velocity and direction) were measured by fluorescein dye markers, neutral floats, and a Savonius rotor-type current meter. Salinity, temperature, and oxygen concentration were also determined at selected locations in the lagoon. Aerial Surveys. -Aerial surveys were conducted with an ultralight aircraft (Wizard J-3) on five occasions. Details of the aircraft and techniques are given in Gruber (l982b; 1984b). Typically, a compass course was flown over the lagoon at a speed of 35 km/h and altitude of 50-70 m. The shoreline of South Bimini lies in an east-west plane, and the pilot flew back and forth across the lagoon in a northsouth direction. With each crossing, the aircraft flew ever closer to the western limit of the lagoon. Individual surveys required about 45 min of flight time, during which the pilot kept a record of type of shark sighted and its location. If an interesting group of sharks was spotted during a transect, the pilot would descend, circle and photograph it with a 35 mm still camera or a video camera. Thus, observations of social behavior as well as abundance were recorded.


65

Figure 2. Observed activity spaces (maximum area polygons) for the first three days of tracking of sharks #1 (left), #3 (middle), and #5 (right). Note the day-to-day overlap indicating degree of site attachment.

RESULTS

Telemetry. -As shown in Table I, nine lemon sharks were tracked between June 1979 and June 1982. The longest track (shark #3) covered a total of 8 days including a continuous 10 I-h period from days 4-8. Two of the trackings included extensive deepwater excursions. Significantly, these sharks, #2 and #8, were the two largest specimens tracked, and both were mature. Activity Space. - The most thorough analysis of space utilization was done on shark #3 because we had the longest continuous period of contact during this track. The transmitter was fixed to the shark at 1020 h on 3 July 1980. It was tracked for about 12 h and then lost. The signal was reacquired within a few hundred meters of the capture locale 4 days later at 1400 h, then continuously tracked for 101 h. During this 4-day period the shark gradually shifted its center of activity eastward over the Great Bahama Bank into somewhat deeper waters to a maximum distance of 14 km east of Bimini (Figs. 2, 3). On the last day the shark appeared to have stopped its eastward movement and was beginning to head back into shallower water towards Bimini. Its final position when the signal was lost was within about 3 km of its original point of capture. Total Activity Space. - The total activity space for shark #3 observed over the 113 h of tracking amounted to 93 km2 (Fig. 3). The entire activity space encompassed a habitat of sand bottom with seagrass beds and water depth which ranged from 1.5-4 m. Although the shark had free access to the open ocean and coral reefs west of Bimini, at no time during 113 h of contact did it leave the lagoon and banks. By contrast, shark #5 (Figs. 1, 2), a smaller individual, spent essentially the entire tracking over a period of 4 days within the confines of the lagoon. It did enter the harbor but did not exit the pass to the open ocean, although it was directly at the mouth of the pass for a short time (one night) on the night of capture. The total activity space for this individual was 18 km2• The other Bimini trackings were less complete, but, nevertheless, gave no evidence that the sharks ever left the relatively shallow lagoon and bank habitat. Day-to-day Site Attachment. -All the Bimini sharks showed some degree of site attachment, i.e., diel repeatability or overlap of activity spaces. Sharks #1 and #5 showed a high degree of site attachment. They remained in essentially the same area during the day with their daytime centers of activity quite close. For

66

BULLETIN OF MARINE SCIENCE, VOL. 43, NO.1,

1988

N

o

DAY

•

NIGHT

"" 11

10

........

o

•.........."

\

9

8

••

\ I

\ I I

"0 8

1------1 1 km

I

'0

I

9

I

•

/

/

11

Figure 3. Observed activity space (overall maximum area polygon of the plotted positions) of shark #3, ultrasonically tagged on 3 July 1980 and tracked over an eight-day period. The open and closed circles represent the geometric centers of the plotted points (method of Lehner, 1979) for each day and night period of the continuous portion of the tracking (7, 8, 9, 10, and II July).

example, shark # 1 (Fig. 2) was tracked before we had the shallow-water capability of the airboat and was thus lost every night as it swam westward over the shallow flats. Yet, we easily found it the next morning for 3 consecutive days, in a search area of less than 2 km2• Shark #5, tracked both day and night, passed within 0.2 km of the same spot on 3 of the 4 days at 1800 h. The same pattern of diel repeatability may have occurred in the first half of the tracking of shark #3 because the space occupied on day 4 and the morning of day 5 was essentially the same as that of day 1 (signal was lost on days 2 and 3). Then on the afternoon of day 5, the activity pattern changed and for the next 3.5 days, the center of activity gradually shifted eastward about 3 km/day (Fig. 3). The total activity space on the final day of tracking did not overlap the areas occupied on days 1 and 4. Day-night Site Differences. - There was a general tendency for sharks during the day to be located eastward of their nighttime activity space. This is especially clear with shark #3. From a scatter plot of approximately 400 position points, we determined that the overall geometric center of the day points was farther east by about 3 km than the geometric center of the night points, even though this tendency was obscured by the general eastward shift of the daily activity spaces, during days 5-8 (Fig. 3). When the data were converted to histogram form (Fig. 4) and subjected to x2 analysis, results showed that the day-night distributions were significantly different from each other (X2 = 87.5, d.f. = 13, P < .001). This result is also seen in Figure 3, which shows that nearly all of the eastward shift occurred during the daylight hours, i.e., the daytime activity centers were always located well eastward of the activity centers of the previous night, whereas the following night-time activity centers were hardly eastward, if at all, relative to the previous daytime center.

GRUBER ET AL.: ACfIVITY

67

OF LEMON SHARKS

40 Ul

Z D

i

30

II:

III

Ul

ID D

...D

20

II: III

ID

:E:l 10 Z

Figure 4. Histogram of the east-west distribution of all 403 plotted positions of shark #3, collected over the 8-day tracking period. The lagoon is divided into a series of equal-area bins, seven to the east of the shark's overall activity center, and seven to the west as shown on the abscissa. The number of day and night position points in each bin is represented by the open (day) and closed (night) bars. There are more total daytime points because the summer day is longer than the night. The distribution shows that shark #3 was located relatively more easterly during the days and westerly during the nights.

Data from sharks #1 and #5, though more intermittent, also show the tendency to be located farther west at night than during the day. For example, shark #1 was always lost at night during a move westward over the lagoon flats. We tracked shark #5 completely over the flats at night and into the harbor abutting North Bimini, well to the west of the lagoon flats. The next morning this shark returned eastward over the flats to its original position. Rate of Movement vs. Time of Day. -Movements determined from the individual plotted points were analyzed in terms of (1) direction within eight points of the compass and (2) rates of movement, i.e., distance between successive 15min positions divided by time to give a value in km/h. Table 2 shows the composite data for diel rates-of-movement for shark #3. The mean rate was higher at night than during the day, with the highest rates occurring at evening and morning twilights. However, the rate-of-movement data were so variable that a t-test of the differences between the four periods showed no statistical significance. Instantaneous swimming speeds were telemetered from sharks #7 and #9 (Table

Table 2. Comparison of measures of field activity of lemon sharks Rate of movement (Point-to-point;

Shark 3 Day Eve. twilight Night Mom. twilight Shark 7 Shark 9

(overall) (overall) (overall)

1.78 2.50 1.97 2.00 1.89 (0.23 blls) 1.85 (0.29 bl/s) 1.26 (0.17 bl/s)

km/h)

Swimming speed (Sensor; km/h)

2.66 (0.42 bl/s) 2.50 (0.33 bl/s)

68

BULLETIN OF MARING SCIENCE, VOL. 43, NO.1,

EASTERN

DAYLIGHT STANDARD

1988

TIME

02:45

20:45

08:45

20:00 SUNSET

Figure 5, Diel-phase diagram of the relation between direction-of-movement and time-of-day for the final 5 days of continuous tracking of shark #3. Columns of numbers in each sector represent the net easterly or westerly movement, in meters, within each 3-h segment of the diel cycle. Around sunset the previous easterly direction reversed to westerly. The direction again switched near sunrise. This activity pattern suggests that the shark may have used the sun as an orientational cue.

2). Telemetered swimming speeds would be higher than the rates of movement except in cases where the shark swam in a straight line between two of the 15min position points, and, as expected, telemetered speeds were up to two times faster than their corresponding rates of movement (Table 2). For example, the overall rate-of-movement of shark #9 over 14-h, based on 27 pairs of positionpoints was 1.26 ± 0.11 SD km/h. The corresponding instantaneous speed averaged over 55 observations was 2.50 ± 0.05 SD km/h (0.33 body lengths per second). This demonstrates that the shark was not swimming in a straight line. Orientation of Movements. -Figure 5 shows the relation between direction of movement and time of day (divided into eight 3-h sectors) for the continuous portion of the track of shark #3. The most obvious feature of this chart is that the major easterly-oriented movement commences with the sector containing

GRUBER ET AL.: ACfIVITY OF LEMON SHARKS

69

Figure 6. Aerial photographs of inter- and intraspecific social activity of lemon sharks in Bimini lagoon: A, Three sharks in a Circle Formation; B, Milling group of 11 sharks; C, Two large sharks closely associated with a group of about 10 carangid Uack) fishes; D, Three sharks in a straight-line Follow Formation.

morning twilight and sunrise, whereas the net westerly movement begins with the sector containing sunset and evening twilight. The strongest and most consistent tendency for directed orientation was in the sunrise sector when, on all 4 days, the shark showed a concerted easterly movement. As mentioned, sharks # I and #5 showed similar patterns of orientation. For example, on the single track when shark #5 was followed from the late afternoon through sunset until the early morning hours, it began a concerted westerly move at evening twilight (1945 h). In addition, on the previous day, this shark was heading westward at 2200 h, just before the signal was lost. Finally, sharks #5 and #6 were captured at the western edge of the lagoon, in the deep channel of the harbor early on the morning (0415 h) ofthe 18th of August. The implication is that these sharks had moved westward over the flats at night, were captured, released and then swam eastward at sunrise. Other Behavioral Observations. - In addition to the telemetry findings, a number of direct observations were made on lemon sharks both during the trackings and at other times, such as during aerial surveys and tag-recapture operations. Observations were also made from boats and underwater. Interspecific Associations. -On several occasions, both from the tracking boat and from aerial and underwater observations, lemon sharks were seen in association with other elasmobranchs and teleosts. For example, during tracking #3 the shark was seen close to or among schools of jacks (Carangidae) on several occasions. At one point on day 8, two trackers entered the water with an ultrasonic receiver and located shark #3 at three different times within a I-h period. Each time, shark #3 was observed to be in 3 m of water over grass patches amidst a

70

BULLETIN OF MARINE SCIENCE, VOL. 43, NO. I, 1988

large school of fishes, mainly jacks (Caranx spp.), but also including barracuda (Sphyraena barracuda) and at least two nurse sharks (Ginglymostoma cirratum). Shark-jack associations were also recorded with shark #5 and during aerial observations (Fig. 6A). Other interspecific associations included apparently social interactions between lemon and nurse sharks, as well as lemon sharks and southern stingrays (Dasyatis americana). In both cases the lemon sharks closely followed the other species matching its heading and speed for the entire time the two animals were in the observer's visual range. Neither animal of the pair appeared to be alarmed and swimming was maintained at a routine to slow rate. Remoras, Echeneis naucrates, were frequently associated with lemon sharks larger than about 100 cm (TL), Intraspecific Associations.-Lemon sharks were frequently observed in groups of two or more individuals both from the tracking boat and from aerial surveys. Indirect evidence from telemetry was gathered on two occasions when two sharks were tracked simultaneously. The best evidence for social interactions was from the aerial observations. Aggregations of sharks were seen more frequently than individuals. We observed milling groups of up to 12 individuals (Fig. 6B) apparently orienting to one another in a way similar to that reported by McKibben and Nelson (1986) for another shark species. Social behaviors similar to those of bonnethead sharks, Sphyrna tiburo, (Myrberg and Gruber, 1974), were frequently observed from the ultralight aircraft, For example, follow formations (Fig. 6C) involving up to nine individuals were observed several times. Circles involving two or more lemon sharks were also recorded (Fig. 60). Tag-recapture.-During the 1981-1987 period, 332 lemon sharks were tagged and released in Bimini lagoon. 1 Of these, 119 were recaptured after periods up to 1,068 days. Some of these sharks were recaptured in exactly the same location as released up to 1.5 years before. Only a single tagged specimen was reported from any locale other than Bimini lagoon-a shark recaptured at Cat Cay, about 14 km south of Bimini. DISCUSSION

Evidence from the trackings of this study suggest that the lemon sharks occupied, day-after-day, a relatively restricted activity space, thus showing a home-ranging pattern. Shark #3, a mature female, occupied an area of 93 km2 during the 113 h tracked, even though it had direct access to vast areas of potential habitat. In contrast, shark #5, a juvenile female, spent essentially the entire 19 h of contact in an area of 18 km2 within the confines of the lagoon. The difference between the areal data from these two individuals might have been because shark #5 was tracked more intermittently over the 4 days, and may have moved beyond the observed area during those times when contact was lost. However, we believe that shark #5 did not leave the lagoon and that differences in activity spaces of these two individuals were related to the shark's ontogenetic stages. As a working hypothesis we suggest that the space requirement of a lemon shark, and its resultant home-range, increases as it ages. Evidence supporting this hypothesis comes from aerial and other visual observations, systematic fishing, mark and recapture and to a lesser extent, ultrasonic tracking. From these activities, we gained the impression that Bimini Lagoon is partitioned into habitats occupied by different age-groups of lemon sharks. For example, the newborn and youngest specimens are typically found in the northern sound and in two other


71

restricted areas heavily fringed by living mangroves. In more than 100 h of observation and shark collections from an airboat, we never saw a lemon shark larger than 117 cm TL in the sound although we captured (by dipnet) more than 100 specimens, mostly smaller than 80 cm TL. In contrast, we never captured a single lemon shark from the airboat smaller than 137 cm TL in the main lagoon. Our longline fishing gave similar results: all but two larger specimens (including mature males and pregnant females) came from lines set in the lagoon between East and South Bimini, while both small (ca. 80 cm TL) and large lemon sharks were caught in Bonefish Hole. We also captured mature specimens greater than 240 cm TL on the reef at Great Isaac Rock about 38 km north of Bimini and during this study captured and tracked mature specimens on or near the open water of coral reefs at Burrows Cay, Bahamas and Triumph Reef, SE Florida. We also collected adult lemon sharks to depths of 50 m off Miami, Florida. Thus, adults are often found in deeper waters off reefs and probably undergo long migrations, while the juveniles are strongly site-attached to flats and shallow passes near mangrove islands. Most of our recaptured juvenile lemon sharks (nearly 200 specimens from Bimini and the Florida Keys) were caught within 2 km of the original capture site. Only a single recapture was ever recorded from a locale distant from Bimini, i.e., at Cat Cay 14 km south of Bimini. In contrast, of the few tiger sharks, Galeocerdo cuvier, which we tagged at Bimini, at least two were subsequently recaptured hundreds of kilometers away from the tagging site (Casey, pers. comm.). These facts, therefore, lead us to believe that Bimini lagoon is divided up into a nursery zone characterized by shallow water and mangrove fringes, a zone occupied by juveniles of 4-10 years and a larger area for subadults and mature sharks. We also suggest that as lemon sharks age, they select habitats of ever larger area until maturity is reached. Thereafter they spend much time on the reef and possibly undergo long migrations. This hypothesis is being tested using an array of data-logging, bottom-mounted, ultrasonic monitors placed in various locations throughout Bimini lagoon. Sharks of different age-groups fitted with long-life, coded transmitters are being automatically tracked and their preferred habitats confirmed (McKibben and Nelson, 1981; Gruber et al., 1986). Space utilization by an animal can be examined in ways other than measuring an area of occupation. Once the activity space is defined, it can then be considered in terms of two behavioral continua: site defense and site fixity. We consider site defense to be a behavioral continuum which spans between an exclusive, defended, area of occupation (i.e., territoriality) and a completely undefended activity space. To demonstrate territoriality one must show that an individual (or group) has exclusive use of some space, and one must also observe defense of that area (Drickamer and Vessey, 1982). While this study was not designed to demonstrate territoriality, on numerous occasions we observed aggregations of lemon sharks both from the air and from boats. In addition, on several occasions we tracked two independently transmitting sharks simultaneously. No overt aggression or display was ever observed during either aerial or boating observations or during tracking. Because of this we believe that lemon sharks of this study do not hold or defend exclusive territories. Hence, while there is some evidence for site-related dominance in some sharks (Nelson et al., 1986), true territorial behavior in sharks has not been demonstrated and needs further investigation. The second facet of activity space, site fixity, is a behavioral continuum between nomadic and home-ranging life styles. According to Drickamer and Vessey (1982),

72

BULLETIN OF MARINE SCIENCE, VOL. 43, NO.1. 1988

animals which habitually use an area and spend most of their time there are said to have a home range, which may also be a territory. The lemon sharks that were tracked during this study, while not demonstrating territorial behavior, appeared to be relatively site-attached (Gruber, 1982a). For example, shark # I remained in essentially the same area during the day for 3 days and shark #5 remained in the same area for 4 days. Even shark #3 appeared to remain in the same area for the first few days of tracking, until day 6 when it slowly meandered eastward. On day 8 it began a concerted westward movement back towards Bimini and its final reported position was within 3 km of the original position. During aerial surveys we regularly observed numbers of sharks during the day at two specific sites in Bimini lagoon. Our final piece of evidence supporting sitefixity is that recaptured sharks tagged up to 1,068 days priorI were usually caught within 1 or 2 km of the tagging site. As noted, only a single recapture was reported from a locale other than Bimini lagoon. This lemon shark was recaptured approximately 14 km south of Bimini. Therefore, we conclude that the younger lemon sharks of this study are relatively site-attached. Evidence of the regular retum to daytime core areas was demonstrated by the lemon sharks tracked during this study. Shark #1 was found in the same 2 km2 area for three consecutive mornings after having been lost the night before when the shark moved into water too shallow for the tracking craft to follow. Shark #5 passed within 0.2 km of the same spot at the same time of day for 3 of the 4 days that it was tracked. Even shark #3 occupied the same area on days I, 4, and 5 (the signal was lost on days 2 and 3) before it began a gradual eastward journey for 3.5 days. The lemon sharks tracked during the present study did not passively drift with the tide (Gruber, 1982a). Figure 5 shows that the major easterly movement of shark #3 commences with the sector containing morning twilight and sunrise, while the major westerly movement begins with the sector containing evening twilight and sunset. Sharks #1 and #5 oriented in a similar way. In no case did the direction of movement coincide with the tidal currents. The lemon sharks we tracked apparently moved eastward at sunrise and westward at sunset. Many of the individual position plots showed that at mid-day, when the sun was nearly overhead, sharks remained in one general area and meandered without making significant progress in any particular direction. One possibility is that these sharks were "following the sun" without time compensation. Another is that true, timecompensated, sun-compass orientation, was being used. Sun compass orientations have been demonstrated in many other animals, including fishes (Hasler, 1966; Winn et aI., 1964). At Bimini, the conditions are appropriate (calm, shallow water) for lemon sharks to use the sun as a cue, but verification of this must await specific experiments. Gruber (1982a) suggested that lemon sharks in Bimini are crepuscular, although laboratory studies of activity and respiration show them to be more nocturnal. As shown in Table 2, the highest rates of movement were recorded at evening and morning twilight. These data, as well as the use of the sun as an orientational cue by these animals suggests that lemon sharks are perhaps crepuscular (Gruber, 1982a). Additional information is needed to confirm this hypothesis. However, the feeding behavior of juvenile lemon sharks did not conform to any diel cycle (Cortes, 1987). The measurement of diel activity rates is critical to assessing the cost of locomotion. Metabolic expenditures above the standard metabolic rate define the cost of activity. One of the primary objectives of this study was to obtain measures of activity in free-swimming lemon sharks, and to compare those values with


73

laboratory activity rates oflemon sharks swimming in tanks and in a respirometer. Table 2 shows that the rates-of-movement of sharks #7 and #9 were about half the actual swimming speeds. Obviously these sharks were not moving in straight lines between successive IS-min position plots. Bushnell (1982) reported that the routine activity for juvenile lemon sharks swimming in a respirometer is 0.4 body lengthslsecond (bI/s). This swimming rate was often maintained for 3 to 4 h in the respirometer without a resulting oxygen debt. Bushnell (1982) then determined the least-cost velocity for the lemon shark by calculating caloric requirements for a 1 kg shark to swim 1 km at various speeds. The calculated value of 1.2 bI/s is very close to the theoretical value of 1.3 bI/s for a "typical" pelagic, estuarine fish (Wakeman and Wohschlag, 1982). However, shark #9 in our study swam unrestricted at a speed 3.S times slower on the average (2.50 kmlh = 0.33 bI/s). This unrestricted field activity oflemon shark #9 corresponds quite closely with activity rates in an annular respirometer as reported by Bushnell (1982-0.40 bI/s routine) and Nixon and Gruber.s Weihs (1977) predicted the voluntary swimming speeds of aquatic organisms based on theoretical considerations of swimming speed, total length, and routine metabolism, and his predictions match our findings. Solving the formula given by Weihs (1977) for calculating speed for our 210 cm TL lemon shark #9 yields a theoretical speed of 0.693 m/s. Our swimming-speed telemetry data averaged 0.69 mls (=0.33 bI/s)! Weihs et al. (1981) confirmed these findings by reporting speeds of 0.66 mls for large sharks held in captivity. Medved and Marshall (1983) reported that the swimming speed of sandbar sharks, Carcharhinus plumbeus, was slightly higher than the Weihs prediction. Thus it seems reasonable to conclude from both theoretical, laboratory, and field studies that the routine activity of the lemon shark is 0.3-0.4 bI/s. This value has important implications for the energy budget oflemon sharks and is discussed in detail in Gruber (1984a). Other Behavioral Observations. - Visual observations made on numerous occasions provided an indication of intra- and interspecific associations between lemon sharks and other fishes. As mentioned, lemon sharks did not exhibit any type of intraspecific aggression or territoriality. On the contrary, they appeared to be quite social. We frequently observed lemon sharks in groups oftwo or more individuals during tracking operations, aerial or boat surveys. Although the telemetry offered indirect evidence, i.e., when two sharks were tracked simultaneously, the best observations of social interactions were made from the air. Groups of sharks were seen more frequently than lone individuals, and clusters of up to 12 individuals were seen apparently orienting to one another. Grouping in lemon sharks has been reported previously (Springer, 1950), based on fishery catch records. Myrberg and Gruber (1974) described 18 postures and movement patterns (half of which had social relevance) for bonnethead sharks, S. tiburo, in a semi-natural enclosure. During the present study we observed social behaviors by lemon sharks very similar to those of the bonnetheads. For example, we photographed "Follow Formations" involving up to nine individuals and "Circlings" of up to four or more sharks. It appeared as if these lemon sharks were orienting to one another, rather than aggregating as a result of some other environmental stimulus. From these unsystematic observations we gained the impression that lemon sharks are more social than had been previously suspected. On several occasions, both during tracking operations and aerial surveys, lemon sharks were seen in association with other elasmobranchs, such as southern stingrays and nurse sharks. As described earlier, various teleosts such as remoras, E. naucrates, barracuda, S. barracuda, and large schools of jacks (Caranx spp.) were

74

BULLETIN OF MARINE SCIENCE, VOL. 43, NO. I, 1988

also associated with the lemon sharks. Such associations are frequently reported in the literature, although the exact type of symbiotic relationship has not been fully demonstrated. On five occasions during three different trackings we observed lemon sharks swimming with large schools of blue runner, Caranx chrysos, and other jacks. In each case, the shark and jacks appeared to be orienting to each other (Gruber, 1982a). Our observations, together with those reported by other workers, have led us to the following hypothesis: Lemon sharks benefit from their association with carangids by making use of the jack's expanded sensory-motor apparatus (Gruber, 1982a), as well as their propensity to clean their hosts (Nelson and Johnson, 1980). Jacks, on the other hand, gain protection from their shark hosts, as well as a scratching surface (Eibl-Eibesfeldt, 1970; McKibben and Nelson, 1986) and, perhaps, a hydrodynamic advantage. Hence, because both the lemon sharks and the jacks appear to benefit, it may be that the lemon shark/jack association that we observed in Bimini is a mutualistic relationship. ACKNOWLEDGMENTS This material is based upon work supported by the National Science Foundation under grant OCE 8743949 (to SHG), and partially funded by Earthwatch and its research corps (to JFM). We thank the government of the Commonwealth of the Bahamas and especially C Higgs, Bahamas Ministry of Agriculture and Fisheries, for facilitating this research. The authors thank their corporate supporters for providing products such as skiffs (Aquasport Mfg. Co.), motors (Johnson Outboard Motors), aircraft (US Soaring), standby power (Honda Generators) 8 mm video (Sony Corp.), tetracycline (Pfiser Drug Co.), diving equipment (Mares and Cressi), lubricants (Amsoil Corp.), oxygen and liquid nitrogen (Miami Welding Co.) and specialized underwater apparatus (Gary Belcher Co.). We gratefully acknowledge the participation of Capt. D. Kipnis who spent days on site tracking sharks at Bimini and Capt. R. Schatman who provided us with living sharks to track. We thank J. Fraga for the fine artwork. We also acknowledge the many volunteers and students too numerous to mention by name, but without whom this field study and its offshoots would not have been possible. Finally we express our gratitude to J. N. McKibben whose creative insight, technical skill and long hours at the workbench produced much ofthe electronic gadgetry that we used in this study. This paper is dedicated to the memory of Rev. W. Duncombe, better known as Bonefish Willie. Rev. Duncombe probably knew more about the Bimini flats and creatures thereon than any human, and he freely shared his knowledge with us. We believe that without his help and direct input, this study could not have been accomplished. Thank you Bonefish Willie ... we all miss you very much!

LITERATURE CITED Brett, J. R. and T. D. D. Groves. 1979. Physiological energetics. Pages 279-352 in W. S. Hoar, D. J. Randall and J. R. Brett, eds. Fish physiology. Academic Press, New York. Brown, C A. and S. H. Gruber. 1988. Age assessment of the lemon shark, Negaprion brevirostris, using tetracycline validated vertebral centra. Copeia 1988: 747-783. Bushnell, P. G. 1982. Respiratory and circulatory adjustments to exercise in the lemon shark, Negaprion brevirostris (Poey). M.S. Thesis, University of Miami, Miami, FL. 90 pp. Carey, F. C, J. W. Kanwisher, O. Brazier, G. Gabrielson, J. G. Casey and H. L. Pratt, Jr. 1982. Temperature and activity of a white shark, Carcharodon carcharias. Copeia 1982: 254-260. Cortes, E. 1987. Diet, feeding habits, and daily ration of young lemon sharks, Negaprion brevirostris. and the effect of ration size on their growth and conversion efficiency. M.S. Thesis, University of Miami, Miami, FL. 145 pp. Davis, G. and C Warren. 1971. Estimation of food consumption rate. Pages 215-228 in W. Ricker, ed. Methods for assessment offish production in fresh waters. IBP Handbook No.3, 2nd edition, Blackwell Scientific Pub!., London. Diana, J. S. 1980. Diel activity pattern and swimming speeds of northern pike, (Esox lutris) in Lac Ste. Anne, Alberta. Can. J. Fish. Aquat. Sci. 37: 1454-1458. --, W. C MacKay and M. Ehrman. 1977. Movements and habitat preference of Northern Pike (Esox lutris) in Lac Ste. Anne, Alberta. Trans. Am. Fish. Soc. 106: 560-565.


75

Drickamer, L. C. and S. H. Vessey. 1982. Animal behavior-concepts, processes, and methods. Willard Grant Press, Boston. 510 pp. Eibl-Eibesfeldt, I. 1970. Ethology, the biology of behavior. Holt, Reinhart and Winston Inc., New York. 535 pp. Gilbert, P. W. 1978. Sharks in perspective. Pages 1-10 in N. E. Hodgson and R. Mathewson, eds. Sensory biology of sharks, skates, and rays. U.S. Government Printing Office, Washington. D.C. 690 pp. Grodzinski, W~ 1975. Energy flow through a vertebrate population. Pages 65-94 in Methods for ecological bioenergetics. lBP Handbook. No. 24. Blackwell Scientific, London. Gruber, S. H. 1982a. Role of the lemon shark, Negaprion brevirostris (Poey), as a predator in the tropical marine environment: a multidisciplinary study. Fla. Sci. 45: 46-75. 1982. --. 1982b. Shark research by ultralight. Ultralight Aircraft 2(6): 38-41. ---. 1984a. Bioenergetics of the captive and free ranging lemon shark. AAZPA Annual Proceedings 3: 340-373. --. 1984b. Sharks: research by ultralight II. Ultralight Aircraft 4(2): 35-41. --and R. G. Stout. 1983. Biological materials for the study of age and growth in a tropical elasmobranch, the lemon shark, Negaprion brevirostris (Poey). NOAA Tech. Rept., NMFS Circ. 8: 193-205. ---, D. R. Nelson and J. N. McKibben. 1986. Tracking sharks in Bimini lagoon: one phase of a bioenergetic study. Newsletter of the Int. Assoc. Fish. Ethologists 9(1): 5-8. Hasler, A. P. 1966. Underwater guideposts: homing of salmon. University of Wisconsin Press, Madison. 155 pp. Jacobsen, T. 1987. An ecosystem-level study ofa shallow, subtropical, marine lagoon, North Sound, Bimini, Bahamas. Ph.D. Thesis, University of Georgia. 287 pp. Klimley, A. P. and D. R. Nelson. 1984. Diel movement patterns of the scalloped hammerhead shark (Sphyrna /ewim) in relation to EI Bajo Espiritu Santo: a refuging central-position social system. Behav. Ecol. Sociobiol. 15: 45-54. Lehner, P. N. 1979. Handbook of ethological methods. Garland STM Press, New York. 403 pp. McKibben, J. N. and D. R. Nelson. 1981. A portable, real-time, X-Y plotting system for ultrasonic tracking of fish. Pages 105-115 in F. M. Long, ed. Proceedings of the Third International Conference on Wildlife Biotelemetry. University of Wyoming, Laramie. --and ---. 1986. Patterns of movement and groupings of gray reef sharks, Carcharhinus amb/yrhynchos. at Eniwetak, Marshall Islands. Bull. Mar. Sci. 38: 89-110. Medved, R. J. and J. A. Marshall. 1983. Short-term movements of young sandbar sharks, Carcharhinus p/umbeus (Pisces, Carcharhinidae). Bull. Mar. Sci. 33: 87-93. Myrberg, A. A. and S. H. Gruber. 1974. The behavior of the bonnethead shark Sphyrna tiburo. Copeia 1974: 358-374. Nelson, D. R. 1977. On the field study of shark behavior. Amer. Zool. 17: 501-508. ---. 1978. Telemetering techniques for the study of free ranging sharks. Pages 419-482 in N. Hodgson and R. Mathewson, eds. Sensory biology of sharks, skates, and rays. U.S. Government Printing Office, Washington, D.C. 690 pp. --and R. H. Johnson. 1980. Behavior of the reef sharks of Rangiroa, French Polynesia. Nat!. Geogr. Soc. Res. Reports 12: 479-499. --and 1. N. McKibben. 1981. Timed-release, recoverable, ultrasonic/radio transmitters for tracking pelagic sharks. Pages 90-104 in F. M. Long, ed. Proceedings of the Third International Conference on Wildlife Biotelemetry. University of Wyoming, Laramie. --, R. R. Johnson, J. N. McKibben and G. G. Pittenger. 1986. Agonistic attacks on divers and submersibles by gray reef sharks, Carcharhinus amb/yrhynchos: anti-predatory or competitive? Bull. Mar. Sci. 38: 68-88. Newell, N. D. and J. Imbrie. 1955. Biogeological reconnaissance in the Bimini area, Great Bahama Bank. Trans. N.Y. Acad. Sci., Ser. II 18(1): 3-14. ---, ---, E. G. Purdy and D. L. Thurber. 1959. Organism communities and the bottom facies, Great Bahama Bank. Bull. Am. Mus. Nat. Hist. 117(4): 177-228. Priede, I. and A. H. Young. 1977. The ultrasonic telemetry of cardiac rhythms of wild brown trout (Sa/mo trutta L.) as an indicator of bioenergetics and behavior. J. Fish. BioI. 10: 299-318. Sanderson, G. C. 1966. The study of mammal movements-a review. J. Wildl. Manag. 30: 215235. Scharold, J. V. and F. C. Carey. 1986. Behavior of free swimming blue sharks: depth and speed. Published abstracts, 2nd annual meeting AES, Victoria, B.C., Canada. Sciarrotta, T. C. and D. R. Nelson. 1977. Diel behavior of the blue shark, Prionace g/auca, near Santa Catalina Island, California. U.S. Fish Wildl. Fish. Bull. 75: 519-528. Springer, S. 1950. Natural history notes on the lemon shark, Negaprion brevirostris. Tex. 1. Sci. 3: 349-359.

76

BULLETIN OFMARINESCIENCE, VOL.43, NO.1, 1988

Tricas, T., L. R. Taylor and G. Naftel. 1981. Diel behavior of the tiger shark, Galeocerdo cuvier, at French Frigate Shoals, Hawaiian Islands. Copeia 1981: 904-908. Voss, G. L. and N. A. Voss. 1960. An ecological survey of the marine invertebrates of Bimini, Bahamas, with a consideration of their geographical relationships. Bull. Mar. Sci. Gulf Carib. 10: 96-] 16. Wakeman, J. M. and D. E. Wohschlag. 1982. Least-cost swimming speed and transportation costs in some pelagic estuarine fishes. Fish. Res. 1(1981/82): 117-127. Weihs, D. 1977. Effects of size on sustained swimming speeds of aquatic organisms. Pages 333-338 in T. J. Pedley, ed. Scale effects in animal locomotion. Academic Press, New York. ---, R. S. Keyes and D. M. Stalls. 1981. Voluntary swimming speeds of two species of large carcharhinid sharks. Copeia 1981: 219-222. Wetherbee, B. J., S. H. Gruber and A. L. Ramsey. 1988. X-Radiographic observations of food passage through the digestive tract of the lemon shark. Trans. Am. Fish. Soc. 116: 763-767. Winn, H. E., M. Salmon and N. Roberts. 1964. Sun-orientation by parrot fishes. Z. Fur. Tierpsych. 21: 798-812. Yano, K. and S. Tanaka. 1986. A telemetric study on the movements of the deep sea squaloid shark, Centrophorus acus. Pages 372-380 in T. Uyeno, R. Arai, T. Taniuchi, and K. Matsuura, eds. Indo-Pacific fish biology. The ichthyological society of Japan, Tokyo. DATEACCEPTED: February 17, 1988. ADDRESSES: (S.H.G. and J.F.M.) Division of Biology and Living Resources, Rosenstiel School of Marine and Atmospheric Science, University of Miami, Miami, Florida, 33149; (D.R.N.) Department of Biology, California State University, Long Beach, California, 90840.